IJSPT April 2020 by SPTS

IJSPT VOL 15, ISSUE 2 APRIL 2020

An Official Publication of

INTERNATIONAL JOURNAL OF SPORTS PHYSICAL THERAPY

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IJSPT

INTERNATIONAL JOURNAL OF SPORTS PHYSICAL THERAPY

Editor in Chief Michael L. Voight, PT, DHSc, OCS, SCS, ATC, CSCS Belmont University Nashville, Tennessee – USA

Associate Editors: John Dewitt PT, DPT, SCS, ATC The Ohio State University Sports Medicine Columbus, Ohio - USA

Senior Associate Editor Barbara Hoogenboom, PT, EdD, SCS, ATC Grand Valley State University Grand Rapids, Michigan - USA

Terry Grindstaff PhD, PT, ATC Creighton University Omaha, Nebraska - USA

Associate Editor, Manuscript Coordinator Ashley Campbell, PT, DPT, SCS, CSCS Nashville Hip Institute Nashville, Tennessee – USA Associate Editor, Thematic Issues Robert Manske, PT, DPT, Med, SCS, ATC, CSCS Wichita State University Wichita, Kansas – USA Associate Review Editor Phil Page, PT, PhD, ATC, CSCS Performance Health Baton Rouge, Louisiana—USA

International Associate Editors: Colin Paterson, University of Brighton Brighton, England —United Kingdom Anthony G. Schneiders, PT, PhD Central Queensland University Bundaberg, Queensland – Australia Kristian Thorborg, PT, PhD Copenhagen University Hospital Hvidovre Hvidovre—Denmark

Editorial Board: Scott Anderson, PT, Dip Sport PT Alliance Health and Wellness Regina, Saskatchewan – Canada

Robert J. Butler, PT, DPT, PhD St. Louis Cardinals Jupiter, Florida – USA

Lindsay Becker, PT, DPT, SCS, CSCS Buckeye Performance Golf Columbus, Ohio – USA

Duane Button, PhD, CSEP-CEP Memorial University St. John’s, Newfoundland and Labrador – Canada

David Behm, PhD Memorial University of Newfoundland St. John’s, Newfoundland—Canada

Rick Clark, PT, DScPT, CCCE Tennessee State University Nashville, Tennessee – USA

Barton Bishop, PT, DPT, SCS, CSCS Sport and Spine Rehab of Rockville Rockville, Maryland – USA

George J. Davies, PT, DPT, SCS, ATC, FAPTA Armstrong Atlantic State University Savannah, Georgia – USA

Mario Bizzini, PT, MSc Schulthess Clinic Zürich – Switzerland

Todd S. Ellenbecker, DPT, SCS, OCS Physiotherapy Associates Scottsdale Sports Clinic Scottsdale, Arizona – USA

Turner A. “TAB” Blackburn, Jr., MEd, PT, ATC Clemson Sports Medicine and Rehabilitation Manchester, Georgia – USA

John A. Guido, Jr., PT, MHS, SCS, ATC, CSCS Ochsner Health Systems New Orleans, Louisiana – USA

Lori A Bolgla, PT, PhD, MAcc, ATC Augusta University Augusta, Georgia – USA

Walter L. Jenkins, PT, DHS, ATC Nazareth College Rochester, New York - USA

EDITORIAL STAFF & BOARD

Henning Langberg, PT, PhD, MSc Institute of Sports Medicine Copenhagen – Denmark

Timothy F. Tyler, PT, ATC NISMAT Lenox Hill Hospital New York, New York – USA

Daniel S. Lorenz, PT, DPT, ATC, CSCS Providence Medical Center Kansas City, Kansas - USA

Timothy Uhl, PT, PhD, ATC University of Kentucky Lexington, Kentucky – USA

Terry Malone, PT, EdD, ATC, FAPTA University of Kentucky Lexington, Kentucky – USA

Mark D. Weber, PT, PhD, SCS, ATC University of Mississippi Medical Center Jackson, Mississippi – USA

Charles E. Rainey, PT, DSc, DPT, MS, OCS, SCS, CSCS, FAAOMPT United States Public Health Service Springfield, Missouri - USA Michael P. Reiman, PT, DPT, OCS, SCS, ATC, FAAOMPT, CSCS Duke University School of Medicine Durham, North Carolina – USA Mark F. Reinking, PT, PhD, SCS, ATC Regis University Denver, Colorado – USA Kevin Robinson, PT, DSc, OCS Belmont University Nashville, Tennessee – USA Barbara Sanders, PT, PhD, SCS, FAPTA Texas State University-San Marcos San Marcos, Texas – USA Teresa L. Schuemann, PT, DPT, SCS, ATC, CSCS Colorado Physical Therapy Specialists Fort Collins, Colorado – USA Brandon Schmitt, PT, DPT, ATC PRO Sports Physical Therapy of Westchester Scarsdale, New York - USA Barry I. Shafer, PT, DPT, ATC Elite Motion Physical Therapy and Sports Medicine Pasadena, California - USA Laurie Stickler, MSPT, OCS Grand Valley State University Grand Rapids, Michigan – USA Amir Takla, PT, B.Physio, Mast.Physio (Musc). University of Melbourne Melbourne— Australia Steven R. Tippett, PT, PhD, SCS, ATC Bradley University Peoria, Illinois – USA

Statistical Consultant Patrick Sells, DA, ES Belmont University Nashville, Tennessee – USA

IJSPT

international JOURNAL OF SPORTS PHYSICAL THERAPY

I N T E R N AT I O N A L J O U R N A L OF SPORTS PHYSICAL THERAPY

AMERICAN ACADEMY OF SPORTS PHYSICAL THERAPY

Editorial Staff

Executive Committee

Michael L. Voight, PT, DHSc, OCS, SCS, ATC Editor-in-Chief

Walter L. Jenkins, PT, DHS, LATC, ATC President

Barbara Hoogenboom, PT, EdD, SCS, ATC Grand Valley State University Grand Rapids, Michigan - USA Senior Associate Editor

Blaise Williams, PT, PhD Vice President

Robert Manske, PT, DPT, Med, SCS, ATC, CSCS Wichita State University Wichita, Kansas – USA Associate Editor, Thematic Issues Phil Page, PT, PhD, ATC, CSCS Performance Health Baton Rouge, Louisiana—USA Associate Review Editor Associate Editors John Dewitt PT, DPT, SCS, ATC The Ohio State University Sports Medicine Columbus, Ohio - USA Terry Grindstaff PhD, PT, ATC Creighton University Omaha, Nebraska - USA International Associate Editors

Colin Paterson, University of Brighton Brighton, England —United Kingdom

Mitchell Rauh, PT, PhD, MPH, FACSM Secretary Jill Thein-Nissenbaum , PT, MPT, SCS, ATC, DSc Treasurer Erik Meira, PT, DPT, SCS, CSCS Representative-At-Large

Administration Mark S. De Carlo, PT, DPT, MHA, SCS, ATC Executive Director Mary Wilkinson Director of Marketing/Webmaster Managing Editor, Publications Jayme Little Director of Member Engagement

Contact Information P.O. Box 431 Zionsville, Indiana 46077 877.732.5009 Toll Free 317.669.8276 Fax www.spts.org

Anthony G. Schneiders, PT, PhD Central Queensland University Bundaberg, Queensland – Australia Kristian Thorborg, PT, PhD Copenhagen University Hospital Hvidovre Hvidovre—Denmark Ashley Campbell Associate Editor, Manuscript Coordinator Mary Wilkinson Managing Editor

Advertising Sales The International Journal of Sports Physical Therapy accepts advertising. Email Mary Wilkinson, Marketing Director, at mwilkinson@spts.org or contact by phone at 317.501.0805.

IJSPT is a bimonthly publication, with release dates in February, April, June, August, October and December. It is published by the American Academy of Sports Physical Therapy.

ISSN 2159-2896

I N T E R N AT I O N A L J O U R N A L OF SPORTS PHYSICAL THERAPY IJSPT is an official journal of the International Federation of Sports Physical Therapy (IFSPT).

TABLE OF CONTENTS VOLUME 15, NUMBER 2 Page

Article Title

SYSTEMATIC REVIEW/META-ANALYSIS 175 Effect of Aerobic Exercise Training With and Without Blood Flow Restriction on Aerobic Capacity in Healthy Young Adults: A Systematic Review with Meta-Analysis. Authors: Formiga MF, Fay R, Hutchinson S, Locandro N, Ceballos A, Lesh A, Buscheck J, Meanor J, Owens J, Cahalin LP ORIGINAL RESEARCH 188 Posterior Shoulder Tightness and Subacromial Impingement Characteristics in Baseball Pitchers: A Blinded, Matched Control Study. Authors: Laudner K, Wong R, Latal J, Meister K 196

Changes in Infraspinatus and Lower Trapezius Activation in Volleyball Players Following Repetitive Serves. Authors: Khal KM, Moore SD, Pryor JL, Singh B

203

Test-Retest Reliability of the Closed Kinetic Chain Upper Extremity Stability Test (CKCUEST) in a Modified Test Position in Division I Collegiate Basketball Players. Authors: Hollstadt K, Boland M, Mulligan I

210

Comparison of Cryotherapy Modality Application Over the Anterior Thigh Across Rugby Union Positions; A Crossover Randomized Controlled Trial. Authors: Alexander J, Rhodesa D, Birdsall D, Selfec J

221

Is Step Rate Associated with Running Injury Incidence? An Observational Study with 9-Month Follow Up. Authors: Szymanek EB, Miller EM, Weart AN, Morris JB, Goss DL

229

Comparative Analysis of Hip Muscle Activation During Closed-Chain Rehabilitation Exercises in Runners. Authors: Connelly CM, Moran MF, Grimes JK

238

Reliability and Validity of The Hip Abductor Isometric Endurance Test: A New Method to Assess the Endurance of the Hip Abductors. Authors: VanCant J, Detrembleur C, Mahaudens P, Feipel V

246

Eccentric Hamstring Strength is Associated with Age and Duration of Previous Season Hamstring Injury in Male Soccer Players. Authors: Vicens-Borgas J, Esteve E, Fort-Vanmeerhaeghe A, Clausen MB, Bandholm T, Opar D, Shield A, Thorborg K

254

Analysis of Timing of Secondary ACL Injury in Professional Athletes Does Not Support Game Timing or Season Timing as A Contributor To Injury Risk. Authors: Zhou J, Schilaty ND, Hewett TE, Bates NA

CASE SERIES / REPORTS 263 An Exploratory Case Series Analysis of the Use of Primal Reflex Release Techniqueâ&#x201E;˘ to Improve Signs and Symptoms of Hamstring Strain. Authors: Albertin ES, Walters M, May J, Baker RT, Nasypany A, Cheatham S 274

The Management of Plantar Fasciitis with a Musculoskeletal Ultrasound Imaging Guided Approach for Instrument Assisted Soft Tissue Mobilization in a Runner: A Case Report. Authors: Sillevis R, Shamus E, Mouttet B

CLINICAL COMMENTARY / SUGGESTION 287 Rehabilitation Considerations for Spondylolysis in the Youth Athlete. Authors: Selhorst M, Allen M, McHugh R, MacDonald J 301

Past, Current and Future Interventional Orthobiologics Techniques and How They Relate to 3 Regenerative Rehabilitation: A Clinical Commentary. Authors: Centeno CJ, Pastoriza SM

326

Criteria-Based Return to Sprinting Progression Following Lower Extremity Injury. Authors: Lorenz D, Domzalski S

IJSPT

ORIGINAL RESEARCH

EFFECT OF AEROBIC EXERCISE TRAINING WITH AND WITHOUT BLOOD FLOW RESTRICTION ON AEROBIC CAPACITY IN HEALTHY YOUNG ADULTS: A SYSTEMATIC REVIEW WITH META-ANALYSIS Magno F. Formiga, PhD, PT1,2 Rebekah Fay, PT, DPT1 Savannah Hutchinson, PT, DPT1 Nicholas Locandro, PT, DPT1 Angel Ceballos, PT, DPT1 Alexandra Lesh, PT, DPT1 Joel Buscheck, PT, DPT1 Jacy Meanor, PT, DPT1 Johnny G. Owens, MPT3† Lawrence P. Cahalin, PhD, PT1

ABSTRACT Background: Exercise training (ET) with blood flow restriction (BFR) is becoming increasingly popular, but the majority of BFR ET studies have evaluated skeletal muscle strength and hypertrophy. The favorable effect of BFR ET on skeletal muscle and the vasculature appears to improve aerobic capacity (AC) although conflicting results have been observed. Purpose: The purposes of this systematic review with meta- analysis were to examine the effects of aerobic ET with and without BFR on AC and to compare the effect of low-to-moderate aerobic ET with and without BFR to high-intensity aerobic ET with and without BFR on AC. Study Design: Systematic Review with Meta-analysis. Methods: A comprehensive search for studies examining the effects of aerobic ET with and without BFR on AC was performed. Inclusion criteria were: (a) the study was conducted in healthy individuals, (b) there was random allocation of study participants to training and control groups, (c) BFR was the sole intervention difference between the groups. Results: A total of seven studies (5 low-to-moderate ET and 2 high-intensity ET) were included in the meta-analysis providing data from 121 subjects. There was a significant standardized mean difference (SMD) of 0.38 (95% CI = 0.01, 0.75) in AC between the BFR and non-BFR groups of all seven studies (z = 2.01; p = 0.04). Separate analyses of the five low-to-moderate aerobic ET studies found similar results with aerobic ET with BFR eliciting a significantly greater AC (z = 2.47; p=0.01) than aerobic ET without BFR (SMD of 0.57; 95% CI = 0.12, 1.01). Separate analyses of the two high-intensity aerobic ET studies with and without BFR found no significant difference in AC between the groups (SMD of - 0.01; 95% CI = - 0.67, 0.64). Conclusion: Aerobic ET with BFR elicits a significantly greater AC than aerobic ET without BFR in healthy young adults. However, low-to-moderate intensity aerobic ET with BFR elicited a greater improvement in AC than aerobic ET without BFR while highintensity aerobic ET with BFR did not elicit an improvement in AC over high-intensity aerobic ET without BFR. Level of Evidence: 1a Keywords: aerobic capacity, blood flow restriction, maximal oxygen consumption, meta-analysis, oxygen uptake, vascular occlusion training, VO2max.

Department of Physical Therapy, Miller School of Medicine, University of Miami, Coral Gables, FL, USA. 2 Departamento de Fisioterapia, Universidade Estadual da Paraíba, Campina Grande, PB, Brazil. 3 Owens Recovery Science, San Antonio, TX, USA. Conﬂict of interest: The authors declare no conﬂict of interest.

CORRESPONDING AUTHOR Lawrence P. Cahalin and Magno F. Formiga University of Miami Miller School of Medicine Department of Physical Therapy 5915 Ponce de Leon Boulevard, 5th Floor Coral Gables, FL 33146 Phone: 305-284-4535, Fax: 305-284-6128 E-mail: l.cahalin@miami.edu, magno@miami.edu

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 175 DOI: 10.26603/ijspt20200175

INTRODUCTION Exercise training (ET) with blood flow restriction (BFR) is becoming increasingly popular in rehabilitation, allowing skeletal muscle strengthening and hypertrophy to be accomplished using lower workloads, fewer repetitions, and shorter durations.1 These benefits have been seen across a variety of musculoskeletal conditions and age ranges. Furthermore, research on different cuff width, size, and pressure distribution has led to the development and implementation of more sophisticated cuffs for a safer and more precise reduction in blood flow to the exercising limb.2 While the majority of BFR ET studies have evaluated these effects on skeletal muscle strength and hypertrophy, the effects of BFR ET on aerobic capacity (AC) have also been studied, albeit on a smaller scale and with conflicting conclusions. Just as BFR with low-load resistance ET elicits a localized metabolic response similar to high-load resistance ET without BFR, it is reasonable to question whether BFR with aerobic ET may have superior cardiovascular effects compared to aerobic ET without BFR. Aerobic ET with BFR has the potential to improve AC due to improvements in components of the Fick equation [VO2 = HR x SV x (a-vO2 difference)] as well as several other factors including the effects of hypoxia on vascular endothelial growth factor (VEGF) during BFR and the increase in endothelium-dependent vasodilation from increased shear

stress and nitric oxide production during cuff release and reperfusion after BFR, as shown in Figure 1.3 Increased VEGF and endothelium-dependent vasodilation from BFR ET have the capacity to improve oxygen delivery and uptake, but may not have the same degree of improvement during high-intensity aerobic ET compared to low-to-moderate aerobic ET due to the possibility of a limited training duration and muscle damage associated with high-intensity aerobic ET with BFR.4,5 However, a recent systematic review on the effects of BFR ET on AC and exercise performance suggested that aerobic ET with BFR improved AC irrespective of training intensity.6 In view of these findings, the purposes of this systematic review with meta-analysis were to examine the effects of aerobic ET with and without BFR on AC and to compare the effect of low-to-moderate aerobic ET with and without BFR to high-intensity aerobic ET with and without BFR on AC hypothesizing that (a) AC would be greater with aerobic ET and BFR compared to aerobic ET without BFR and (b) AC would be greater during low-tomoderate intensity aerobic ET with BFR compared to high-intensity aerobic ET with BFR. METHODS Search strategy and inclusion criteria A comprehensive literature review was performed in PubMed and the Cochrane library through December

Figure 1. Potential mechanisms of action during and immediately post-blood ďŹ&#x201A;ow restricted exercise contributing to improvements in aerobic capacity. The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 176

2018. The search strategy was conducted in English and included a mix of terms for the key concepts Blood Flow Restriction, Maximal Oxygen Consumption, Oxygen Consumption, Oxygen Uptake, Aerobic Capacity, Exercise Training, and Exercise and these were later combined with an advanced search strategy (Appendix 1) to identify randomized controlled trials for inclusion purposes. The reference list of eligible studies was also screened to identify other potentially relevant publications. To be included in the systematic review and meta-analysis, a study had to meet the following criteria: (a) the study was conducted in healthy individuals of all ages (i.e. free of overt acute or chronic diseases), (b) there was random allocation of study participants to training and control groups, (c) BFR was applied during aerobic ET, (d) BFR was the sole intervention difference between the groups, and (e) direct measurement rather than estimated maximal oxygen consumption was reported for each group. Any studies not meeting these criteria were excluded. Disagreement related to eligibility of studies was resolved through discussions among all authors. To assist with the interpretation of results, all included studies were assessed for methodological

quality using the PEDro scale, which is comprised of 11 items to evaluate the risk of bias and statistical reporting of randomized control trials (Table 1). The first item in the scale relates to external validity and items 2-11 assess the internal validity of a trial. Each item in the scale was scored yes (1 point) or no (0 points). Since the first item is not included in the total PEDro score of an article, a maximum of 10 points was possible for each study with scores ranging from 0 to 10. Higher scores indicate greater methodological quality. Data extraction Two authors independently read and coded each study for descriptive information including: (a) publication year (b) source of publication (i.e. journal article or published theses) (c) gender (1 = only males; 2 = only females; 3 = mixed) and (d) age of the participants in the studies. For both BFR and standard training protocols, the mode of ET and ET intensity were coded (1 = walking/treadmill protocol, 2 = bicycle protocol and 1 = low-to-moderate intensity if ET intensity was < 80% of maximal capacity, 2 = high-intensity if ET intensity was â&#x2030;Ľ 80% of maximal capacity, respectively). Means and standard deviations of post-intervention maximal

Table 1. Methodological quality of the included studies assessed with the PEDro scale.

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 177

oxygen consumption were recorded as continuous variables in mL/kg/min. Means and standard deviations of post-intervention minute ventilation (VE) in L.min-1 and isometric knee extension strength in N/m were also recorded as continuous variables when available for supplementary pooled analyses carried out for discussion purposes. Inter-rater reliability of the coding by the two authors was calculated for all continuous and categorical variables. Cohen’s Kappa determined that the raters were in complete agreement (k = 1). Pearson correlation analysis also demonstrated complete consistency among coders (r = 1). Data analysis Hedge’s g was computed for each study using the metafor package with the statistical software R (3.0.2 version), providing an unbiased estimate of the population standardized mean difference. The overall effect was computed from effect sizes extracted from the individual studies, each of which was weighted by its inverse of the associated variance. Review Manager (RevMan, 5.3 version) was also used for data analyses to measure the standardized mean difference and I2. Heterogeneity of effect sizes was examined using the Q statistic, a standardized measure of the total amount of variation observed across studies. A nonsignificant Q statistic indicated that a fixed-effects model, rather than a random-effects model, was preferred for the analysis. Subgroup analyses were carried out based on ET intensity. Statistical significance was set at a p-value < 0.05. Risk of publication bias could not be assessed because of the low number of included studies. As a rule of thumb, publication bias assessment can only be performed when there are at least 10 studies entered in the meta-analysis. RESULTS Selected studies A total of seven trials were identified as eligible.7-13 A flow diagram of the studies retrieved for the metaanalysis is presented in Figure 2, as per PRISMA reporting guidelines. The studies were all randomized controlled trials with a BFR ET group and an ET control group with no vascular occlusion. The included studies evaluated a total of 121 subjects

from both genders (79.3% men), with a mean sample size of 17.3 (SD = 2.7). The age across studies ranged from 20-25 years (combined mean ± SD age = 23.5 ± 4.1). The methodological quality of the studies using the PEDro scale was moderate with all studies scoring 6 of 10, as shown in Table 1. Four of the studies examined treadmill training with and without BFR and the other three studies examined cycling with and without BFR. Baseline characteristics of the study participants are shown in Table 2 with the majority of subjects being physically active except for the subjects in the study by Keramidas et al in which physically inactive subjects were enrolled. Table 3 provides information about the protocols and outcomes of each study. All included studies except for possibly the work by Amani et al, which was difficult to interpret, applied BFR bilaterally at the most proximal portion of the subject’s thighs with all but the study by Paton et al using pressurized cuffs. Paton et al used elastic wraps instead (Get Strength Heavy Duty 75 mm, Waiuku, New Zealand) that were wrapped to a pressure that elicited a subject-perceived (self-reported) pressure of 7 out of 10 described as moderate, but pain free.11 The elastic wraps used in the Paton et al study were unwrapped between treadmill sets for a period of 150 seconds to provide a break from wearing the wraps and to provide time to re-apply the wraps. Two other studies deflated the pressure in the cuffs during rest periods.9,10 The size of the occlusion devices varied from 50 mm to 180 mm and the protocols to occlude the thighs also varied. The pressure used to occlude the thighs also varied with one study using perceived pressure,11 several other studies gradually increasing the occlusion pressure until a maximal level was achieved,7,8,10,12,13 and one study applying a cuff pressure of 90 mm Hg.9 (Table 3) The exercise prescriptions used in each study also varied with the shortest duration of exercise training being two weeks in two studies,8,13 and the longest duration being eight weeks.7 The majority of studies performed exercise 3x/week,7,9,10,12 but one study performed exercise 2x/week,11 while another study performed exercise 12x/week.8 Amani et al did not report the frequency of exercise per week or the duration of exercise for each session.13 The duration of exercise for each session varied from 15

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 178

Figure 2. Flow diagram of study selection.

Table 2. Overall characteristics of participants per study.

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 179

Table 3. Summary of protocols and outcomes from the included studies.

minutes to 30-33 minutes. The intensity of exercise was similar in four of the studies with three using an intensity of 40% of AC,7,8,10 and one using 30-45% of the oxygen reserve.12 One additional study grouped with the above low-intensity aerobic exercise studies used an intensity of 60-70% of the heart rate reserve.13 (Table 3) The two high-intensity studies used an intensity of 90% of AC and 80% of peak running velocity. The two high-intensity studies performed exercise for shorter periods of time and with more frequent rest periods. Keramidas et al had subjects cycle for two minutes at 90% of AC followed by two minutes of cycling at 50% of AC (with thigh cuffs deflated) which was repeated for a total exercise duration of 30 minutes.9 Paton et al had subjects run for 30 seconds at 80% of peak running velocity followed by 30 seconds of rest while straddling the treadmill and repeating this five to eight times after which 150 seconds of rest was provided and the elastic wraps were unwrapped.11 One to two additional sets of the above procedures were performed for a total exercise duration of 12 minutes and 12 minutes of rest.11 The rate of perceived exertion (RPE) during BFR ET was compared to ET without BFR in four of the

seven studies with two of the studies finding significantly greater RPE with BFR compared to ET without BFR.7,11 Park et al demonstrated the progressive increase in RPE during each of the five sets of walking with BFR, but did not statistically compare the RPE between sets or between BFR and non-BFR conditions.8 Keramidas et al found no significant difference in RPE between the BFR and non-BFR groups.9 No complications or adverse events were reported in any of the studies. (Table 3) Maximal exercise testing methods The methods used to determine maximal AC included bicycle exercise testing in four of the studies,7-10 and treadmill exercise testing in three of the studies.11-13 All studies performed a ramping protocol to exhaustion and utilized calibrated respiratory gas analysis systems, but only three studies utilized strict criteria (i.e. plateau in oxygen consumption, attainment of near maximal age predicted heart rate, respiratory exchange ratio > 1.10) to identify maximal oxygen consumption (VO2max).7-9 Because only three studies utilized strict VO2max criteria, the term maximal AC was used rather than VO2max. All studies identified maximal AC using the highest oxygen consumption during the final 15 to 30 seconds

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 180

of exercise testing. Despite only three of the studies using strict VO2max criteria, the maximal AC of the seven studies was similar and reflective of the activity level of the subjects in each study. (Table 2) Synthesized ďŹ ndings A test of heterogeneity yielded a non-significant Q-statistic of 7.19 (df = 6, p = 0.30) indicating that no between-study variance in observed effects for AC existed. Under the fixed-effects model, the overall standardized mean difference of all seven studies was 0.38 (SE = 0.18), which was found to be statistically significant (z = 2.01, p = 0.04; 95% CI = 0.01, 0.75). Differences across subgroups classified according to ET intensity were also assessed using fixed-effects models, given that tests of heterogeneity performed for both the low-to-moderate ET intensity [Q (df = 4) = 5.06, p = 0.28] and the highintensity ET [Q (df = 1) = 0.09, p = 0.76] groups indicated that effects were from the same population. A significant standardized mean difference of 0.57 (SE = 0.22) in AC was found between BFR and non-BFR groups in studies examining low-tomoderate ET intensity (z = 2.47, p = 0.01; 95% CI 0.12, 1.01) while no significant mean difference in AC was found between the groups when the highintensity ET studies were analyzed together (z = 0.04, p = 0.97; 95% CI -0.67, 0.64). Forest plots for the overall and sub-analyses are shown in Figure 3.

Supplementary pooled analyses revealed no significant standardized mean difference in either VE [Q (df = 2) = 1.4, p = 0.49; fixed-effects model: z = 0.69, p = 0.48; 95% CI -0.36, 0.77)] or isometric knee extension strength [Q (df = 2) = 7.9, p = 0.01; random-effects model: z = 1.56, p = 0.11; 95% CI -0.23, 2.05)] post-intervention between the groups. DISCUSSION The overall findings from this systematic review with meta-analysis reveal that aerobic ET performed with BFR significantly improves AC more than aerobic exercise without BFR. A recent systematic review also concluded that aerobic ET with BFR increased AC,6 but provided no meta-analytic results making this the first pooled analysis of previous studies assessing the effects of aerobic ET with BFR on AC. Furthermore, although the finding that no significant improvement in AC was observed when high-intensity aerobic ET was combined with BFR is important, the results should be cautiously interpreted highlighting the need for further investigation of high-intensity ET with and without BFR. Nonetheless, the effects of low-to-moderate intensity aerobic ET with BFR demonstrate significant and consistent improvements in AC compared to low-to-moderate intensity aerobic ET without BFR in healthy mostly active individuals. Furthermore, the RPE was significantly greater during BFR ET

Figure 3. Forest plot of the overall and subgroup effects of blood ďŹ&#x201A;ow restricted exercise on aerobic capacity. The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 181

compared to non-BFR ET in two 7,10 of the four studies in which it was measured and importantly, no complications or adverse events were reported in any of the studies. The reasons for the findings observed in this metaanalysis and the differences found between low-tomoderate intensity aerobic ET with BFR compared to high-intensity aerobic ET with BFR are likely due to the effects of BFR ET on components of the Fick equation, the physiological differences between low-to-moderate versus high-intensity aerobic ET, and possibly muscle damage and oxidative stress from high-intensity aerobic ET with BFR compared to low-to-moderate intensity aerobic ET with BFR. The Impact of the Fick Equation on the Observed Results The Fick equation [VO2 = HR x SV x (a-vO2 difference)] is understandably responsible for the changes observed in this meta-analysis and provides a framework to understand the effects of both low-to-moderate intensity and high-intensity aerobic ET with BFR. Figure 1 provides several possible explanations of how aerobic ET with BFR may improve AC, including the effects of hypoxia on VEGF during BFR as well as the increase in endothelium-dependent vasodilation from increased shear stress and nitric oxide production during cuff release and reperfusion after BFR. Increased VEGF and endothelium-dependent vasodilation from BFR ET have the capacity to improve oxygen delivery and uptake. In fact, Sundberg et al found an improvement in capillary density, oxidative metabolism, and AC after four weeks of one-legged cycle ET with BFR â&#x20AC;&#x153;at the highest tolerable workload that could be sustainedâ&#x20AC;? for 45 minutes.14 Furthermore, the study by de Oliveira et al included in this meta-analysis examined the effects of low-to-moderate intensity aerobic ET with and without BFR on the onset of blood lactate accumulation and found that the BFR group improved 16% compared to the 6% improvement in the non-BFR group reinforcing the above findings of Sundberg et al.10 Several of the studies included in this meta-analysis examined one or more components of the Fick equation besides VO2,7-12 which will provide insight into the physiologic mechanisms responsible for the observed findings.

Although the changes in resting 8,12 and peak heart rate 7-9,12 were similar after aerobic ET with and without BFR, the heart rate during aerobic ET with BFR was significantly greater than aerobic ET without BFR in three studies,7,10,11 while one study observed similar heart rates during such ET.9 The increased training intensity observed during aerobic ET with BFR in the above three studies may be partly responsible for the greater increase in AC after aerobic ET with BFR compared to aerobic ET without BFR. A possible reason for the similar resting and peak heart rates after aerobic ET with and without BFR may be due to the relatively high activity level and fitness of the subjects in all of the studies except Keramidas et al,9 and attainment of maximal or near maximal heart rates during maximal exercise testing, respectively. Park et al did not compare heart rate response between aerobic ET with and without BFR, but they did examine heart rate change during the first and last BFR ET session and found that heart rate was significantly lower at the mid-point and maximal point of BFR ET after performing BFR 2x/day, 6 days/ week, for two weeks.8 Associated with the reduced heart rate in the Park et al study was a significant increase in stroke volume (approximately 22%) during the last aerobic ET with BFR session compared to the first aerobic ET with BFR session. The study by Esparza also examined the effects of aerobic ET with and without BFR on stroke volume and despite finding no significant difference between groups, the BFR group experienced a 5% increase in stroke volume while the stroke volume of the non-BFR group was unchanged.12 Therefore, an improvement in stroke volume from aerobic ET with BFR may be partly responsible for the significant increase in AC we observed in this meta-analysis, but further investigation of this is needed. Another factor that may have contributed to the significant improvement in AC during aerobic ET with BFR is the effect that BFR ET appears to have on minute ventilation (VE). Three of the studies included in this meta-analysis examined change in VE after aerobic ET with and without BFR.8,9,11 Park et al found that VE increased significantly in the BFR group (10%), but was unchanged in the non-BFR group.8 The two high-intensity aerobic ET studies

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with and without BFR found similar results with both the BFR and non-BFR groups increasing VE.9,11 Although the BFR group in the Paton et al study had a 6.8% increase compared to the 0.8% increase in VE in the non-BFR group, the difference was not statistically significant. Keramidas et al found more similar increases in VE in the BFR and non-BFR groups (15.6% versus 13.7%, respectively). Thus, both lowto-moderate and high-intensity ET appear to elicit improvements in VE, but the results of an additional meta-analysis performed on these three studies demonstrated a non-significant effect of aerobic ET with BFR which was likely due to the different ET intensities and the small number of studies and subjects included in the studies. Therefore, due to the small number of studies that examined VE, further investigation of the effects of low-to-moderate and high-intensity aerobic ET with and without BFR is needed to determine the role VE may have in the improvement of AC. An additional factor that may be responsible for the effects of aerobic ET with BFR on improving AC in this meta-analysis is an increase in hematopoietic factors such as erythropoietin, hemoglobin, and hematocrit concentrations during hypoxic conditions such as that during BFR.15,16 Only one of the studies in this meta-analysis examined hemoglobin and hematocrit and found no change in either measure after six weeks of cycling at 90% of AC for two minutes followed by two minutes of cycling at 50% of AC with BFR cuffs deflated which was repeated for 30 minutes, 3x/week.9 Despite Keramidas et al observing no change in hemoglobin or hematocrit concentration, near-infrared spectroscopy applied to the right vastus lateralis muscle during a submaximal exercise test found the change in total hemoglobin and oxyhemoglobin increased in both the BFR and non-BFR groups. Furthermore, after ET oxygen consumption was significantly lower in both groups during the submaximal exercise test at the same relative workload reflecting greater muscular efficiency.9 Additionally, Paton et al observed an improvement in running economy only in the BFR group despite AC improving similarly in both the BFR and nonBFR groups. Therefore, the Fick equation peripheral component (a-vO2 difference) and possibly the central components (HR and SV) contributed to greater

muscular efficiency during submaximal exercise as a result of high-intensity ET.9,11 In view of these results, further investigation of aerobic ET with and without BFR on muscular efficiency and hematopoietic factors appears warranted. Change in particular characteristics of skeletal muscle associated with aerobic ET and BFR may also be responsible for the improvements that were observed in AC. All included studies but the work by Amani et al examined some characteristic of skeletal muscle including strength (n=3), hypertrophy (n=1), power (n=3), and peak running velocity (n=1). Across the studies, isometric knee extension strength tended to be greater post-ET with BFR when compared to ET alone, even though no significant standardized mean difference between the groups was observed in our supplementary analysis. Improvements in hypertrophy and power also seemed to be greater in the aerobic ET with BFR groups when compared to the non-BFR groups, but the methodology that the above characteristics were measured and reported prevented these data from being subjected to an additional pooled analysis. Therefore, increased skeletal muscle strength, hypertrophy, and power may be partly responsible for the improvement in AC observed in this metaanalysis, but further investigation is warranted. Minimal Clinically Important Difference in Aerobic Capacity It is important to interpret the change in AC from aerobic ET with and without BFR presented in this meta-analysis with the minimal clinically important difference (MCID) in AC in healthy adults. Hays and Woolley suggest that the threshold for a MCID corresponds to a small effect size (0.20) while others suggest that a MCID reflects a difference or change of Â˝ of the baseline standard deviation (SD).17,18 The data presented in Figure 2 for the combined high-intensity and the low-to-moderate intensity ET studies shows that the effect size (std. mean difference) exceeds 0.20 (0.38) and that the low-to-moderate intensity ET studies with BFR far exceeds this threshold (0.57) while the high-intensity ET studies fall far below it (-0.01). Furthermore, half of the baseline SD data from both the low-to-moderate and high-intensity ET studies reveals that a threshold of 3.3 ml/kg/min in AC was needed

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to achieve a MCID which was exceeded by two of the five low-to-moderate intensity ET studies with BFR,7,8 and neither of the high-intensity ET studies with BFR exceeded this value.9,11 The above effect size (std. mean difference) results are also supported by a previous study which found that a 3.4% increase in AC was considered to be a MCID in healthy adults.19 In view of the results of this meta-analysis, all included studies but the work by Keramidas et al had an increase in AC in the BFR group that exceeded 3.4% and only two of the seven studies (i.e. Esparza and Paton et al) observed an improvement in AC in the non-BFR group that exceeded 3.4%. The change in AC of the non-BFR groups in the five other studies ranged from – 4.2% to + 0.7%.7-10,13 Finally, the one study in which the BFR group did not exceed a 3.4% improvement in AC (a high-intensity study) did observe a decrease in AC that was less than the non-BFR group (– 2.2% versus – 4.2%, respectively).9 Thus, BFR with aerobic ET appears to facilitate an improvement in AC with a MCID in AC in the majority of studies. Low-to-Moderate Intensity Versus HighIntensity Exercise with and without Blood Flow Restriction The results of this systematic review with meta-analysis suggest that low-to-moderate intensity aerobic ET with BFR physiologically elicits more AC compared to high-intensity ET with BFR which appears to elicit more anaerobic capacity.7-13 However, high-intensity aerobic ET without BFR also elicits improvements in AC as observed in two comprehensive meta-analyses.20,21 One meta-analysis found that ET intensity divided into tertiles based on intensity (60-70%, 80-92.5%, and over 100% of VO2max) had no statistically significant effect on the magnitude of improvement in AC in healthy adults with effect sizes of 0.77, 0.68, and 0.80, respectively.20 Thus, the highest ET intensity (over 100% of VO2max) produced the greatest effect on AC. The second metaanalysis found that both low-to-moderate aerobic ET and high-intensity ET elicit significant increases in AC in healthy adults with greater gains in AC following high-intensity ET compared to endurance training.21 However, the effect of high-intensity aerobic ET with BFR requires further investigation and discussion in view of the results observed in this systematic review and meta-analysis.

The two high-intensity ET studies included in this meta-analysis used an intensity of 90% of AC 9 and 80% of peak running velocity 11 and performed exercise for shorter periods of time and with more frequent rest periods than the low-to-moderate intensity ET studies. Also, during high-intensity aerobic ET with BFR, both studies eliminated BFR repeatedly during the rest periods. The results of high-intensity ET with BFR found an increase in AC in only one study (i.e. Paton et al) which increased more in the BFR group compared to the non-BFR group (2.9 versus 1.8 ml/kg/min, respectively), but it was not a statistically significant difference.11 In contrast, Keramidas et al found AC to decrease in both the BFR and non-BFR groups with less of a decrease in the BFR group (0.8 versus 1.6 ml/kg/min, respectively), which was also statistically insignificant. In view of the above, a limited ET duration and more frequent rest periods with deflated cuffs may be responsible for the lack of improvement in AC during high-intensity aerobic ET with BFR observed in this meta-analysis. This is particularly interesting given that only one of the low-to-moderate intensity studies provided reperfusion during one-minute passive rest periods.10 Thus, further investigation of low-to-moderate and high-intensity ET with BFR followed by reperfusion on AC is needed. An important consideration given the above studies and the findings of high-intensity aerobic ET with BFR is the manner by which high-intensity aerobic ET with BFR may potentially damage skeletal muscle compared to low-to-moderate intensity aerobic ET with BFR. Studies of high-intensity resistance ET (≥ 70% 1RM) of a large muscle mass have consistently observed substantial increases in blood oxidative stress markers while low-intensity resistance training (≤ 30% 1RM) with BFR has not been found to increase oxidative stress.4 Similarly, high-intensity resistance ET has been observed to significantly increase creatine kinase values while low-intensity resistance and aerobic ET has not been found to increase creatine kinase or myoglobin content.4 Although the above research on skeletal muscle damage is limited, from the available literature it appears that low-to-moderate intensity ET with BFR is less likely to damage skeletal muscle compared to high-intensity ET with BFR. In fact, Loenneke

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et al concluded that low-intensity ET with BFR does not produce skeletal muscle damage in view of the absence of prolonged decrements in muscle function, no prolonged swelling, soreness ratings were similar to a submaximal low load control, and no elevation in blood biomarkers of muscle damage have been reported.5 Additionally, no complications or adverse events were reported in any of the studies included in this meta-analysis. In view of the above, further investigation of the effects of low-to-moderate and high-intensity aerobic ET with and without BFR on skeletal muscle damage is needed since little literature appears to exist.4,5 Limitations The limitations of this meta-analysis include a variety of aerobic ET regimens and methods to employ BFR as well as the limited number of high-intensity aerobic ET studies comparing the effects of aerobic ET with and without BFR on AC. Other limitations include the absence of consistent and similar measures of skeletal muscle characteristics such as strength, hypertrophy, and power as well as the absence of data on the effects of varying intensities of aerobic ET with BFR on skeletal muscle damage. Further research in the above areas is needed to fully understand the effects of aerobic ET with BFR. CONCLUSIONS The results of this systematic review and meta-analysis reveal that aerobic ET with BFR elicits a greater improvement in AC than aerobic ET without BFR. Although high-intensity aerobic ET with BFR did not appear to elicit an improvement in AC over highintensity aerobic ET without BFR only two studies were available to be included in this analysis for which reason these results should be interpreted cautiously. Further investigation of the effects of low-to-moderate and high-intensity aerobic ET with and with BFR on AC as well as the components of the Fick equation and VE are needed. REFERENCES 1. Hughes L, Paton B, Rosenblatt B, Gissane C, Patterson SD. Blood ﬂow restriction training in clinical musculoskeletal rehabilitation: a systematic review and meta-analysis. Br J Sports Med. 2017;51(13):1003-1011.

2. Ipavec M, Grapar Zargi T, Jelenc J, Kacin A. Efficiency of pneumatic tourniquet cuff with asymmetric pressure distribution at rest and during isometric muscle action. J Strength Cond Res. 2018;33(9):2570-2578. 3. Wong ML, Formiga MF, Owens J, Asken T, Cahalin LP. Safety of blood flow restricted exercise in hypertension: a meta-analysis and systematic review with potential applications in orthopedic care. Tech Orthop. 2018;33(2):80-88. 4. Loenneke JP, Wilson JM, Wilson GJ, Pujol TJ, Bemben MG. Potential safety issues with blood flow restriction training. Scand J Med Sci Sports. 2011;21(4):510-518. 5. Loenneke JP, Thiebaud RS, Abe T. Does blood flow restriction result in skeletal muscle damage? A critical review of available evidence. Scand J Med Sci Sports. 2014;24(6):e415-422. 6. Bennett H, Slattery F. Effects of blood flow restriction training on aerobic capacity and performance: a systematic review. J Strength Cond Res. 2019;33(2):572-583. 7. Abe T, Fujita S, Nakajima T, et al. Effects of lowintensity cycle training with restricted leg blood flow on thigh muscle volume and VO2max in young men. J Sport Sci Med. 2010;9(3):452-458. 8. Park S, Kim JK, Choi HM, Kim HG, Beekley MD, Nho H. Increase in maximal oxygen uptake following 2-week walk training with blood flow occlusion in athletes. Eur J Appl Physiol. 2010;109(4):591-600. 9. Keramidas ME, Kounalakis SN, Geladas ND. The effect of interval training combined with thigh cuffs pressure on maximal and submaximal exercise performance. Clin Physiol Funct Imaging. 2012;32(3):205-213. 10. de Oliveira MF, Caputo F, Corvino RB, Denadai BS. Short-term low-intensity blood flow restricted interval training improves both aerobic fitness and muscle strength. Scand J Med Sci Sports. 2016;26(9):1017-1025. 11. Paton CD, Addis SM, Taylor LA. The effects of muscle blood flow restriction during running training on measures of aerobic capacity and run time to exhaustion. Eur J Appl Physiol. 2017;117(12):2579-2585. 12. Esparza BN. The effects of a short-term endurance training program with blood flow restriction cuffs versus ACSM recommended endurance training on arterial compliance and muscular adaptations in recreationally active males. ProQuest Dissertations Publishing. Published 2017. Accessed 2018.

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13. Amani A, Sadeghi H, Afsharnezhad T. Interval training with blood ﬂow restriction on aerobic performance among young soccer players at transition phase. Monten J Sports Sci Med. 2018;7(2):5-10. 14. Sundberg CJ, Eiken O, Nygren A, Kaijser L. Effects of ischaemic training on local aerobic muscle performance in man. Acta Physiol Scand. 1993;148(1):13-19. 15. Dale EA, Ben Mabrouk F, Mitchell GS. Unexpected beneﬁts of intermittent hypoxia: enhanced respiratory and nonrespiratory motor function. Physiology. 2014;29(1):39-48. 16. Koistinen PO, Rusko H, Irjala K, et al. EPO, red cells, and serum transferrin receptor in continuous and intermittent hypoxia. Med Sci Sports Exerc. 2000;32(4):800-804. 17. Hays RD, Woolley JM. The concept of clinically meaningful difference in health-related quality-oflife research. How meaningful is it? PharmacoEconomics. 2000;18(5):419-423.

18. Jaeschke R, Singer J, Guyatt GH. Measurement of health status. Ascertaining the minimal clinically important difference. Control Clin Trials. 1989;10(4):407-415. 19. Clark NA, Edwards AM, Morton RH, Butterly RJ. Season-to-season variations of physiological ﬁtness within a squad of professional male soccer players. J Sport Sci Med. 2008;7(1):157-165. 20. Scribbans TD, Vecsey S, Hankinson PB, Foster WS, Gurd BJ. The effect of training intensity on VO2max in young healthy adults: a meta-regression and meta-analysis. Int J Exerc Sci. 2016;9(2):230-247. 21. Milanovic Z, Sporis G, Weston M. Effectiveness of high-intensity interval training (HIT) and continuous endurance training for VO2max improvements: a systematic review and metaanalysis of controlled trials. Sports Med. 2015;45(10):1469-1481.

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Appendix 1.

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IJSPT

ORIGINAL RESEARCH

POSTERIOR SHOULDER TIGHTNESS AND SUBACROMIAL IMPINGEMENT CHARACTERISTICS IN BASEBALL PITCHERS: A BLINDED, MATCHED CONTROL STUDY Kevin Laudner, PhD, ATC1 Regan Wong, PT2 James Latal, ATC3 Keith Meister, MD2

ABSTRACT Background: Baseball pitchers frequently develop varying levels of posterior shoulder tightness (PST) and often present with characteristics associated with subacromial impingement. Purpose: To determine if a group of baseball pitchers with excessive PST (bilateral internal rotation ROM difference >18° and bilateral total arc of motion difference >5°) have differences in subacromial joint space, forward scapular posture, or glenohumeral elevation range of motion (ROM) when compared to a control group. Study Design: Descriptive, cross-sectional study. Methods: Thirty-five asymptomatic professional baseball pitchers with excessive PST were matched with 35 pitchers with acceptable levels of PST. The investigators measured subacromial space using diagnostic ultrasound, glenohumeral elevation ROM using a digital goniometer, and scapular posture using a double square, and were blinded to the group of each participant. Separate t-tests were used to determine significant differences between groups (p<0.05). Results: The excessive PST group presented with significantly less subacromial space (p=.0007) and glenohumeral elevation ROM (p=.03) compared to the acceptable level PST group. The excessive PST group also had significantly more forward scapular posture than the control group (p=.03). Conclusion: The baseball pitchers with excessive PST had less subacromial space and glenohumeral elevation ROM, as well as more forward scapular posture in their throwing arms compared to pitchers with acceptable levels of PST. Level of Evidence: 3 Keywords: Baseball, glenohumeral, scapula, subacromial space

Department of Health Sciences, University of Colorado Colorado Springs, Colorado Springs, CO, USA 2 Texas Metroplex Institute for Sports Medicine and Orthopedics, Arlington, TX, USA 3 School of Kinesiology and Recreation, Illinois State University, Normal, IL, USA Funding: No ﬁnancial support was provided for this study.

CORRESPONDING AUTHOR Kevin Laudner, PhD, ATC University of Colorado Colorado Springs 1420 Austin Bluffs Parkway Colorado Springs, CO 80918 Phone: (719) 255-4411 E-mail: klaudner@uccs.edu

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 188 DOI: 10.26603/ijspt20200188

INTRODUCTION Because of the violent and repetitive nature of throwing a baseball, physical adaptations are common among pitchers. Numerous studies have demonstrated decreases in shoulder strength,1,2 scapular kinematics,3 hip range of motion (ROM) and strength,4 as well as trunk ROM.5 However, one of the most common and largest changes is the loss of glenohumeral internal rotation ROM in the throwing arm of pitchers compared to their nonthrowing arm.6,7 This loss is often the result of posterior shoulder tightness (PST).6-8 Structures affected can include the posterior glenohumeral capsule,8 as well as the posterior shoulder muscles,7 such as the infraspinatus, teres minor, and posterior deltoid that are responsible for eccentrically controlling internal rotation and horizontal adduction during the follow through phase of the throwing motion.9

PST in baseball pitchers and its relationship with subacromial impingement syndrome, it is not clear whether pitchers with excessive PST have an increased risk of characteristics associated with subacromial impingement syndrome. Being able to identify these potentially pathologic characteristics could provide clinicians an advantage for addressing such deficiencies and positively affecting movement strategies prior to injury. The purpose of this study was to determine if a group of baseball pitchers with excessive PST have differences in subacromial joint space, forward scapular posture, or glenohumeral elevation range of motion (ROM) when compared to a control group. The investigators hypothesized that asymptomatic pitchers with excessive PST would have less subacromial joint space, glenohumeral elevation ROM, and more forward scapular posture than pitchers without PST.

Although PST is a common characteristic among many baseball players, excessive losses in glenohumeral internal rotation can become pathologic. Pathologies such as internal impingement, SLAP lesions, UCL elbow sprains, and subacromial impingement syndrome have been associated with PST.7,10-13 Subacromial impingement syndrome is the most commonly diagnosed shoulder pathology within the general population14-16 and is also a frequent pathology seen in baseball pitchers.17-20 This pathology contributes up to 67% of upper extremity injuries and 74 days on the disabled list experienced by major league baseball players annually.21

METHODS All participants provided informed consent as mandated by the universityâ&#x20AC;&#x2122;s institutional review board prior to testing. The Institutional Review Board at Illinois State University approved the study and the rights of all participants were protected.

Along with symptoms of excessive PST, subacromial impingement patients also present with decreased subacromial joint space,22 decreased glenohumeral elevation ROM,23 and increased forward scapular posture, which can be the result of increased scapular protraction and anterior tilt.24,25 Although the decreased glenohumeral elevation ROM may be an attempt to avoid soft tissue contact in patients with subacromial impingement26 the decreased subacromial space and forward scapular posture may actually increase soft tissue contact.27-30 Excessive PST has been defined as a bilateral difference in glenohumeral internal rotation ROM of greater than 18Â° and a greater than 5Â° difference in the total arc of motion.31 Despite the recognized

Seventy professional baseball pitchers volunteered to participate in this study. Thirty-five pitchers identified with excessive PST (31 right-handed, 4 lefthanded) were matched to 35 control pitchers (20 right-handed, 15 left-handed) based on age, height, and mass (Table 1). These participants were chosen based on a sample of convenience. All participants were asymptomatic at the time of testing. Exclusion criteria consisted of any recent upper extremity injury (injury within past year) or any history of upper extremity surgery. An upper extremity injury was defined as any injury that caused the individual to miss any amount of time from practice or competition. All testing was conducted in the athletic training room of the spring training facility of a professional baseball organization. No testing was conducted following any conditioning workout or throwing session. The same two investigators conducted all measurements for elevation ROM, subacromial joint space, and forward scapular posture, while separate investigators measured internal and external

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Table 1. Descriptive Participant Demographics (n= 70, all subjects were male).

ROM. Therefore, the investigators measuring the dependent variables (e.g. subacromial joint space, forward scapular posture, glenohumeral elevation ROM) were blinded to the group assignment of each participant. Passive glenohumeral internal rotation, external rotation, and elevation ROM were measured using a Pro 3600 Digital Inclinometer (SPI-Tronic, Garden Grove, CA). All ROM measurements were conducted with the participant supine on a standard treatment table. For rotational motion the test shoulder was placed in 90° of abduction and neutral rotation. One investigator then stabilized the scapula by providing a posterior force to the anterior acromion while passively moving each participant’s arm into either internal or external rotation until the first point of resistance. In this position a second examiner aligned the inclinometer with the forearm for measurement. The total arc of motion was calculated as the sum of maximum internal and external rotation. Elevation motion was measured with participants in the same position. One investigator applied a posterior force to the lateral border of the scapula and moved the shoulder until the first point of resistance in elevation. In this position the second investigator then aligned the inclinometer with the humeral shaft to determine the angle between the humerus and the horizontal plane. A priori intratester reliability was examined, and strong reliability was demonstrated for the investigators conducting these measurements (internal rotation ICC=0.98, SEM=2°, external rotation ICC=0.95, SEM=3°, and elevation ICC=.92, SEM=3°). Subacromial joint space was measured using the Terason t3000 M-series ultrasound system (Teratech, Burlington, MA). For this measurement each participate stood in a relaxed position with their shoulder in approximately 0° of abduction. The ultrasound head was placed over the lateral aspect

of the acromion, as determined by palpation, and in line with scapular plane. From this single, static image the shortest distance between the inferior acromion and the humeral head was then measured using the ultrasound software caliper function. A priori intra-test reliability testing showed strong reliability (ICC=0.83, SEM=0.84mm) for the investigators conducting this measurement. Forward scapular posture was measured using the double square method.32 For this measurement each participant stood in a relaxed position with their back against a wall. An investigator then used the double square to measure the distance between the wall and the most anterior aspect of the acromion. The bilateral difference between forward scapular posture measurements was used to determine the amount of forward scapular posture for the throwing arm. The intra-tester reliability of this measurement had strong reliability (ICC=0.84, SEM=4.6mm). The means and standard deviations for all dependent variables were calculated and separate paired t tests were run to determine significant differences between groups (IBM SPSS Statistics 22; IBM Corporation, Armonk, NY). Findings were considered significant at an alpha level of p<0.05. Cohen’s d effect sizes were determined to provide an indication of the clinical meaningfulness for between group differences. Effect size was calculated as excessive PST group mean – control group mean / control group standard deviation. Effect sizes were

interpreted as small=0.20, medium=0.50, and large=0.80.33 RESULTS The descriptive glenohumeral ROM characteristics for each group can be viewed in Table 2. There were no between group differences for age, height, or mass (p>0.30). The excessive PST group presented with significantly less subacromial space (p=.0007; effect

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Table 2. Descriptive Glenohumeral Range of Motion Characteristics by Group.

Table 3. Between Group Descriptive Statistics (mean Âą standard deviation).

size=0.74) and glenohumeral elevation ROM (p=.03; effect size=0.52) than the control group (Table 3). The excessive PST group also had significantly more forward scapular posture of their throwing arm than the control group (p=.03; effect size=0.51) (Table 3). All of the identified differences had moderate effects sizes. Furthermore, the between group differences were larger than their respective standard error of measurement suggesting clinical significance, as well as statistical significance. DISCUSSION Due to the recognized relationship between excessive PST and various shoulder disorders it is critical that clinicians understand how PST may contribute to the development of such pathologies. The results of this study are the first to show that

baseball pitchers identified with excessive PST have decreased subacromial joint space, humeral elevation ROM, and increased forward scapular posture, which have all been linked to subacromial impingement syndrome.34 For the purpose of this study the investigators chose not to use the term glenohumeral internal rotation deficit or GIRD because they believe it can be misinterpreted. In the investigatorsâ&#x20AC;&#x2122; clinical experience most baseball players, especially pitchers, have a loss of glenohumeral internal rotation ROM in their dominant shoulder compared to their non-dominant. However, this loss can be attributed to bony and/or soft tissue adaptations. The bony adaptations come from an increase in humeral retroversion, which is often the result of increased rotational forces during the throwing motion while the athlete

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is still skeletally immature.35 This increase in retroversion has actually been reported to reduce the risk of shoulder injury and causes an increase in GH external rotation ROM with a concomitant amount of loss in internal rotation resulting in no bilateral difference in the total arc of motion.35 However, posterior soft tissue tightness would alter the total arc of motion because of lost internal rotation without the subsequent gain in external rotation.36 The investigators of this study attempted to assess the loss of internal rotation caused by soft tissue contributions, which is why the bilateral difference in total arc of motion was used within the definition of excessive PST. Decreased total arc of motion may also be more problematic in regards to pathology than losses in GH internal rotation.37 The precise tissue(s) causing PST remains a topic of debate. Takenaga et al.,8 reported that the posterior capsule in the throwing shoulder of baseball players is thicker and stiffer when compared to their non-throwing shoulder. Conversely, posterior rotator cuff stiffness has been suggested to limit internal rotation ROM.7 Regardless of the specific structures involved, PST remains a common problem among pitchers and can result in various shoulder adaptations.11,12,38 PST can cause a posterior-medial shift in the position of the humeral head on the glenoid resulting in decreased subacromial joint space,11 which may partially explain the decreased subacromial space among the participants with excessive PST in the current study. The pitchers in the excessive PST group also presented with less glenohumeral elevation ROM. Because the humeral head translates superiorly during humeral elevation,39 Steenbrink et al.,26 speculated that with a decreased subacromial joint space at rest there is less room for the humeral head to translate superiorly during humeral elevation prior to contact between the humeral head and subacromial arch. Externally rotating the humerus allows the greater tuberosity to clear the acromion;40 however, the participants in the current study were in neutral rotation during the elevation ROM measurement. Therefore, the loss of glenohumeral elevation, in the participants with excessive PST, may be a preventative technique to avoid increased contact of the soft tissue structures and subsequent pain

within a smaller subacromial joint space. However, further research is necessary to confirm this. Laudner et al.,41 identified an association between PST and increased forward scapular posture and hypothesized that PST causes the humeral head to pull the scapula forward during the follow through phase of the throwing motion, resulting in a more forward scapular position. The results of the current study, which found increased forward scapular posture among the excessive PST group, supports these previous findings. Furthermore, Solem-Bertoft et al.,42 showed that as the scapula moves into a more forward position, such as with increased scapular protraction, the subacromial joint space decreases. This decreased space may then lead to increased contact pressure of the soft tissue structures29 and ultimately to impingement.22,27,28,30,43,44 The subacromial joint space in asymptomatic shoulders has been reported to range from 8.7 â&#x20AC;&#x201C; 11.1mm with the shoulder in a resting position.22,45 Because this small space also houses several soft tissue structures, any reductions in this area, even minor changes, whether it be from humeral head superior migration or from scapular malposition, can result in significant increases in the contact pressure of the soft tissues structures.24,27,43,44 Based on the results of the current study, the investigators suggest that excessive PST should be considered in the prevention, diagnosis, and rehabilitation of pathologies associated with decreased subacromial joint space, decreased glenohumeral elevation ROM, and increased forward scapular posture. The investigators of this study would again like to emphasize that all participants were asymptomatic at the time of testing. Even the excessive PST group did not have pain despite having characteristics similar to those of subacromial impingement patients, such as limited subacromial joint space, decreased glenohumeral elevation, and increased forward scapular posture. There are various potential reasons why these individuals did not present with pain. Most notably, subacromial impingement can be caused by or the result of numerous physical abnormalities. Presenting with one or multiple of these aberrant characteristics does not necessarily result in pain.34 For example, abnormal acromial

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shape, osteophyte formation, increased thoracic spine flexion, as well as weakness of the rotator cuff and periscapular muscles have all been associated with impingement.34 Therefore, it is not surprising that the participants of the current study that had excessive PST in conjunction with deficient subacromial space, glenohumeral elevation, and scapular posture did not present with impingement pain. Furthermore, it is plausible that the detrimental characteristics present among these participants with excessive PST may have not be extensive enough to cause pain. As such, the investigators hypothesize that if the PST continues and the changes in subacromial space, glenohumeral elevation, and scapular posture worsen, the likelihood of pain could then increase in a concomitant fashion. However, future research is needed to prove this hypothesis. There are limitations of this study. First, all participants were asymptomatic at the time of testing. Although, the excessive PST group presented with characteristics similar to those of patients diagnosed with subacromial impingement syndrome, such as decreased subacromial joint space, decreased glenohumeral elevation, and increased forward scapular posture, patients with shoulder disorders may present with different findings. Second, in a prior study examining thoracolumbar rotational ROM in pitchers, pitchers had greater active-assisted rotation to their non-dominant side compared to their dominant side.5 It is possible that this postural adaptation could bias the ribs and thorax to be rotated to the non-dominant side in the resting position. Because the scapula sits on the posterior ribs, a rotated ribcage towards the non-dominant side would naturally cause the scapula to follow the ribs and present in a more protracted, anteriorly tipped, and internally rotated position. This in turn could create a less than optimal glenoid to humeral head alignment and give the perception of PST when assessing glenohumeral internal rotation ROM. Also, worth noting, the subacromial joint space was only measured in the resting position. CONCLUSIONS The results of this study demonstrate that baseball pitchers with excessive PST have less subacromial space, glenohumeral elevation ROM, and increased

forward scapular posture in their throwing arms as compared to pitchers without excessive PST. Increased PST may be a precursor to pathologies associated with these shoulder characteristics, such as subacromial impingement syndrome. REFERENCES 1. Magnusson SP, Gleim GW, Nicholas JA. Shoulder weakness in professional baseball pitchers. Med Sci Sports Exerc. 1994;26(1):5-9. 2. Lin HT, Ko HT, Lee KC, Chen YC, Wang DC. The changes in shoulder rotation strength ratio for various shoulder positions and speeds in the scapular plane between baseball players and nonplayers. J Phys Ther Sci. 2015;27(5):1559-1563. 3. Myers JB, Laudner KG, Pasquale MR, Bradley JP, Lephart SM. Scapular position and orientation in throwing athletes. Am J Sports Med. 2005;33(2): 263-271. 4. Laudner KG, Moore SD, Sipes RC, Meister K. Functional hip characteristics of baseball pitchers and position players. Am J Sports Med. 2010;38(2):383-387. 5. Laudner K, Lynall R, Williams JG, Wong R, Onuki T, Meister K. Thoracolumbar range of motion in baseball pitchers and position players. Int J Sports Phys Ther. 2013;8(6):777-783. 6. Laudner KG, Stanek JM, Meister K. Assessing posterior shoulder contracture: the reliability and validity of measuring glenohumeral joint horizontal adduction. J Athl Train. 2006;41(4):375-380. 7. Shanley E, Kissenberth MJ, Thigpen CA, et al. Preseason shoulder range of motion screening as a predictor of injury among youth and adolescent baseball pitchers. J Shoulder Elbow Surg. 2015;24(7):1005-1013. 8. Takenaga T, Sugimoto K, Goto H, et al. Posterior Shoulder Capsules Are Thicker and Stiffer in the Throwing Shoulders of Healthy College Baseball Players: A Quantitative Assessment Using ShearWave Ultrasound Elastography. Am J Sports Med. 2015;43(12):2935-2942. 9. Pappas AM, Zawacki RM, McCarthy CF. Rehabilitation of the pitching shoulder. Am J Sports Med. 1985;13(4):223-235. 10. Tyler TF, Nicholas SJ, Roy T, Gleim GW. QuantiďŹ cation of posterior capsule tightness and motion loss in patients with shoulder impingement. Am J Sports Med. 2000;28(5):668-673. 11. Maenhout A, Van Eessel V, Van Dyck L, Vanraes A, Cools A. Quantifying acromiohumeral distance in overhead athletes with glenohumeral internal

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rotation loss and the influence of a stretching program. Am J Sports Med. 2012;40(9):2105-2112. 12. Myers JB, Laudner KG, Pasquale MR, Bradley JP, Lephart SM. Glenohumeral range of motion deficits and posterior shoulder tightness in throwers with pathologic internal impingement. Am J Sports Med. 2006;34(3):385-391. 13. Wilk KE, Macrina LC, Fleisig GS, et al. Correlation of glenohumeral internal rotation deficit and total rotational motion to shoulder injuries in professional baseball pitchers. Am J Sports Med. 2011;39(2):329-335. 14. van der Windt DA, Koes BW, Boeke AJ, Deville W, de Jong BA, Bouter LM. Shoulder Disorders in General Practice: Prognostic Indicators of Outcome. Br J Gen Pract. 1996;46:519-523. 15. Vecchio P, Kavanagh R, Hazleman BL, King RH. Shoulder pain in a community-based rheumatology clinic. Br J Rheumatol. 1995;34(5):440-442. 16. Vecchio PC, Kavanagh RT, Hazleman BL, King RH. Community survey of shoulder disorders in the elderly to assess the natural history and effects of treatment. Ann Rheum Dis. 1995;54(2):152-154. 17. Borsa PA, Laudner KG, Sauers EL. Mobility and stability adaptations in the shoulder of the overhead athlete: a theoretical and evidence-based perspective. Sports Med. 2008;38(1):17-36. 18. Jobe FW, Kvitne RS, Giangarra CE. Shoulder pain in the overhand or throwing athlete. The relationship of anterior instability and rotator cuff impingement. Orthop Rev. 1989;18(9):963-975. 19. Park SS, Loebenberg ML, Rokito AS, Zuckerman JD. The shoulder in baseball pitching: biomechanics and related injuries-part 1. Bull Hosp Jt Dis. 2002;61(12):68-79. 20. Cools AM, Witvrouw EE, Declercq GA, Vanderstraeten GG, Cambier DC. Evaluation of isokinetic force production and associated muscle activity in the scapular rotators during a protractionretraction movement in overhead athletes with impingement symptoms. Br J Sports Med. 2004;38(1):64-68. 21. Posner M, Cameron KL, Wolf JM, Belmont PJ, Jr., Owens BD. Epidemiology of Major League Baseball injuries. Am J Sports Med. 2011;39(8):1676-1680.

24. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80(3):276-291. 25. Warner JJ, Micheli LJ, Arslanian LE, Kennedy J, Kennedy R. Scapulothoracic motion in normal shoulders and shoulders with glenohumeral instability and impingement syndrome. A study using Moire topographic analysis. Clin Orthop Relat Res. 1992(285):191-199. 26. Steenbrink F, de Groot JH, Veeger HE, Meskers CG, van de Sande MA, Rozing PM. Pathological muscle activation patterns in patients with massive rotator cuff tears, with and without subacromial anaesthetics. Man Ther. 2006;11(3):231-237. 27. Graichen H, Bonel H, Stammberger T, et al. Threedimensional analysis of the width of the subacromial space in healthy subjects and patients with impingement syndrome. AJR Am J Roentgenol. 1999;172(4):1081-1086. 28. Mayerhoefer ME, Breitenseher MJ, Wurnig C, Roposch A. Shoulder impingement: relationship of clinical symptoms and imaging criteria. Clin J Sport Med. 2009;19(2):83-89. 29. Mihata T, Jun BJ, Bui CN, et al. Effect of scapular orientation on shoulder internal impingement in a cadaveric model of the cocking phase of throwing. J Bone Joint Surg Am. 2012;94(17):1576-1583. 30. Seitz AL, Michener LA. Ultrasonographic measures of subacromial space in patients with rotator cuff disease: A systematic review. J Clin Ultrasound. 2011;39(3):146-154. 31. Manske R, Wilk KE, Davies G, Ellenbecker T, Reinold M. Glenohumeral motion deﬁcits: friend or foe? Int J Sports Phys Ther. 2013;8(5):537-553. 32. Peterson DE, Blankenship KR, Robb JB, et al. Investigation of the validity and reliability of four objective techniques for measuring forward shoulder posture. J Orthop Sports Phys Ther. 1997;25(1):34-42. 33. Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice. Second ed: Prentice-Hall; 2000. 34. Michener LA, McClure PW, Karduna AR. Anatomical and biomechanical mechanisms of subacromial impingement syndrome. Clin Biomech (Bristol, Avon). 2003;18(5):369-379.

22. Hebert LJ, Moffet H, Dufour M, Moisan C. Acromiohumeral distance in a seated position in persons with impingement syndrome. J Magn Reson Imaging. 2003;18(1):72-79.

35. Pieper HG. Humeral torsion in the throwing arm of handball players. Am J Sports Med. 1998;26(2):247-253.

23. Deutsch A, Altchek DW, Schwartz E, Otis JC, Warren RF. Radiologic measurement of superior displacement of the humeral head in the impingement syndrome. J Shoulder Elbow Surg. 1996;5(3):186-193.

36. Reagan KM, Meister K, Horodyski MB, Werner DW, Carruthers C, Wilk K. Humeral retroversion and its relationship to glenohumeral rotation in the shoulder of college baseball players. Am J Sports Med. 2002;30(3):354-360.

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37. Garrison JC, Cole MA, Conway JE, Macko MJ, Thigpen C, Shanley E. Shoulder range of motion deďŹ cits in baseball players with an ulnar collateral ligament tear. Am J Sports Med. 2012;40(11):2597-2603. 38. Mihata T, Gates J, McGarry MH, Neo M, Lee TQ. Effect of posterior shoulder tightness on internal impingement in a cadaveric model of throwing. Knee Surg Sports Traumatol Arthrosc. 2015;23(2):548-554. 39. Chen SK, Simonian PT, Wickiewicz TL, Otis JC, Warren RF. Radiographic evaluation of glenohumeral kinematics: a muscle fatigue model. J Shoulder Elbow Surg. 1999;8(1):49-52. 40. Kent BE. Functional anatomy of the shoulder complex. A review. Phys Ther. 1971;51(8):947. 41. Laudner KG, Moline MT, Meister K. The relationship between forward scapular posture and posterior shoulder tightness among baseball players. Am J Sports Med. 2010;38(10):2106-2112.

42. Solem-Bertoft E, Thuomas KA, Westerberg CE. The inďŹ&#x201A;uence of scapular retraction and protraction on the width of the subacromial space. An MRI study. Clin Orthop Relat Res. 1993(296):99-103. 43. Hyvonen P, Lantto V, Jalovaara P. Local pressures in the subacromial space. Int Orthop. 2003;27(6):373-377. 44. Nordt WE, 3rd, Garretson RB, 3rd, Plotkin E. The measurement of subacromial contact pressure in patients with impingement syndrome. Arthroscopy. 1999;15(2):121-125. 45. Flatow EL, Soslowsky LJ, Ticker JB, et al. Excursion of the rotator cuff under the acromion. Patterns of subacromial contact. Am J Sports Med. 1994;22(6):779-788.

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IJSPT

ORIGINAL RESEARCH

CHANGES IN INFRASPINATUS AND LOWER TRAPEZIUS ACTIVATION IN VOLLEYBALL PLAYERS FOLLOWING REPETITIVE SERVES Katelyn M. Khal, MA, ATC1 Stephanie D. Moore, PhD, ATC2 J. Luke Pryor, PhD, ATC, CSCS3 Bhupinder Singh, PhD, PT4

ABSTRACT Background: Prolonged and repetitive overhead use of the arm, such as during the volleyball serve, has been linked to overuse injuries. Purpose: To examine changes in activation of the infraspinatus and lower trapezius following performance of repetitive jump-float serves. Study Design: Descriptive Cohort study. Methods: Six asymptomatic female Division I college volleyball players (age = 19.2±1.1 years, height = 182.9±2.5 cm, weight = 82.1±12.2 kg) performed 87 jump-float serves in 13 intervals of seven serves each on an NCAA regulated indoor volleyball court. Electromyography (EMG) electrodes were connected to TeleMyo DTS wireless sensor with the DTS EMG lead sampling at 1000 Hz. Dependent variables included Median Power Frequency (MPF) of the infraspinatus (IF) and lower trapezius (LT), as well as rating of perceived exertion (RPE), perceptual fatigue measured using the Borg scale, and heart rate (HR). Paired t-tests were performed to examine differences in variables between interval 1 (serves 1-3) and interval 13 (serves 85-87). Pearson’s r Correlation Coefficients were calculated to examine relationships between the dependent variables across all 13 intervals. Results: IF MPF demonstrated a significant and clinically meaningful decrease from interval 1 to interval 13, indicating muscular fatigue. The decrease in LT MPF from interval 1 to interval 13 was not statistically significant, though it met criteria for clinical meaningfulness and was underpowered. RPE and perceptual fatigue were strongly correlated (r = 0.889. p < 0.01) as were RPE and HR (r = 0.679, p <0.01) and HR and fatigue (r = 0.631, p < 0.01). IF MPF was weakly related to LT MPF (r = 0.227, p < 0.05). LT MPF was weakly related to RPE (r = 0.352, p < 0.01), perceptual fatigue (r = 0.313, p < 0.01), and HR (r = 0.322, p < 0.01). Conclusions: Repeated overhead jump-float serves, common in volleyball players, required high effort and induced clinically meaningful muscular fatigue that was not perceived by the participant. Significant changes were observed in IF MPF and percent change and effect size suggest that a meaningful change occurred in LT MPF related to jumpfloat serving. Level of Evidence: 2. Key Words: electromyography, fatigue, glenohumeral joint, movement system, volleyball

Clovis North Educational Center, Clovis, CA, USA Department of Kinesiology, California State University, Fresno, CA, USA 3 Department of Exercise and Nutrition Sciences, University at Buffalo, Buffalo, NY, USA 4 Department of Physical Therapy, California State University, Fresno, CA, USA 2

The authors have no conﬂicts of interest to disclose.

CORRESPONDING AUTHOR Stephanie D. Moore, PhD, ATC Associate Professor Department of Kinesiology California State University, Fresno 5275 N. Campus Dr. M/S SG28 Fresno CA 93711-8018 E-mail: stmoore@csufresno.edu 559-278-0255

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 196 DOI: 10.26603/ijspt20200196

INTRODUCTION Shoulder pain is the third most common musculoskeletal complaint in the general public1 and the third most common overuse pain complaint in professional volleyball players.2 Among volleyball athletes, shoulder injuries resulted in the longest duration of time off from play or practice3 and approximately 42% of injuries occurring during practice and games result in a ten-day loss of participation.4 Although more shoulder injuries are seen in contact sports such as football or wrestling, volleyball consists of more vigorous repetitions of actions involving the shoulder girdle. Significantly greater shoulder abduction and horizontal adduction have been observed in the volleyball overhead arm motion compared to tennis or baseball.5,6 Additionally, the volleyball overhead arm motion elicited an external rotation torque that initiated deceleration immediately following ball contact, which was not reported during the tennis serve or baseball pitch.5 The jump-float serve is the most popular serve among female collegiate volleyball athletes.6-8 It allows the player to place the ball in a specific area of the opponent’s side of the court, instead of trying for maximum speed.8 As the shoulder accelerates the arm through the serving motion, the infraspinatus, teres minor, and posterior deltoid are responsible for the extreme concentric abduction and external rotation, and eccentric deceleration is primarily controlled by the infraspinatus muscle.9,10 Additionally, this type of serve involves a sharp and sudden retraction of the arm after ball contact.7,8 However, both cross-body spikes and float serves produce comparable external rotation torques when decelerating the arm.5 The motion of the float serve performed repetitively may increase muscle fatigue and change posterior shoulder muscle activation.10-13 Increased fatigue due to the repetitive overhead motion leads to altered scapular kinematics which may increase the risk of shoulder injury.11,13 Fatigue may also lead to alterations in muscle activation, however, conflicting reports describe either the infraspinatus or lower trapezius as being the primary muscle to become fatigued during repetitive shoulder elevation and external rotation movements.10,13 Previous authors have examined the effect of fatigue on muscle activation of the infraspinatus and lower trapezius in a

controlled laboratory setting finding the posterior muscles of the shoulder to fatigue after performing the PNF D2 pattern fatigue protocol.10,13 The PNF D2 flexion/extension pattern is very similar to the volleyball jump-float serve with regards to shoulder mechanics and arm motions. In both the PNF D2 extension pattern and serve movements, the upper extremity goes through flexion, abduction, and external rotation during the ascending phase, and extension, adduction, and internal rotation during the descending phase. However, no study has examined muscle activity as the muscles contract throughout the entire serving motion in a practice-like situation. It is unknown whether the data observed in a laboratory are similar to practice-like simulation. The purpose of this study was to examine changes in activation of the infraspinatus and lower trapezius following performance of repetitive jump-float serves. Understanding how muscles of the posterior shoulder and scapula react during the serving motion may help sports medicine and rehabilitation professionals optimize prevention, training, and rehabilitation to address overuse injuries and facilitate recovery. METHODS Participants Six Division I female volleyball athletes participated in this study (age = 19.33 ± 1.03 years, height = 179.07 ± 9.60 cm, weight = 78.62 ± 13.82 kg, five were right arm dominant) after their competitive season. All participants had to have competed in the previous season and had to be asymptomatic. Each participant completed the Penn Shoulder Pain; a score of ≥ 26/30 on the pain subscale and a ≥ 54/60 on the functional subscale was required for inclusion. Exclusion criteria included any shoulder injury resulting in missed practice or events for more than one week in the six months prior to the study, or shoulder surgery in the year prior to the study. All subjects read and signed an informed consent form approved by the California State University, Fresno Institutional Review Board prior to participation in the study. Instrumentation Electromyography (EMG) was used to identify muscle activation amplitude and potential muscle

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Figure 1. Electrode placement for the infraspinatus muscle.

fatigue. Bipolar surface electrodes (MVAP Medical supplies, 1” x 1 7/8”, foam electrode with two snaps and two gel sites, 1 cm space between electrodes) were placed over the infraspinatus and lower trapezius. The portable TeleMyo DTS receiver was connected to the laptop recording device. Four TeleMyo DTS sensors were attached on the participant’s skin near the surface electrodes with Noraxon adhesive tape. Four bipolar recording electrodes were connected to TeleMyo DTS wireless sensor with the DTS EMG lead set. The sampling rate was set at 1000 Hz. All raw myoelectric signals were preamplified with an overall gain of 1000 Hz. The common rejection ratio rate was set at 100 dB and signal-to-noise ratio <1 μV RMS baseline noise. The filter to produce a bandwidth was set at 10-1000 Hz. Electrode Placement and Testing Positions The infraspinatus electrode was placed while the participant’s arm was abducted and externally rotated at 90 degrees. The electrode was located half way between the inferior angle of the scapula and the lateral acromion, 2 cm lateral from the medial border (Fig. 1).14 After electrode placement a clinical test to measure MVIC of the infraspiantus was performed. The participant lay prone on the treatment table with the arm abducted and externally rotated to 90 degrees. The examiner applied pressure on the forearm while rotating the humerus internally.15 The lower trapezius electrode was placed while the participant’s arm was elevated to 120 degrees in the scapular plane. The electrode was located at the

Figure 2. Electrode placement for lower trapezius muscle.

midpoint between the spinous process of T7 and the inferior angle of the scapula (Fig.2).14 After electrode placement a clinical test to measure MVIC of the lower trapezius was performed. The participant lay prone on the treatment table with the arm abducted to 120 degrees with shoulder externally rotated and elbow extended. The examiner applied force to the radial side of the distal forearm as the subject performed horizontal abduction.14

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Procedures All participants were instructed not to participate in heavy lifting 24 hours prior to data collection and to record the time of all physical and weightlifting activities performed 24 hours before data collection to confirm. The skin was cleansed with alcohol and lightly abraded according to SENIAM regulations and procedures.16 This allowed for optimal electrode performance during the testing trials. Electrodes were applied parallel over the muscle bellies of the infraspinatus and lower trapezius. The study took place on an NCAA regulation indoor volleyball court. Following EMG instrumentation, the participants started off with a dynamic warmup routine consisting of four warm-up laps around the gymnasium, shoulder internal and external rotation with a thera-band consisting of 20 repetitions of each, and three minutes of ball hits against the wall. Participants then performed 13 intervals of seven jump-float serves each for a total of 87 jumpfloat serves; the thirteenth interval consisted of only three serves. Data were recorded during the first three serves in each interval. Participants were given a 30-second rest between each interval, during which time three measures were obtained: heart rate (HR), rating of perceived exertion (RPE) experienced in the local muscles, and perceptual fatigue. Heart rate was recorded using a wireless HR monitor strapped around the participant’s chest, electrodes placed beneath breast tissue, and transmitter over the xiphoid process. The participant was then asked to verbally evaluate their rating of perceived exertion (RPE) in the shoulder using the Borg scale of perceived exertion and perceptual fatigue using the fatigue scale. On the Borg scale17, 6 represents no exertion at all and 20 maximal exertion. On the fatigue scale18,19 0 represents no fatigue at all and 10 completely fatigued. Prior to use, subjects were familiarized with both scales. The shoulder was considered to be fatigued when the patient reported ≥18 on the Borg scale of perceived exertion and ≥8 on the fatigue scale.18-20 If the fatigue criteria were not reached, the trial ended when the participant reached 87 serves. Limited data are available regarding the typical number of serves performed in a volleyball practice and the number

likely varies based on institution and coaching philosophy.21 Therefore, this maximum was determined based on an average from observed practices at the author’s institution. Furthermore, Hurd et al21 developed an interval hitting program for female college volleyball players. The final step of each hitting program included the athlete completing between 60-67 total swings depending on position played. Eightyseven represents a 30-33% increase over the number of swings in the final step in the published interval hitting program progression.21 STATISTICAL ANALYSIS Median power frequency (MPF) was calculated for EMG data collected during the first three serves of the first (serves 1-3) and thirteenth (serves 85-87) intervals to be used for comparison. The primary dependent variables examined during this study were MPF of the infraspinatus and lower trapezius. Secondary dependent variables included HR, RPE, and perceptual fatigue. SPSS was used to perform all statistical analyses. Paired t-tests were performed to determine the differences in all dependent variables between serving interval 1 (serves 1-3) and interval 13 (serves 85-87). Percent change in MPF was calculated as the difference in MPF between interval 1 and 13 divided by the MPF at interval 1. A decrease of ≥ 8% in MPF was used as an indicator of significant local muscle fatigue.13 Additionally, Pearson’s r Correlation Coefficients were calculated to examine relationships between the dependent variables. Cohen’s d calculation was used to determine effect size. A priori α ≤ 0.05. RESULTS All participants completed 87 serves; none were stopped early due to meeting fatigue criteria described. Results of the paired t-Tests are provided in Table 1. Comparison of infraspinatus MPF between serving interval 1 and serving interval 13 showed a statistically and clinically significant decrease in muscle activation (mean percent change 20.7 ± 19.3%), t(1,5) = 2.82, p = 0.037, d = 1.05, surpassing the 8% indicator of local muscle fatigue. Comparison of lower trapezius MPF between serving interval 1 and serving interval 13 showed a clinically significant decrease in muscle activation (14.9 ± 21.1%) that exceeds the indicator of local muscle

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Table 1. Descriptive statistics.

Table 2. Pearson correlation coefﬁcients.

fatigue and effect size exceeding Cohen’s22 convention for a large effect, but this difference was not statistically significant, t(1,5) = 1.817, p = 0.129, d = 0.83. Post-hoc power for this comparison was calculated to be 26%, indicating insufficient statistical power. Pearson’s correlation coefficients are presented in Table 2. Heart rate, RPE, and perceptual fatigue were all strongly correlated. Infraspinatus MPF was weakly related to lower trapezius MPF but no reliable correlation was observed with any other variable. Lower trapezius MPF was weakly related to RPE, perceptual fatigue, and HR. DISCUSSION The purpose of this study was to examine changes in activation of the infraspinatus and lower trapezius muscles following performance of repetitive jumpfloat serves in a practice-like setting. This study used a PNF D2 pattern that had been examined in previous research10,13 and assessed it in a practical setting with an athletic population to determine if infraspinatus and lower trapezius muscular activation during a jump-float serve would respond in a similar manner.

In the present study, statistically significant and clinically meaningful local muscle fatigue of the infraspinatus was observed following 87 jump-float serves. Previous research has produced conflicting results. These findings support those of Ebaugh et al13 who reported a 21.5% decrease in infraspinatus MPF following a fatigue protocol that included PNF D2 pattern. However, Joshi et al10,13 did not observe fatigue of the infraspinatus during the PNF D2 pattern following an external rotation fatiguing protocol as measured by Average Root Mean Square (%MVIC). Local muscle fatigue of the lower trapezius was observed and is supported by Cohen’s d effect size and percent change, but was not statistically significant; however, due to low statistical power for this comparison, caution must be used with the interpretation of these data. Previous research has produced conflicting results. Ebaugh et al13 did not report fatigue of the lower trapezius as a result of their fatigue protocol while Joshi et al10 observed fatigue of the lower trapezius during the PNF D2 pattern following their external rotation fatiguing protocol. Small differences in methodology and data reduction may contribute to the differing results among studies. The fatigue protocol used by Ebaugh et al13 included repetitive elevation in PNF D2 flexion pattern along with repetitive elevation in the scapular plane and manipulation of small objects. Joshi et al10 implemented a fatigue protocol consisting of external rotation of the glenohumeral joint at 90 degrees with weight and used the PNF D2 pattern for collection of EMG data only. While one study13 utilized the PNF D2 pattern for the fatigue protocol and another10 utilized the PNF D2 pattern to collect EMG data, the present study used the jump-float serves themselves (as a replication of PNF D2 pattern) to both

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fatigue the muscles and collect EMG data. Finally, the present study and Ebaugh et al reported MPF, while Joshi et al reported Average RMS (% MVIC). MPF is a common procedure used for evaluation of frequency shift associated with local muscle fatigue, while MVIC looks more at the maximal isometric force generation.

break may mimic that experienced in game situations. This would allow the participants to feel adequately recovered before the next bout of serves began. Regardless, reductions in MPF in the infraspinatus and lower trapezius muscles were observed suggesting that local muscle fatigue did in fact take place.

Heart rate, RPE, and perceptual fatigue were moderately to strongly positively correlated. This was a surprising finding since RPE and fatigue were assessed specifically related to sensations arising from the active shoulder and not assessment of whole-body responses to exercise as such scales are typically utilized. It may be that, despite instruction, subjects could not disassociate RPE and fatigue perceptions from whole body sensations after exercise. Alternatively, RPE and fatigue (assessed specific to the active shoulder) demonstrated the most robust relationship (r = 0.889, p < 0.01) suggesting some similarity between localized assessments. Furthermore, after the 87 serves, moderate levels of perceived exertion (12/20) and fatigue (4/10) were observed whereas HR (an indicator of whole-body exercise strain) averaged 78% of age-predicted HR maximum. Participantsâ&#x20AC;&#x2122; ratings on the Borg scale indicate moderate intensity,23 while their HR response is defined as vigorous physical activity according to the American College of Sports Medicine thresholds.20 Muscle activation of the infraspinatus and lower trapezius decreased by 20.6% and 18.3%, respectively, at this time point. The greater relative HR response to this exercise bout compared to the moderate fatigue responses at the shoulder may be due to the sport specific training of the subjects.

These data support that the posterior muscles of these athletes experienced local muscle fatigue within the first 30-minutes of a typical two-hour practice. However, the RPE and perceptual fatigue values reported indicate the athletes were unable to perceive this fatigue and, under normal conditions, would continue to practice in this impaired condition. It may be advantageous to implement strategies to mitigate or attenuate this fatigue in order to perfect motor patterns and avoid overuse injuries. Some strategies are to schedule shorter bouts of practice or to intersperse or â&#x20AC;&#x153;supersetâ&#x20AC;? lower body exercises or footwork drills between overhead volleyball drills.24,25 These strategies may allow for more time in between training protocols for the posterior shoulder muscles to adequately recover before the next bout of overhead activity begins.

The participants in this study were well trained Division I volleyball players with conditioning intervals geared toward replicating the anaerobic demands of volleyball. Completion of the protocol, including 87 serves and rest intervals, lasted for about 30 to 35 minutes; a typical practice for a NCAA Division I college volleyball team is about two hours. Because these participants perform serves at high repetitions on a daily basis, the fatiguing protocol simply may not have been demanding or long enough to cause DI volleyball athletes to perceptually gauge the protocol as taxing or requiring high exertion. Furthermore, the short bouts of activity and the 30-second

There are a few limitations in the present study that should be acknowledged. First, every participant was allowed to bounce the volleyball in between serves, but no more than two bounces, in order to eliminate unnecessary EMG noise. This study was underpowered for analysis of the lower trapezius muscle. The post-hoc statistical power for the t-test performed on the lower trapezius was 26%, thus, future studies should recruit multiple teams to allow for a larger pool of participants and also examine muscle activation between male and female collegiate volleyball athletes. Additionally, shoulder mechanics should be evaluated pre- and post-fatigue trial to monitor any significant mechanical changes they may be caused by the fatiguing protocol. Future studies should examine how muscle activation changes with increased activity time, and could include blood lactate measurements to better determine exertion, level of activity, and fitness level of participants. CONCLUSION The results of the current study offer insight into how the posterior shoulder muscles respond to

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repetitive overhead volleyball serves. EMG data demonstrate statistically significant and clinically meaningful muscular fatigue of the infraspinatus, while overall fatigue was not detected using traditional assessments of fatigue including HR, Borg RPE, and a fatigue scale. Sports Medicine clinicians and coaches should consider this when designing practices. Future research is needed to better understand the effects of local muscle fatigue and compensations of the posterior shoulder muscles in a larger sample. REFERENCES 1. Bernhardsson S, Klintberg IH, Wendt GK. Evaluation of an exercise concept focusing on eccentric strength training of the rotator cuff for patients with subacromial impingement syndrome. Clin Rehabil. 2011;25(1):69-78. 2. Bahr R, Reeser JC. Injuries among world-class professional beach volleyball players: The fédération internationale de volleyball beach volleyball injury study. Am J Sports Med. 2003;31(1):119-125. 3. Verhagen E, Van der Beek AJ, Bouter L, et al. A one season prospective cohort study of volleyball injuries. Br J Sports Med. 2004;38(4):477-481. 4. Agel J, Palmieri-Smith RM, Dick R, et al. Descriptive epidemiology of collegiate women’s volleyball injuries: National collegiate athletic association injury surveillance system, 1988-1989 through 2003-2004. J Athl Train. 2007;42(2):295. 5. Reeser JC, Fleisig GS, Cools AM, et al. Biomechanical insights into the aetiology of infraspinatus syndrome. Br J Sports Med. 2012;47(4):239-244.

11. Tsai N-T, McClure PW, Karduna AR. Effects of muscle fatigue on 3-dimensional scapular kinematics. Arch Phys Med Rehabil. 2003;84(7):1000-1005. 12. McQuade KJ, Dawson J, Smidt GL. Scapulothoracic muscle fatique associated with alterations in scapulohumeral rhythm kinematics during maximum resistive shoulder elevation. J Orthop Sports Phys Ther. 1998;28(2):74-80. 13. Ebaugh DD, McClure PW, Karduna AR. Effects of shoulder muscle fatigue caused by repetitive overhead activities on scapulothoracic and glenohumeral kinematics. J Electromyogr Kinesiol. 2006;16(3):224-235. 14. Seitz AL, Uhl TL. Reliability and minimal detectable change in scapulothoracic neuromuscular activity. J Electromyogr Kinesiol. 2012;22(6):968-974. 15. Kendall FP, McCreary EK, Provance PG, et al. Muscles testing and function. Baltimore: Williams and Wilkins; 1993. 16. Hermens D, Freriks B. Surface electromyography for the non-invasive assessment of muscles (seniam). Brussels; 2005. 17. Borg G. Psychophysical scaling with applications in physical work and the perception of exertion. Scand J Work Environ Health. 1990:55-58. 18. Micklewright D, Gibson ASC, Gladwell V, et al. Development and validity of the rating-of-fatigue scale. Sports Med. 2017;47(11):2375-2393. 19. Whittaker RL, La Delfa NJ, Dickerson CR. Algorithmically detectable directional changes in upper extremity motion indicate substantial myoelectric shoulder muscle fatigue during a repetitive manual task. Ergonomics. 2019;62(3):431-443. 20. ACSM. Acsm’s guidelines for exercise testing and prescription. 10th ed ed. Philadephia: Wolters Kluwer; 2016.

6. Reeser JC, Fleisig GS, Bolt B, et al. Upper limb biomechanics during the volleyball serve and spike. Sports Health. 2010;2(5):368-374.

21. Hurd W, Hunter-Giordano A, Axe M, et al. Databased interval hitting program for female college volleyball players. Sports Health. 2009;1(6):522-530.

7. Ferretti A, Cerullo G, Russo G. Suprascapular neuropathy in volleyball players. J Bone Joint Surg Am. 1987;69(2):260-263.

22. Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. New Jersey: Lawrence Erlbaum Associates, Inc; 1988.

8. Ferretti A, De Carli A, Fontana M. Injury of the suprascapular nerve at the spinoglenoid notch. Am J Sports Med. 1998;26(6):759-763.

23. Smutok MA, Skrinar GS, Pandolf KB. Exercise intensity: Subjective regulation by perceived exertion. Arch Phys Med Rehabil. 1980;61(12):569-574.

9. Rokito AS, Jobe FW, Pink MM, et al. Electromyographic analysis of shoulder function during the volleyball serve and spike. J Shoulder Elbow Surg. 1998;7(3):256-263.

24. Río-Rodríguez D, Iglesias-Soler E, del Olmo MF. Set conﬁguration in resistance exercise: Muscle fatigue and cardiovascular effects. PloS one. 2016;11(3):e0151163.

10. Joshi M, Thigpen CA, Bunn K, et al. Shoulder external rotation fatigue and scapular muscle activation and kinematics in overhead athletes. J Athl Train. 2011;46(4):349-357.

25. Myers JB, Guskiewicz KM, Schneider RA, et al. Proprioception and neuromuscular control of the shoulder after muscle fatigue. J Athl Train. 1999;34(4):362.

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ORIGINAL RESEARCH

TEST-RETEST RELIABILITY OF THE CLOSED KINETIC CHAIN UPPER EXTREMITY STABILITY TEST (CKCUEST) IN A MODIFIED TEST POSITION IN DIVISION I COLLEGIATE BASKETBALL PLAYERS Kayla Hollstadt, PT, DPT, OCS1 Mark Boland, PT, DPT, OCS, MBA1,2 Ivan Mulligan, PT, DSc, SCS, ATC, CSCS1,2

ABSTRACT Background: The closed kinetic chain upper extremity stability test (CKCUEST) as originally described may not be appropriate for assessing athletes interchangeably considering body size variations. A modified test position may be warranted to normalize the CKCUEST to body size, in order to reflect an accurate representation of upper limb function. Purpose: To determine test-retest reliability of the CKCUEST in a modified test position in Division I collegiate basketball players. Study Design: Test-retest reliability Methods: 15 subjects (8 male, 7 female) were recruited from Division I basketball teams. Subjects began in a push-up position with their hands located directly under their shoulders. Subjects performed one 15 second trial of the modified CKCUEST initially and a second trial one week later. Hand-written data was transferred to a spreadsheet for analysis using Minitab Statistical Software for comparison. Results: Test-retest reliability was 0.88 for men’s basketball, 0.79 for women’s basketball, and 0.90 when both teams were combined. Test mean for men’s basketball were 29.5 ± 4.78, and retest mean were 31.88 ± 4.99. Test mean for women’s basketball were 24.86 ±5.52, and retest mean were 26.71 ± 5.41. Test mean for both teams combined were 27.33 ± 5.5, and retest mean were 29.47 ± 5.67. Conclusions: The CKCUEST in a modified test position is a reliable assessment tool. Results support previous findings and may contribute to injury prevention and return to sport decision-making. Level of Evidence: 3b Keywords: College athletes, functional testing, movement system, upper extremity

1 2

DiSepio Institute for Rural Health & Wellness Loretto, PA Saint Francis University Department of Physical Therapy Loretto, PA

The authors of this study declare no conﬂicts of interest.

CORRESPONDING AUTHOR Kayla Hollstadt 14000 N 94th St Unit 1169 Scottsdale, AZ 85260 612-226-1235 E-mail: Kaylamhvassallo@gmail.com

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 203 DOI: 10.26603/ijspt20200203

INTRODUCTION The Closed Kinetic Chain Upper Extremity Stability Test (CKCUEST) was developed by clinicians in order to provide a functional testing measure for the upper extremity. Clinicians wanted a test that would help them determine an athleteâ&#x20AC;&#x2122;s readiness to return to sport or need to continue further physical therapy treatment.1 The CKCUEST is commonly utilized in todayâ&#x20AC;&#x2122;s clinical practice as it is cost-efficient, simple to prepare and administer, and is a reliable assessment tool for varying patient populations.1,2 However, the CKCUEST as originally described by Goldbeck and Davies may not be appropriate for assessing all athletes interchangeably.2-4 In the original test procedure all participants began the test with their hands touching parallel pieces of tape that were placed 36 inches apart.1 This did not account for variability in shoulder width and/or arm length. As the athletic population ranges in body-build, age, gender, and type of sport they participate in, Taylor et al. determined that narrower shoulder width and/ or shorter arm length placed athletes at a disadvantage when performing the original CKCUEST.4 This was attributed to increased effort needed to stabilize the upper body and trunk in order to maintain the arms at a distance of 36 inches apart.4 Thus a modified test position was determined and was described by placing the upper extremities in a push-up position with hands located directly under the shoulders to begin the test.4 The parallel pieces of tape remain 36 inches apart, however these serve only as markers for cross-body reaches. The modified CKCUEST has demonstrated good test-retest, interrater reliability, and precision, and the authors established normative reference values pertaining to Division I athletes considering sport, gender, and age.4 Multiple studies have reported excellent test-retest reliability for the CKCUEST in the original test position across many populations as used to measure stability and power of the upper extremities.1,5-7 Goldbeck and Davies reported test-retest reliability in collegiate males.1 Sciascia and Uhl reported testretest reliability in young adults averaging 30 years of age with shoulder pain and in young adults averaging 29 years of age without shoulder pain respectively.8 Tucci et al. reported test-retest reliability in subjects with and without subacromial impingement

comparing intersession and intrasession reliability respectively.5 Lee and Kim. reported test-retest reliability in healthy Korean adults averaging 29.96 years of age, and Oliveira et al. reported test-retest reliability in healthy adolescents averaging 16.9 years of age.2,7 Currently there is only one study that has reported test-retest reliability for the CKCUEST in the modified test position specific to collegiate club sport athletes, by Tarara et al.9 Multiple authors have reported normative reference values for the CKCUEST in the original test position across various populations, but few have reported normative reference values in the modified test position. In the original test position Goldbeck and Davies determined a test reference value in collegiate males.1 Tucci et al. determined test-retest reference values in sedentary males, in active males, in males with subacromial impingement, in sedentary females, in active females, and in females with subacromial impingement.5 Lee and Kim determined test-retest reference values in healthy Korean adults averaging 29.96 years of age.7 Oliveira et al. determined test-retest reference values in healthy adolescents averaging 16.9 years of age.2 Rousch et al. determined a test reference value in male collegiate baseball players,11 and Botnmark et al. determined a test reference value in healthy young adults averaging 26.1 years of age.12 Currently only one study has reported normative reference values for the CKCUEST in a modified test position. Taylor et al.4 determined a test reference value for both male and female Division I collegiate athletes including basketball, baseball, lacrosse, track and field, cross country running, volleyball, and soccer. The authors also determined reference values specific to sport and provided demographic and descriptive subject data that may be used to determine reference values specific to age, height, and weight.4 However, evidence regarding the modified test position is still limited. Further research is warranted to support the findings determined by Taylor et al. and to provide additional evidence to support the use of a modified test position in clinical rehabilitation. Thus, the purpose of the current study was to determine test-retest reliability of the CKCUEST in a

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modified test position in Division I collegiate basketball players. As functional tests continue to develop and discrepancies in the original procedures ensue, reliability must be examined. This is to ensure accuracy when using these assessment tools to measure progress of each patient. Results of the study will be compared to normative reference values established by Taylor et al. and other studies in order to examine the current findings with specific consideration to test position and higher-level athletes. With additional evidence, clinicians may have more confidence when using the modified CKCUEST to assess an athlete’s performance relative to others. This may help to identify specific upper extremity joint stability, proprioception, and kinesthesia deficits to target during training or may contribute to return to play decision-making. METHODS Participants Participants were recruited from NCAA Division I basketball teams during the summer semester at the authors’ institution. The prospective study was presented to each team following a scheduled practice. 15 basketball players (8 male, 7 female) agreed to participate in the study. Athletes were included if they were 18 years of age or older, an NCAA Division I basketball player, and if they had access to a phone or computer for purposes of communication. Athletes were excluded if they were less than 18 years of age, had experienced pain or an acute injury to their upper extremity in the previous six weeks, had undergone general surgery in the previous six weeks, had undergone surgery to their upper extremity within the previous year, or were restricted from sport participation by their team physician. Exclusion criteria were determined to avoid potential risk for injury or limitation in the ability to perform the CKCUEST in a modified

test position. Athletes who voluntarily agreed to participate in the study provided written informed consent, which was approved by the Institutional Review Board at Saint Francis University. Testing Methods Participants were tested and retested with their team following a men’s basketball recovery practice or prior to a women’s basketball lifting practice. Both practices were typical for off-season training programs conducted during the summer semester. Prior to the first testing session, demographic and anthropometric data pertaining to gender, age, sport, height, weight, and arm length was collected (Table 1) and followed by a description of the test. The principal and co-investigator conducted the test. Each possessed clinical experience with Division I athletes and use of functional performance testing. A verbal and demonstrated description of the test was provided by the principal investigator. Only one trial was performed at each of the two testing sessions, which were conducted approximately one week apart. Data was collected and organized using an intake data sheet, and was later hand-entered into a Microsoft Excel spreadsheet. The Modiﬁed CKCUEST The CKCUEST in a modified test position described by Taylor et al. was utilized for this study. Two pieces of tape were placed 36 inches apart and made parallel to each other on the floor, as described in previous studies.1,3-4 Participants were instructed to start in a push-up position with their hands located directly under their shoulders (Figure 1a).4 This is a modification to the original test position, where participants began with their hands touching the parallel pieces of tape 36 inches apart.1,3 The CKCUEST in a modified test position normalizes placement of the upper extremities to each Participant, thus accounting for variability among athletic populations.4 Start

Table 1. Demographic characteristics means (standard deviation) of the total sample and stratiﬁed by team.

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Figure 1. (A) Absolute number of ACL injuries that occurred within each quarter of a game separated by sport. (B) Percentage of ACL injuries that occurred within each quarter of a game separated by sport.

Table 2. Mean (standard deviation) and test-retest reliability of the Closed Kinetic Chain Upper-Extremity Stability Test (CKCUEST)

positon was approved by the tester followed by a verbal cue to begin the test. Participants completed cross-body reaches alternating each hand to the contralateral piece of tape as quickly as possible during a 15 second trial (Figure 1b). Scores reflect the total number of cross-body reaches to each piece of tape using both hands. Statistical analysis Data were entered into a Microsoft Excel spreadsheet for organization prior to using Minitab Statistical Software (Minitab, Inc. State College, PA) for analysis. Male basketball players, female basketball players, and both teams combined were assessed using a Spearman Rho correlation to determine reliability of test and retest scores to account for a smaller population size. Descriptive statistics were used to assess demographics and anthropometric data, and to compare scores of the CKCUEST in a modified test position to male players, female players, and both teams combined (Table 2).

RESULTS Participants Men’s and women’s basketball players were recruited following a scheduled practice. Men’s basketball players were tested and retested following a practice and women’s basketball players were tested and retested prior to a practice. Retests were completed one week apart. Two participants that met inclusion criteria and completed testing session one were removed from the study as scheduling conflicts prevented them from participating in testing session two. Test Results Test-retest reliability was 0.88 for men’s basketball, 0.79 for women’s basketball, and 0.90 when both teams were combined. The test mean for men’s basketball was 29.5 touches with a standard deviation of 4.78, and the retest scores had a mean of 31.88 touches with a standard deviation of 4.99. The test

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mean for womenâ&#x20AC;&#x2122;s basketball was 24.86 touches with a standard deviation of 5.52, and the retest scores had a mean of 26.71 touches with a standard deviation of 5.41. For both teams combined, the test mean was 27.33 touches with a standard deviation of 5.5, and the retest score had a mean of 29.47 touches with a standard deviation of 5.67. DISCUSSION This study was conducted to assess test-retest reliability of the CKCUEST in a modified test position of NCAA Division I collegiate basketball players. In addition to comparing results to normative reference values for the modified position established by Taylor et al. this study adds to the evidence that supports the potential use of a modified test position for the CKCUEST compared to the original description. Previous studies have developed normative reference values for the CKCUEST, however work by Taylor et al. is the only to utilize a modified test position and to establish normative reference values specific to male and female NCAA Division I collegiate athletes. As gender, sport, and skill impact performance, it is important to utilize the same testing procedures and normative reference data that are specific to the population being assessed. Thus, further research is warranted to establish the reliability of the CKCUEST in a modified test position, and to support normative reference values specific to higher-level athletes proposed by Taylor et al. This may improve use of the test as an injury predictor during baseline testing and as a sideline screen, or to determine readiness for return to play.1,4 Previous authors have reported test-retest reliability of the CKCUEST as originally described, and have demonstrated excellent reliability between sessions.1,5-7 Goldbeck and Davies created the CKCUEST as originally described to evaluate the upper extremity comparable to closed kinetic chain interventions and sport-specific demands.1 They determined an ICC of 0.92 reflecting the average score in collegiate males.1 Sciascia and Uhl determined an ICC of 0.86 and 0.85 reflecting the average score in young adults averaging 30 years of age with shoulder pain and in young adults averaging 29 years of age without shoulder pain respectively.8 Tucci et al. determined an ICC range between 0.85 to 0.96, reflecting the average score in subjects with and without subacromial

impingement.5 Lee and Kim determined an ICC of 0.97 reflecting the average score in healthy Korean adults, and Oliveira et al. reported an ICC of 0.680.87 reflecting the average score in healthy adolescents averaging 16.9 years of age.2,7 Currently only the study by Tarara et al has reported test-retest reliability for the CKCUEST in a modified test position, who reported an ICC of 0.73 in collegiate club sport athletes.9 Previous authors have reported normative reference values for the CKCUEST; however, results vary due to population, test position, number of trials performed, and number of sessions performed. In the original test position Goldbeck and Davies determined 27.8 touches as a test reference value in collegiate males.1 Tucci et al. determined 22.67 and 25.30 touches as test-retest reference values in sedentary males, 27.97 and 31.97 touches in active males, 10.10 and 11.82 touches in males with subacromial impingement, 24.58 and 28.47 touches in sedentary females, 24.78 and 27.13 touches in active females, and 12.20 and 13.73 touches in females with subacromial impingement.5 Lee and Kim determined 13.31 and 13.10 touches as test-retest reference values in healthy Korean adults averaging 29.96 years of age.7 Oliveira et al. determined 25.6 and 28 touches as test-retest reference values in healthy adolescents averaging 16.9 years of age.2 Rousch et al. determined 30.41 touches as a test reference value in male collegiate baseball players.11 Botnmark et al. determined 19.9 touches as a test reference value in healthy young adults averaging 26.1 years of age, and Hegedus et al. determined 27.8 touches as a test reference value in general college males.12,13 In the current study menâ&#x20AC;&#x2122;s basketball demonstrated 29.5 and 31.88 touches as test-retest reference values, and womenâ&#x20AC;&#x2122;s basketball demonstrated 24.86 and 26.71 touches as test-retest reference values. In the current findings, the retest values exceeded the initial test values in both groups which was consistent with other authors findings.2,5,7 This may be attributed to a small learning effect which may need to be taken into consideration when implementing the test. Currently only one study has reported normative reference values for the CKCUEST in a modified test position. Taylor et al. determined 25.0 and

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22.9 touches as a test reference values for male and female Division I collegiate athletes respectively. 4-7,13 The CKCUEST as originally described was adjusted to body size by instructing participants to place hands directly underneath their shoulders, in a push-up position, and to complete across-body reaches to each piece of tape marked 36 inches apart. This modification was suggested in order to reduce excessive stabilization efforts experienced by athletes small in stature and/or with a narrow build, thereby eliminating any disadvantage due to body size.4 Their results indicated comparable outcomes to previous studies, however it was noted that women scored higher in the modified test position compared to the original test position.4 To ensure consistency and to minimize a learning effect, participants in the current study were instructed to perform one trial per each of the two testing sessions as implemented in the study by Taylor et al.4 This is different from the original procedure described by Goldbeck and Davies which included a warm-up trial prior to three scored trials. The average of the three trials is the recorded score.12,5-6 Due to variations in the way the CKCUEST is implemented, the current results may not compare to the all reference values that are available. Results of the current study including (test-retest values for men’s basketball as 29.5 and 31.88 touches; women’s basketball as 24.86 and 26.71 touches) are comparable to previous studies that reported testretest reliability and/or normative reference values of the CKCUEST in both the original and modified test position. Although prior studies vary in start position, population, and scoring, results of the current study regarding test-retest reliability compared closely to studies conducted by Goldbeck and Davies in the original test position determining 27.8 touches as a test reference value in collegiate males and Tarara et al. in a modified test position determining an ICC of 0.73 in collegiate club sport athletes.9 Test and retest means for both Saint Francis University’s men’s and women’s basketball teams compared closely to normative reference values determined by Tucci et al. for active males and active females. Saint Francis University’s men’s basketball scores compared closely to reference values determined by Taylor et al. for male Division I athletes and Roush

et al. for collegiate baseball players. However, Saint Francis University’s men’s basketball scores were higher when compared to reference values determined by Taylor et al. for men’s basketball players. Women’s scores compared closely to reference values determined by Taylor et al. specific to women’s basketball players and female Division I athletes overall. Thus, results of the current study support the current evidence regarding the CKCUEST and its implementation in clinical practice to assess upper extremity function. In addition, results of the current study support the use of a modified test position as a measure to normalize the CKCUEST to body size, which may prove to be a useful alternative when administering the CKCUEST to injured and/or higher-level athletes. Limitations A small number of subjects were included in the study, and the CKCUEST as performed with the modifications in the start position may differ in how the athlete performs the reaching/returning task. CONCLUSIONS The results of the current study demonstrate that the CKCUEST in a modified test position is a reliable assessment tool. Using a modified testing position may be advantageous for athletes who are small in stature or have a narrow-shouldered body build. It may prove to be a useful alternative to the traditional test for assessing athletes in order to gain a representation of an athlete’s abilities. The testing procedures used in the current study demonstrated consistent results compared to recent findings and established normative values specific to Division I collegiate athletes. The CKCUEST is easy to set up and administer, and may be used as an injury screen, to identify progress made in rehabilitation, and to assist in return to sport decision-making. REFERENCES 1. Goldbeck TG, Davies GJ. Test-retest reliability of the closed kinetic chain upper extremity stability test: a clinical ﬁeld test. J Sports Rehabil. 2000;9:35-45. 2. Oliveira VMA, Pitangui ACR, Nascimento VYS, et al. Test-retest reliability of the closed kinetic chain upper extremity stability test in adolescents: reliability of CKCUEST in adolescents. Int J Sports Phys Ther. 2017;12:125-132.

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3. Davies GJ, Zillmer DA. Functional progression of a patient through a rehabilitation program. Orthop Phys Ther Clinics North Am, 2000;9:103-118. 4. Taylor JB, Wright AA, Smoliga JM, et al. Upper extremity physical performance tests in collegiate athletes. J Sports Rehabil. 2016;25(2):164-54. 5. Tucci HT, Martins J, Sposit GC, et al. Closed kinetic chain upper extremity stability test (CKCUES test): a reliability study in persons with and without shoulder impingement syndrome. BMC Musculoskelet Disord. 2014;15(1):1-9. 6. Tucci HT, Felicio LR, McQuade KJ, et al. Biomechanical analysis off closed kinetic chain upper extremity stability test. J Sports Rehabil. 2016;24:1-27. 7. Lee DR, Kim LJ. Reliability and validity of the closed kinetic chain upper extremity stability test. J Phys Ther Sci. 2015;27:1071-1073. 8. Sciascia A, Uhl TL. Reliability of strength and performance testing measures and their ability to differentiate persons with and without shoulder symptoms. Int J Sports Phys Ther. 2015;5:655-666. 9. Tarara DT, Hegedus EJ, Taylor JB. Real-time testretest and interrater reliability of select physical performance measures in physically active collegeaged student. Int J Sports Phys Ther. 2014;9:874-887. 10. Snyder J. Closed kinetic chain upper extremity stability test. John Snyder, DPT. https:// johnsnyderdpt.com/for-clinicians/functionaltesting/closed-kinetic-chain-upper-extremitystability-test/. Accessed March 1, 2017. 11. Rousch JR, Kitamura J, Waits MC. Reference values for the closed kinetic chain upper extremity stability test (CKCUEST) for collegiate baseball players. N Am J Sports Phys Ther. 2007;2(3):159-63.

12. Botnmark I, Tumilty S, Mani R. Tactile acuity, body schema integrity and physical performance of the shoulder: a cross-sectional study. Musc Sci Practice. 2016;23:9-16. 13. Hegedus EJ, Vidt ME, Tarara DT. The best combination of physical performance and self-report measures to capture function in three patient groups. Phys Ther Reviews. 2014; 19(3):196-203. 14. Westrick RB, Miller JM, Carow SD, Gerber JP. Exploration of the Y-balance Test for assessment of upper quarter closed kinetic chain performance. Int J Sports Phys Ther. 2012;7:139-147. 15. Ellenbecker T, Manske RM Davies G. Closed kinetic chain testing techniques of the upper extremities. Orthop Phys Ther Clin N Am. 2000;9:219-229. 16. Pontillo M, Spinelli BA, Sennet BJ. Prediction of inseason shoulder injury from preseason testing in division I collegiate football players. Sports Heath. 2014;6:497-503. 17. Negrete RJ, Hanney WJ, Kobler MJ, et al. Reliability minimal detectable change, and normative values for tests of upper extremity function and power. J Strength Cond Res. 2010;24:3318-3325. 18. Negrete RJ, Hanney WJ, Kolber MJ, Davies GJ, Reinmann B. Can upper extremity functional tests predict the softball throw for distance: a predictive validity investigation. Int J Sports Phys Ther. 2011;6:104-111. 19. Davies GJ. The need for critical thinking in rehabilitation. J Sports Rehabil. 1995;4:1-22. 20. Borsa PA, Lephart SM, Kocher MS, Lephart SP. Functional assessment and rehabilitation of shoulder proprioception for glenohumeral instability. J Sport Rehabil. 1994;3:84-104.

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ORIGINAL RESEARCH

COMPARISON OF CRYOTHERAPY MODALITY APPLICATION OVER THE ANTERIOR THIGH ACROSS RUGBY UNION POSITIONS; A CROSSOVER RANDOMIZED CONTROLLED TRIAL. Jill Alexander MSc1 Dr David Rhodes PhD2 Daniel Birdsall BSc1 Prof. James Selfe DSc3

ABSTRACT Background: In deliberation of the diverse physical traits of rugby union and the known interference adipose tissue has on the ability to cool deeper tissues, evidence is required to understand the effect of cryotherapy modalities to provide optimum outcomes post-injury. Purpose: To investigate differences in the cooling ability of three different cryotherapy modalities in a rugby union population in an attempt to describe optimum cooling protocols for the anterior thigh. Study Design: Within-subjects randomized control crossover. Methods: Twenty-one healthy male rugby union players took part. Skin surface temperature measured via thermal imaging camera (ThermoVision A40M, Flir Systems, Danderyd, Sweden) alongside Thermal Comfort and Sensation questionnaires following interventions of either Wetted Ice (WI), Crushed Ice (CI) applied in a polythene bag secured by plastic wrap, or CryoCuff® (CC), applied for 20-minutes over the anterior thigh. Participants were grouped by their typical playing position for the sport of rugby union; i.e. forwards and backs. Results: Significant differences (p=<0.05) in Tsk for all modalities compared to baseline and comparing post Tsk between CI and CC (p=0.01) and WI to CC (p=0.01) were displayed. Significantly greater reductions in Tsk noted immediately-post in the ‘forwards’ group (p=≤0.05) compared to the ‘backs’ group for, all modalities (p=≤0.05). Thermal Comfort and Sensation scores demonstrated significant changes baseline compared to post for all modalities (p=<0.05). No significant differences were found when comparing between modalities for Thermal Comfort (p=0.755) or Sensation (p=0.225) for whole group or between positional groups. Conclusions: Physiological responses to cooling differed across modalities with WI producing the greatest decrease in Tsk. Significant variability in Tsk was also displayed between positional factions. Results uphold the importance of the individualization of local cooling protocols when considering physical traits and characteristics within a rugby union population. Findings provide further understanding of the physiological responses to cooling through Tsk quantification in specific populations, helping to guide sports medicine practitioners on optimal cooling application development in sport. Level of Evidence: Level 2b Keywords: Cryotherapy, Rugby Union, Thermal Imaging, Movement System

University of Central Lancashire, School of Sport and Health Sciences, Preston, Lancashire, UK. 2 Institute of Coaching and Performance (ICaP), University of Central Lancashire, School of Sport and Health Sciences, Preston, Lancashire, UK. 3 Manchester Metropolitan University, Faculty of Health, Psychology and Social Care, Manchester, UK. The authors report no conﬂicts of interest.

CORRESPONDING AUTHOR Jill Alexander, MSc University of Central Lancashire School of Sport and Health Sciences Preston, Lancashire, PR1 2HE United Kingdom E-mail: JAlexander3@uclan.ac.uk

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 210 DOI: 10.26603/ijspt20200210

INTRODUCTION Selection and application of cryotherapeutic modalities in sport vary, with optimum exposure protocols still under debate in practice when considering clinical effectiveness and thermodynamics.1,2,3,4 Common cooling modalities include ice variations such as crushed, flaked, cubed, and wetted (typically crushed ice mixed with water); ice packs, gel packs, cold sprays, frozen peas, cryotherapy cuffs (CryoCuff®) and coldwater immersion.2,5,6,7 Modalities are often applied via several methods for example with or without compression adjuncts. No definitive consensus is available on individual parameters of optimal cooling applications, either clinically or applicable to pitch side injury. Understanding the implications of different local cooling exposures are imperative to the management of sports injuries,5,8 with inadequate treatment paradigms being potentially detrimental to recovery timelines.4 Key cellular and physiological changes following cryotherapy are well reported through the of heat extraction from the body to achieve therapeutic effects.1,9,10,11 This includes an analgesic response and reductions in nerve conduction velocity,10 metabolism and inflammation.9 The efﬁcacy of cryotherapy is often investigated through quantification of skin surface temperature (Tsk), via thermal imaging.6,7,12,13,14 To what extent cryotherapy alters temperature of deep muscle tissue is of clinical importance and interest in the literature.1,15 Although previously argued that Tsk was a weak predictor of deeper tissue temperatures,1 subsequent research presented a significant quadratic relationship between Tsk and intramuscular temperature (Tim).3 This developed knowledge regarding the physiological effects of cooling in areas other than Tsk relevant to cryotherapy applications in sport. Thermodynamic properties of cryotherapy modalities are reported with differences noted between the cooling abilities of crushed ice, wetted ice, and gel packs.16 Further differences between frozen peas, crushed ice, gel packs, and ice-water immersion are also reported.2 In addition, it has been suggested that pre-application modality temperatures do not influence the effectiveness of a cryotherapeutic modality in terms of Tsk reduction, however discerning the type of modality to be used with consideration of other variables in clinical decision-making is necessary.2 The magnitude of soft tissue temperature change caused by physiological response to cryotherapy

is subject to the interaction of four factors.17 These include consideration of Fourier’s Law, length of cooling exposure, heat capacity of the cooled area relating to thermal conductivity, and the thermodynamic properties of the cooling modality.17 Adipose tissue levels affect the clinical effectiveness of cooling8 and therefore influence the decisions regarding cooling dose or choice of modality. Although magnitude and depth of cooling into Tim have been investigated,1,2,3,8 research has not explored this in any sport specific context. Early literature examining temperature change in deep tissue inversely relates to skinfold levels (as a measure of body fat) and limb circumference.18 However, several studies have failed to report on the heterogeneities of participant characteristics or physical properties of the cryotherapy modalities. A clinically important relationship between adipose thickness and required cooling time exists, suggesting that an adjustment to application duration of crushed ice is required to produce similar Tim temperature changes, dependent on skin fold measurements.19 Lipocytes, present in adipose tissue and low in diffusivity and conductivity, conserve heat from underlying tissues therefore acting as an insulating layer.3 Earlier authors have reported similar observations when exploring relationships between adipose, subcutaneous tissue, and depth of cooling achieved.18,20 Although, to the authors’ knowledge no profiling of Tsk data relating physiological responses to cooling within specific sporting positions in rugby union is available. Examining these factors may be useful in the design of appropriate cooling protocols in sporting contexts. In the sport of rugby union, characteristics vary between playing position21 demonstrating a diverse range of anthropometric attributes.22 This multiplicity of bodily appearance across players supports the both the demands of each playing position and performance differences seen across the sport.22 Homogeneity of form and performance attributes is less common in rugby union, presenting it as an ‘atypical’ sport in comparison to other team sports,22 with playing positions commonly referred to as ‘forwards’ or ‘backs’.23 These positional differences are centered around game demands.24,25 Subsequently, some authors have presented further differences in movement characteristics in these groups.26,27 Consistent with previous research on physical traits of rugby

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union players the current study provides comparison regarding several anthropometric parameters and characteristics, such as body mass, which has been found to be greater in forwards compared to backs.28 This larger size for forwards corresponds to the consideration of force-generation required in the scrum,29 with extra mass traditionally consisting of adipose tissue rather than lean tissue.22 However, in recent years, this has changed with forwards presenting with lower levels of body fat to enable increased mobility generally required in elite level participation.30 Literature suggests that differences in body fat percentage between levels of play also exist, with non-elite populations presenting with higher levels of adipose tissue.22 In consideration of the diverse physical traits present in rugby union players and the known interference between adipose tissue and the ability to cool deeper tissues, further evidence is required to determine optimal application of cryotherapy in this population. Additionally, comparison of cooling between commonly applied cryotherapeutic modalities in sport is insufficiently described. Therefore, the purpose of the current study was to investigate differences in the cooling ability of three different cryotherapy modalities in a rugby union population in an attempt to describe optimum cooling protocols for the anterior thigh. METHODS Design Within subjects randomized crossover trial. Participants Inclusion criteria required participants to be male, take part in team, competitive rugby union across University, RFU National One or Two English league level. Due to consideration of gender differences in response to cooling an all-male population was sought.31 All participants were required to Exclusion criteria included any contraindications to cryotherapy,2 previous knee joint surgery, any lower limb injuries in the prior six months, or referred pain either to or from the knee. All participants provided written consent to take part in the study and completed a Physical Activity Readiness Questionnaire (PAR-Q) prior to participation in the study. The study was conducted according to the Declaration of Helsinki and approved by the host university ethics committee.

Procedures Data were collected in a rugby union clinical setting with ambient room temperature collected to note any noteworthy fluctuations in room temperature during testing; mean ambient room temperature was recorded at 21.5±1.2°C. A 15-minute acclimatization period-allowed participant temperature equilibrium to take place prior to baseline data collection during which the collection of participants’ height, weight, dominant leg, age, and thigh circumference was completed. Skinfold measures using Harpenden Skinfold Callipers (model HSB-BI; Baty International, Burgess Hill, West Sussex, UK), were used to estimate the percentage body fat based on the sum of skin fold thickness for adipose tissue measurements taken from the following sites: thigh, abdomen, medial calf, triceps, biceps, iliac crest, supraspinatus and subscapularis.32 Quantification of anthropometric assessment commonly considers body fat percentage via the collection of skinfold measurement. Although errors in precision of skin fold testing occur, research suggests that it is common practice in elite groups of athletes across sports.22 Participants were randomly assigned following acclimatization, each participant to one method of cryotherapy intervention (Randomisation.com). Prior to application of cryotherapy, baseline measurements were taken, via three Tsk images of the anterior thigh, using a thermal imaging camera (ThermoVision A40M, Flir Systems, Danderyd, Sweden) and the mean of these measurements was used for data analysis. The anterior thigh location was chosen as the area to investigate because it is considered as a common site for contact injury, such as a contusion. In order to standardize an area of interest relevant to each participant in consideration of individual size differences and characteristics, wooden markers were applied to the non-dominant anterior thigh that defined a region of interest (ROI). This ROI was formulated by measuring the circumference of the thigh, 50% between anatomical points of the greater trochanter of the femur and lateral joint line of the knee; circumference of the thigh served as the horizontal axis of the ROI.33 The vertical axis of the ROI measured from the anterior superior iliac spine to the superior pole of the patella.34 Where horizontal

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and vertical axes merge, central ROI was determined.33,34 Superior to inferior borders of the ROI represented as one third of the ASIS to superior pole of patella measurement. Medial to lateral borders of the ROI represented as 25% of the circumference of the thigh (Figure 2).33,34 Once the ROI was determined, skin was marked with a washable pen and wooden markers applied to the determined locations (Figure 2), and pre-intervention images were taken. Emissivity of the thermal imaging camera was set at 0.97-0.98 following standard medical protocols. Thermacam Researcher Pro 2.8 software was used to analyse skin temperature images. The thermal imaging camera positioned over a plinth, facing inferiorly to allow participants to remain in a semirecumbent supine position during application of the intervention and for additional measurements of the Tsk over the anterior thigh. The camera was mounted on a tripod arranged at a distance between the camera and participant ranging from 1.5–2.m dependent on limb size for image focus. Participants were exposed to three different cryotherapy modalities, Crushed Ice (CI), Thigh CryoCuff® (DJO Global, Surrey, UK) (CC), and Wetted Ice (WI) in a random order. Each modality was applied for 20 minutes.4,19 CI consisted of 800g of crushed ice in a clear 22x40cm 1-mil polyethene bag with excess air removed secured over the anterior thigh with plastic wrap; WI consisted of 500g of crushed ice combined with 500ml of water in a 22x40cm 1-mil polyethene bag secured with plastic wrap; CC prepared using a thigh wrap attachment and the standard Cryo/Cuff® tub filled, half water and half crushed ice to the advised limit. A standard cling wrap held in place the CI and WI during testing. Each exposure was separated by at least seven days,12 according to the within subjects randomized crossover design study. Subjects were asked to refrain from ingestion of caffeine, food or alcohol and energetic exercise and for at least two hours prior to the application of the icing modalities.34 Each participant recorded thermal sensation and comfort ratings35 pre- and post-intervention for each condition (CI, CC and WI). Thermal sensation35 was measured by asking the question: ‘How are you feeling now?’ Participants responded by

grading the sensation of temperature relevant to their anterior thigh, on a standardized scale from -4 to 4 (-4=very cold, -3=cold, -2=cool, -1=slightly cool, 0=neutral, +1=slightly warm, +2=slightly hot, +3=hot, +4=very hot). Thermal comfort12,36 was determined by asking participants the question: ‘Do you find this…?’. Participants answered using a five-point scale, where 0=comfortable, 1=slightly comfortable, 2=uncomfortable, 3=very uncomfortable, 4=extremely uncomfortable. After completion of the 20-minute cryotherapy exposure and removal of the modality, five thermal images of the anterior thigh were taken and used for data analysis. STATISTICAL ANALYSIS Data were analyzed using a repeated measures model (SPSS Version 24, SPSS Inc. Chicago, IL), using data pre-exposure as a covariate when comparing between all three applications of cryotherapy, applying least significant pairwise comparisons. The distribution of data about the mean were assessed and found to be suitable for parametric testing for Tsk. Non-parametric Friedman tests were used for comparison of thermal comfort and sensation data to explore differences between applications of cryotherapy.12 RESULTS Twenty-one rugby union players (20±2.9 years, body mass 96.2±16.7Kg, height 179.9±7.1cm, BMI 29.7±2.6kg/m2 and thigh circumference 62.5±7.1cm) volunteered to take part in the study (Figure 1). SKIN SURFACE TEMPERATURE (TSK) Tsk Whole Group When comparing whole group baseline Tsk to immediately post removal Tsk, statistically significant reductions in Tsk occurred for all three applications, CI (p=0.000), CC (p=0.000) and WI (p=0.000). A statistically significant difference was observed in Tsk when comparing post application CI to CC (p=0.000), with CI producing significantly cooler Tsk than CC (Table 1). Additionally, a statistically significant difference in Tsk was noted when comparing post WI to CC (p=0.01) with WI producing significantly cooler Tsk than CC (Table 1). No significant differences in

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Figure 1. CONSORT diagram, demonstrating ﬂow of participant recruitment, allocation and analysis.

Tsk were demonstrated when comparing between CI and WI Tsk post intervention (p=0.141). Tsk Comparisons between Forwards and Backs Statistically significant differences in Tsk were noted when comparing playing positions, with significantly greater reductions in Tsk immediately post-intervention in the ‘forwards’ position group (p=<0.05) compared to the ‘backs’ position group for, all three modalities (p=<0.05), (Table 1).

Thermal Comfort and Thermal Sensation Whole Group There was a significant decrease in reported thermal comfort post intervention when compared to pre-intervention measures for CI (p=0.014), WI (p=0.014) and CC (p=0.025). No significant differences were noted when comparing between modalities for thermal comfort (p=0.755). There were significant decreases in reported thermal sensation post-intervention when compared to

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pre-intervention measures for CI (p=0.001), WI (p=0.000) and CC (p=0.000). No significant differences were noted when comparing between modalities for thermal sensation (p=0.225) (Table 1).

Figure 2. Region of Interest (ROI) over the anterior thigh of the non-dominant limb determined by percentage circumference and anatomical location points for each participant.

Thermal Comfort and Thermal Sensation for Forwards and Backs With data collapsed into positional groupings of forwards and backs, a statistically significant decrease in thermal comfort post-intervention when compared to pre-intervention measures was displayed for WI in the forwards group (p=≤0.05). No significant change in thermal comfort was displayed for CI or CC in the forwards group (p=>0.05) (Table 1). A statistically significant decrease in thermal comfort post-intervention when compared to preintervention measures was displayed for both WI (p=0.014) and CI (p=0.014) in the backs group. No significant change in thermal comfort was displayed for CC in the backs group (p=>0.05) (Table 1). A significant decrease in thermal sensation was observed post intervention when compared to preintervention for CI, WI, and CC in both forwards and backs groups (p=≤0.05) (Table 1). No statistically significant differences were observed in thermal comfort or thermal sensation in both forwards and backs groups, when comparing between any modality (p=≥0.05).

Table 1. Skin Temperature (Tsk), self-reported scale for thermal comfort and thermal sensation data for whole group, and rugby union positional groups of forwards and backs.

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DISCUSSION Despite the common application techniques of cryotherapeutic modalities and their use in sports injury management, consensus for optimum protocols are inconsistent across literature.1,2,3,4 The present study investigated a comparison of three cooling modalities frequently applied in the sporting context for pitch-side management of soft tissue injury in a rugby union population. CI, CC and WI were applied on separate occasions over the anterior thigh in a rugby union population, representing all playing positions, sub-grouped into ‘forwards’ and ‘backs’. Results suggest differences in the ability to reduce Tsk to within the desired therapeutic range of cooling occurs between cryotherapeutic modalities, in line with similar investigations.2 Comparison between modalities for whole group data, reported differences in Tsk, with WI displaying the greatest reduction of Tsk (12.0±3.0°C) and CC offering the least reduction in Tsk,(15.8±1.4°C) recorded immediately post removal. Evaluation of Tsk between the two positional groups; ‘forwards’ compared to ‘backs’, demonstrated significant differences in Tsk between positional groups and between types of applications (p=>0.05). These findings have implications on optimal cooling protocol development and application choice when applied to a rugby union population. When comparing whole group Tsk data to baseline, most modalities (CI, WI) demonstrated the ability to cool Tsk to within the desired therapeutic range of 10-15°C (Table 1).37,38 Tsk findings suggest these modalities may be capable of initiating positive physiological responses within deeper tissues, such as intramuscular cooling determined through observation of Tsk in consideration of the proposed quadratic relationship reported in earlier literature.3 Although, aside from Tsk measures, other physiological responses were not quantified in this study, therefore, the suggested responses can only be assumed to occur based on previous literature.3 Observations of Tsk displayed different responses between modalities supporting previous literature2,5,17,39 with WI achieving the coldest average Tsk in whole group data (12.0±3.0°C) compared to CC and CI. Interestingly, when comparing positional groups, WI application achieved the coolest Tsk in

the ‘forwards’ group (10.9±2.6°C), but not in the ‘backs’ group (15.4±1.6°C). Forwards demonstrated a larger thigh circumference compared to backs (forwards = 64.3±7.9cm; backs = 57.8±2.4cm), which was accompanied by a higher body fat percentage (forwards = 23.3±6.3cm; backs = 15.4±4.1cm). Contrary to what was expected, forwards displayed lower Tsk across all modalities compared to the backs. Indicating, that an increased adipose tissue has an effect on superficial Tsk responses. Consideration of the process of conduction and the insulating dynamics that adipose tissue presents however provides an explanation as to why participants in the ‘forwards’ group illustrated lower Tsk. It could be postulated that heat was more efficiently extracted in the group with lower adipose tissue (backs). Consequently, at the point of application removal (20 minutes) Tsk may have already begun to demonstrate ‘rewarming’ of the superficial tissues in this group (backs) due to efficient heat extraction from deeper tissues. This was represented by higher Tsk compared to the forwards group at the same time point. It was considered that the forwards groups displayed cooler Tsk because the higher levels of adipose tissue reduces efficient extraction of heat at the same capacity when compared to those with lower levels of adipose tissue. This would agree with earlier assumptions suggesting a dilution of net loss of heat lost to the cold modality16. With that in mind we assume that deeper tissues that are also of greater distance from the cooling modality were negatively affected in terms of intramuscular temperature reduction by the levels of insulating tissues. Although this principle is not unknown by any means, the discussion highlights that on the surface although data appears to show more efficient cooling of Tsk in the group with higher levels of adipose tissue (forwards) compared to the group with lower adipose tissue (backs), due to cooler Tsk reported. We presume on this basis that deeper physiological responses were likely affected differently amongst positional groups in the current study. Findings represent specific sporting populations not previously investigated. Sports physical therapists should consider these implications for optimal cryotherapy protocol development within specific population groups that present with distinct physical characteristic differences in relation to adipose tissue.

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Comparison of cooling distribution between modalities as examined visually via thermal imaging may support the post-intervention Tsk values (Table 1), with CC demonstrating an uneven distribution in cooling of the anterior aspect of the thigh, compared to WI or CI. This appeared to be consistent among participants, regardless of position. This pattern of cooling may be due to the potential uneven contact between the CC modality and skin surface, potentially facilitated by the compression of the device around the limb when expansion of the wrap commences following the introduction of fluid flow into the cuff. Although considered perhaps as a negative when attempting to achieve a significant or consistent cooling response over skin surface, the CC modality is advantageous in respect to the size of the area covered and the ability to provide circumferential pressure around the entire thigh, compared to the smaller targeted anterior limb region covered by the applications of CI and WI (contained in polythene bags secured by plastic wrap). Optimal compression protocols are unknown and further investigation of contemporary cryo-compressive products are warranted in terms of magnitudes of cooling with the adjunct of compression. Furthermore, investigations that consider targeted treatment vs circumferential over not only muscle but joint structures may be beneficial for future development of optimal cryotherapy protocols in sport. The differences in Tsk between modalities reported in the current study for whole group data (Table 1) may be explained by phase change capability. Phase change in terms of thermodynamics is explained as the efficacy of cooling modalities to absorb heat. Modes of cooling differ in respect to their phase change ability and consequently demonstrated by the magnitude of Tsk reduction achieved post application.16,17 Findings in the current study are in line with previous literature that suggest CI is particularly effective in latent heat transfer.2 Our results demonstrate lower Tsk temperatures for CI and WI compared to CC therefore suggesting greater phase change capability occurring in CI and WI modalities. Clearly the modality of water and crushed ice is efficient in reducing Tsk, therefore an explanation as to why CC did not achieve a therapeutic cooling range in whole group data may be explained simply as the

poor conductivity of the interface material in contact with the skin consequently affecting the ability of the ice-water to extract heat. Again this may be mitigated by longer application dose, of which needs further investigation to develop optimal contemporary cryotherapeutic modality applications in sport. A dose of 30-minutes CI over the quadriceps in a similar fashion reported by Merrick et al.16 achieved slightly cooler reductions in Tsk suggesting longer applications influence resultant Tsk. This in turn has an effect on deeper intramuscular temperature. 3,16 In summary the results of the current study suggest that some modalities may be more appropriate for the acute management of sports injuries than others due to their phase change ability. Thermal comfort and sensation outcomes demonstrated predictable reports in response to cooling and cold temperatures, that being self-reported reductions across both scores (Table 1) for the modalities with lower Tsk reductions (WI and CI). The modality with the lesser reduction in Tsk (CC) demonstrated no change in comfort scores despite reductions in Tsk occurring, however interestingly sensation was reported to increase from 0 (neutral) to 1 (slightly warm), evident across both whole group and sub group data (Table 1). When observing different responses in thermal comfort between forwards and backs, WI achieved the same response being â&#x20AC;&#x2DC;slightly uncomfortableâ&#x20AC;&#x2122;. The backs group also reported this for CI, but forwards reported no change in comfort for that particular modality. With regard to why one application is perceived as more of less comfortable, the findings may be due to the insulating effects of adipose tissue, notably as discussed earlier typically this is higher in forwards compared to backs, which may have influenced level of comfort interpreted. Considering thermal sensation scores, both CI and WI applications influenced a predicated reduction in sensation of temperature in both groups but interestingly the forwards group reported a lower feeling of cold for WI compared to the backs. It is unsure why this occurred but the findings correspond to the observed reductions in Tsk reported post removal, that being lower in the forwards than backs (Table 1). Subjective response to cooling in terms of comfort and sensation amongst different modalities has implications on optimal cryotherapy applications.

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Further investigation is required, and scores collected during application may be more beneficial rather than those collected once cooling had been removed. It is difficult to compare current results with other published literature due to the number of variables, such as exposure times, thermodynamics of the modalities, population group, application protocol, and modality location in respect to Tsk responses. Although perhaps not directly comparable, the current results are likely relevant to contemporary discussions in the literature regarding optimum cooling protocols used both clinically and pitch-side for the management of injury.40 Additionally these results offer relevance regarding cryotherapy considerations within specific sporting populations where physical traits vary within a squad. Results support previous literature when considering the impact adipose tissue has on the effects of cooling modalities.1,8,19 Previous authors have encouraged clinicians to measure skinfold thickness in order to determine an appropriate cryotherapy duration.39 Adherence to identification, marking, and measurement of the defined site of skinfold testing is essential for accurate quantification of adipose tissue levels.41 Recommendations for treatment times based on target tissue depth suggest a minimum of 15 minutes of cryotherapy application to achieve 0-15mm target tissue depth for cooling,40 but does not compare type of modality to best inform potential differences in application. Nor does the current evidence base investigate several modalities within specific sporting populations recognising the varying levels of adipose tissue related to positional characteristics. When collapsing the data into sub groups of forwards and backs, data indicates that adipose tissue levels representative of physical traits in the sport of rugby union affects Tsk response (Table 1). Findings are similar to previous literature and consider that adipose tissue levels dictate application dose.19 With this in mind however it is important to consider that all applications in the current study followed the same duration protocol of 20-minutes, with resultant differences in average Tsk, post removal. Although dose exposure length (minutes) was not investigated in the current study, it is clear that adaptations in application protocols between modalities

to achieve desired cooling should be considered. To achieve optimal treatment outcomes in response to cooling in rugby union populations, adaptations to dose therefore may be required as well as choice of modality, when applied to the anterior thigh. This agrees with previous suggestions in literature in relation to altering cooling dose in respect to adipose tissue levels, although presumptuous in the current study, as dose was standardised.19 The choice of cooling modality is an important part of clinical decision making in terms of treatment.2 Adaptations for individual cooling protocols not only regarding the choice of modality but also regarding the duration of exposure and dosage within safe limits is important. In a much larger sample, of multiple playing positions and elite levels, it may be advantageous to investigate positional subgroups further, such as the characteristics of forwards, such as props and locks compared to back row or hooker positions. Researchers have suggested that movement and game demands differ across playing positions,25 affecting the physical characteristics and possibly the interference for application of modalities. The development of a framework representing optimal cooling applications requires consideration of multiple variables behind the mechanisms of cryotherapy. This may support individual approaches to optimum cryotherapeutic protocols defined specifically by type of application, adipose tissue levels,19 the depth of target tissue to be cooled,40 and the circumference of thigh in rugby union populations for example. Comparison of cooling duration and compression adjuncts in future studies is of merit utilizing contemporary technological advances available in cooling modalities. In consideration of current practice for the management of muscular injury, further development of cooling protocols that investigate contemporary cooling devices should consider the impact on latent intramuscular changes post application, which may fluctuate between modalities as Tsk does. LIMITATIONS The generalizability of findings may be limited due to the voluntary participation of a healthy all-male population group of rugby union players. Due to differences in thermoregulation, adipose thickness

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and that all participants were non-injured, the use of these procedures cannot be assumed in other populations, such as those of different academy age, females, or injured populations that may respond differently. Specific consideration of further study of temperature changes that occur in injured populations is required.

5. Dykstra JH, Hill HM, Miller MG, Cheatham CC, Michael TJ, Baker RJ. Comparisons of cubed ice, crushed ice, and wetted ice on intramuscular and surface temperature changes. J Athl Train. 2009;44:136-141.

CONCLUSIONS Variability in approaches of cryotherapy application by Sports Physical Therapists, demonstrates a lack of consensus due to limited data to substantiate cryotherapy guidelines.40 The results of the current study concur with earlier research that suggests that differences in the cooling ability between cryotherapy applications exist. WI was able to produce the greatest decrease in Tsk corresponding with self-reported thermal comfort and sensation scores. The greatest implication of the current study supports recommendations to further the research in cryotherapy application to meet therapeutic goals through adaptation of protocols to each athlete.42 The significant variability in Tsk between cooling in the two positional groups affirms the importance of the individualization of local cooling protocols when considering physical traits and characteristics within a rugby union population. Future research may consider extending observation beyond the dichotomy of forwards/backs and to other sports in which variability in physical characteristics vary across a squad.

7. Costello J, McInerney C, Bleakley C, Selfe J, Donnelly A. The use of thermal imaging in assessing skin temperature following cryotherapy: A Review. J Thermal Bio. 2012;37:103-110.

REFERENCES 1. Jutte LS, Merrick MA, Ingersol CD, Edwards JE. The relationship between intramuscular temperature, skin temperature, and adipose thickness during cryotherapy and rewarming. Archives Phys Med & Rehab. 2001;82:845-850. 2. Kennet J, Hardaker N, Hobbs S, Selfe J. Cooling efﬁciency of 4 common cryotherapeutic agents. J Athl Train. 2007;42:343-348. 3. Hardaker N, Moss A, Richards J, Jarvis S, McEwan I, Selfe J. The relationship between skin surface temperatures measured via Non-contact Thermal Imaging and intra-muscular temperature of the rectus femoris muscle. Thermo Int. 2007;17: 45-50. 4. Bleakley C, Costello JT, Glasgow PD. Should athletes return to sport after applying ice. A systematic review of the effect of local cooling on functional performance. Sports Med. 2012;42:69-87.

6. Selfe J, Hardaker N, Whittaker J, Hayes C. An investigation into the effect on skin surface temperature of three cryotherapy modalities. Thermol Int. 2009;19:121-126.

8. Bleakley C, Glasgow P, Phillps N, Hanna L, Callaghan M, Davison G, Hopkins T and Delahunt E. Management of acute soft tissue injury using protection, rest, ice, compression and elevation recommendations from the Association of Chartered Physiotherapists in Sports and Exercise Medicine (ACPSM). Physio Sport, 2011;1:1-22. 9. Knight KL, Brucker JB, Stoneman PD, Rubley MD. Muscle injury management with cryotherapy. Athl Ther Today. 2000;5:26-30. 10. Algaﬂy AA, George KP. The effect of cryotherapy on nerve conduction velocity, pain threshold, and pain tolerance. Br J Sports Med. 2007;41:365-369. 11. White G, Wells G. Cold-water immersion and other forms of cryotherapy: physiological changes potentially affecting recovery from high-intensity exercise. Extreme Physiol & Med. 2013;2:2-11. 12. Selfe J, Alexander J, Costello JT, May K, Garratt N, Atkins S, et al. The effect of three different (-135°C) whole body cryotherapy exposure durations on elite rugby league players. PLoS ONE. 2014;9:1-9. 13. Alexander J, Selfe J, Oliver B, Mee D, Carter A, Scott M, May K. An exploratory study into the effects of a 2 minute crushed ice application on knee joint position sense during a small knee bend. Phys Ther Sport. 2016;18:21-26. 14. Alexander J, Richards J, Attah O, Cheema S, Snook J, Wisdell C, et al. Delayed effects of a 20-min crushed ice application on knee joint position sense assessed by a functional task during a re-warming period. Gait Posture. 2018;62:173-178. 15. Enwemeka CS, Allen C, Avilla P, Bina J, Konrade J, Munns S. Soft tissue thermodynamics before, during and after cold pack therapy. Med Sci Sports Ex. 2002;34:45-50. 16. Merrick M, Jutte L, Smith M. Cold modalities with different thermo-dynamic properties produce different surface and intramuscular temperatures. J Athl Train. 2003;38:28–33.

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17. Von Nieda K, Michlovitz SL. Cryotherapy. In: Michlovitz SL (Ed). Thermal agents in rehabilitation 3rd Edition. F.A. Davies Company, Philadelphia. 1996. 18. Lowden BJ, Moore RJ. Determinants and nature of intramuscular temperature changes during cold therapy. Am J Phys Med. 1975;54:223–233. 19. Otte JW, Merrick MA, Ingersoll CD, Cordova ML. Subcutaneous adipose tissue thickness alters cooling time during cryotherapy. Arch Phys Med Rehab, 2002;83:1501-1505. 20. Zemke JE, Andersen JC, Guion K, McMillam J, Joyner B. Intramuscular Temperature Responses in the Human Leg to Two Forms of Cryotherapy: Ice Massage and Ice Bag. J Orthop Sport Phys Ther. 1998;27:301–307. 21. Cahill N, Lamb K, Worsfold P, Headey R, Murray S. The movement characteristic of English Premiership rugby union players. J Sports Sci. 2013;31:229-237. 22. Duthie GM, Pyne DB, Hooper S. The applied physiology and game analysis of rugby union. Sports Med. 2003;33:973-991. 23. Twist C, Worsfold P. (2014). Science of rugby. London: Routledge. 24. Duthie GM, Pyne DB, Hooper S. Time motion analysis of 2001 and 2002 Super 12 rugby. J Sports Sci. 2005;23:523-530. 25. Roberts SP, Trewartha G, Higgitt RJ, El-Abd J, Stokes KA. The physical demands of elite English rugby union. J Sports Sci. 2008;26:825-833. 26. Eaton C, George K. Position speciﬁc rehabilitation for rugby union players. Part 1: Empirical movement analysis data. Phys Ther Sport. 2006;7:22-29. 27. Deutsch MU, Kearney G, Rehrer N. Time-motion analysis of professional rugby union players during match play. J Sports Sci. 2007;25:461-472. 28. La Monica MB, Fukuda DH, Miramonti AA, Beyer KS, Hoffman MW, Boone CH, et al. Physical differences between forwards and backs in American collegiate rugby players. J Strength Cond Res. 2016;30:2382-2391. 29. Quarrie KL, Wilson BD. Force production in the rugby union scrum. J Sports Sci. 2000;18:237-246. 30. Olds T. The evolution of physique in male rugby union players in the twentieth century. J Sports Sci. 2001;19:253-262.

31. Cankar K, Finderle Z. Gender differences in cutaneous vascular and autonomic nervous response to local cooling. Clin Autonomic Res. 2003;13:214-220. 32. Duthie GM, Pyne DB, Hopkins WG, Livingstone S, Hooper SL. Anthropometry proﬁles of elite rugby players: quantifying changes in lean mass. Br J Sports Med. 2006;40:202–207. 33. Doxey GE. The association of anthropometric measurements of thigh size and B-mode ultrasound scanning of muscle thickness. J Orthop Sports Phys Ther. 1987;8:462-468. 34. Janwantanakul P. The effect of quantity of ice and size of contact area on ice pack/skin interface temperature. Physiotherapy. 2009;95:120-125. 35. Cholewka A, Drzazga Z, Sieron A. Thermography study of skin response due to whole-body cryotherapy. Skin Res Technol. 2012;18:180–187. 36. International Organization for Standardization (ISO). Ergonomics of the thermal environment-assessment of the inﬂuence of the thermal environment using subjective judgement scales. International Organisation for Standardisation, Geneva, Switzerland, 2011. 37. Chesterton LS, Foster NE, Ross L. Skin temperature response to cryotherapy. Arch Phys Med Rehab. 2002;83:543–549. 38. Kanlayanaphotporn R, Janwantanakul P. Comparison of skin surface temperature during the application of various cryotherapy modalities. Arch Phys Med, Rehab. 2005;86:1411–1415. 39. Jutte LS, Hawkins JR, Miller KC, Long BC, Knight KL. Skinfold thickness at 8 common cryotherapy sites in various athletic populations. J Athl Train. 2012;47:170-177. 40. Hawkins JR, Miller KC. The importance of target tissue depth in cryotherapy application. J Athl Enhance. 2012;1:2. 41. Hume P, Marfell-Jones M. The importance of accurate site location for skinfold measurement. J Sports Sci. 2008;26:1333-1340. 42. Hawkins SW, Hawkins JR. Clinical applications of cryotherapy among sports physical therapists. Int J Sports Phys Ther. 2016;11:141-148.

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ORIGINAL RESEARCH

IS STEP RATE ASSOCIATED WITH RUNNING INJURY INCIDENCE? AN OBSERVATIONAL STUDY WITH 9- MONTH FOLLOW UP Eliza B. Szymanek, DPT, DSc1 Erin M. Miller, MS, ATC2 Amy N. Weart, DPT2 Jamie B. Morris, DPT, DSc3 Donald L. Goss, PT, PhD4

ABSTRACT Background: Several strategies have been proposed to reduce loading of the lower extremity while running including step rate manipulation. It is unclear however, whether step rate influences the incidence of lower extremity injuries. Purpose: To examine the association between step rate and risk of injury in an adult recreational runner population. Study Design: Prospective Cohort Methods: A total of 381 runners were prospectively followed for an average of nine months. Two-dimensional video was used to assess preferred step rate during a timed two-mile run or a 5K race. Injury surveillance to record sub-clinical injuries (those for which medical treatment was not sought) was performed via semi-monthly email surveys over the course of one year. Injury surveillance for clinical injuries (those for which medical treatment was sought) was performed via a full medical record review using the Armed Forces Health Longitudinal Technology Application. Clinical, sub-clinical and combined clinical and sub-clinical injury incidence were assessed in separate analyses. Injury was operationally defined as seven or more days of reduced activity due to pain. To assess the predictive validity of running step rate, the step rate of participants who did not develop a musculoskeletal injury during the observation period were compared with the running step rate of participants who did develop an injury during the observation period. Results: Out of 381 runners, 16 sustained a clinical overuse injury for which medical treatment was sought. Mean step rate for clinically un-injured runners was 172 steps/min and mean step rate for clinically injured runners was 173 steps/min which was not statistically significantly different (p = 0.77.) Out of 381 runners, 95 completed all four sub-clinical injury surveys (95/381 = 25%). Out of those 95 runners, 19 sustained a clinical (n=4) or sub-clinical injury (n=15). The step rate of sub-clinically injured and non-injured runners in this sub-sample was also not statistically significantly different (p = 0.08), with a mean of 174 steps/min for the uninjured group and a mean step rate of 170 steps/min for those in the sub-clinical injured group. Conclusion: Preferred step rate was not associated with lower extremity injury rates in this sample of DoD runners. Additional research is needed to justify preferred step rate manipulation as a means to reduce lower extremity injury risk. Level of Evidence: Level 3 Key Terms: step rate, cadence, running injuries

Madigan Army Medical Center, Tacoma, WA, USA Baylor University - Keller Army Community Hospital Division I Sports Physical Therapy Fellowship, West Point, NY, USA 3 Army-Baylor University Doctoral Program in Physical Therapy, Fort Sam Houston, TX, USA 4 High Point University, Department of Physical Therapy, High Point, NC, USA 2

The study protocol was approved by the Keller Army Community Hospital Institutional Review Board (KACH IRB). Statement of Financial Disclosure and Conflict of Interest: We affirm that we have no financial affiliation (including research funding) or involvement with any commercial organization that has a direct financial interest in any matter included in this manuscript.

CORRESPONDING AUTHOR Eliza Szymanek 1424 Heron Ct Dupont, WA 98327 E-mail: eliza.b.szymanek@gmail.com

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 221 DOI: 10.26603/ijspt20200221

INTRODUCTION Forty-five percent of military sport-related injuries occur due to running.1 Several strategies have been proposed to reduce loads to the lower extremity while running, including the alteration of the running form.2-4 One strategy that has been employed is increasing step rate, which subsequently results in a decrease in stride length. It has been proposed that shortening one’s stride length may decrease the propensity for running injuries.5 Thompson et al6 reported that decreasing stride length whether in barefoot or shod conditions, reduced both vertical ground reaction force and joint moments. Advocates of a running style with an increased step rate claim that employing this technique will reduce loading of the knee and hip joints and has potential to reduce running injuries. 2-4,7,8 Minimizing the forces associated with ground contact is thought to be important to prevent injury. Heiderscheit et al2 reported that with as little as a 5% increase in step rate there was a 20% decrease in load to the hip and knee. Willson et al8 reported that there was a significant reduction in patellofemoral (PF) joint stress per step, and a 9-12% reduction in cumulative P F joint stress in a 1 kilometer run. In the laboratory setting, altering step rate has demonstrated a reduction in biomechanical stress to the hip and knee,2,6 however the relationship between self-selected step rate and lower extremity injuries in recreational runners has not been reported. Though step rate has been proposed as a method to decrease lower extremity loading while running, there have been few prospective studies observing step rate and its relationship to lower extremity injuries. To the authors’ knowledge, Luedke et al9

are the only authors to observe this relationship in high school cross country runners. Those authors reported that cross country runners with a step rate less than or equal to 164 were 6.7 times more likely to sustain a shin injury compared to runners who ran greater than or equal to 174 steps per minute.9 However, the Luedke et al9 study had a sample of 68 high school cross country runners, which makes the generalizability to all runners difficult. Luedke et al’s9 study also focused only on shin and knee injuries as opposed to all lower extremity injuries. Due to the limited body of research observing step rate and its relationship to lower extremity injuries, more research is needed in this area. Therefore, the primary aim was to examine the association between step rate and risk of injury. It was hypothesized that runners with a greater step rate would have a decreased incidence of injury. METHODS A total of 407 Department of Defense (DoD) beneficiaries (includes service and family members) were screened for inclusion/exclusion criteria (Table 1) prior to the Army Physical Fitness Test and 5K. The study protocol was approved by the Keller Army Community Hospital Institutional Review Board (KACH IRB). All subjects provided informed consent. Initial intake forms collected information including: date of Army Physical Fitness Test (APFT), age, sex, height (inches), weight (lbs), and average running mileage per week. A total of 381 runners met the inclusion/exclusion criteria and continued with the study, see Figure 1. The 381 runners were prospectively followed for an average of nine months. (270 men, 111 women, age

Table 1. Study Inclusion and Exclusion Criteria.

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deviation of 12 steps, resulting in an effect size of 0.50. G Power analysis determined a sample of 210 runners was estimated to be needed to show a statistically significant relationship between step rate and injury. However, due to poor survey response rates reported in previous studies,11 a sample of 400 runners were recruited for this study.

Figure 1. Total number of runners recruited, included and excluded. Armed Forces Health Longitudinal Technology Application (AHLTA) is a secure medical documentation system.

22.6 ± 6 years, height 174.59 ± 10.34 centimeters, weight 75.65 ± 11.1 kilograms). At baseline, participants’ average weekly running mileage was 9.49 ± 8.74 miles per self-report. An a-priori power analysis was performed in G Power version 3.1. A two-tailed t-test was utilized with alpha set to 0.05, and a power of 0.80. U.S. Military Academy collaborators recently completed a study in a sample of 40 runners,10 and determined that the Minimal Detectable Difference (MDD) in step rate, utilizing the method employed in this study, was six steps with a standard deviation of 12 steps. Effect size for this study was determined by dividing the MDD of six steps by the standard

PROCEDURES To determine preferred step rate, subjects were asked to run at their self-selected run pace for two-miles or 5K. Runners participating in the study were identified by wearing numbered running bibs. To determine step rate, two-dimensional video (frontal plane) was collected during over ground running from two stationary high-speed cameras (Casio Exilim EX-ZR200, Tokyo Japan) sampling at 30 frames per second (Hertz) with a resolution of 640 x 480 pixels and shutter speed of 1/1000s. Stationary cameras were mounted to two Vivitar (Edison, NJ, USA) tripods set to a height of 80 centimeters on a level surface. During the APFT performed on a paved route, 2 cameras were set to capture preferred step rate at approximately 800 meters, 1200 meters, 1800 meters, and 2200 meters. (Figures 2 and 3) During the APFT performed on a standard track, a stationary camera was placed on each of the straight-aways to capture preferred step rate continuously over the two-mile event. During the 5K, one camera was positioned at approximately 1200 meters. Running videos were cut down into 10 second video clips from which participants were identified by their running bib. Step rate data were first reduced from each runner’s 1800 m running video. If 1800 m video data quality were poor, the 1200 m video was used instead. Videos taken at 800 m and 2200 m were only used if both the 1800 and 1200 videos were unusable. Videos were determined to be unusable if the reviewer was unable to identify the runner’s bib number or there was not a full 10 second (s) video clip where each step could be visualized. Preferred step rate was calculated from each 10s video segment by counting every time a runner’s foot hit the ground in the 10s video clip and then multiplying this number by six.10 This method of step rate analysis used in this study (10s method) has been shown to be a reliable and valid method.10

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Figure 3. Army Physical Fitness 2 mile run route set up on the road. Camera 1 captured preferred step rate at 800 and 1800 meters and Camera 2 captured preferred step rate at 1200 and 2200 meters. Lap 1 represented by red, Lap 2 represented by green. Cameras represented by black rectangles. Line of sight of camera represented by gray triangles.

Figure 2. Set up of camera on two-mile Army Physical Fitness Test route.

In the current study, step rate analysis was performed by two separate medical professionals, a physical therapist (Rater 1) and an athletic trainer (Rater 2). Rater 1 and Rater 2 were both experienced in the use of high-speed video for the evaluation of running mechanics. Inter-rater reliability was established between these raters prior to step rate analysis. Each rater evaluated the first 20 participantâ&#x20AC;&#x2122;s high-speed video clips, once, independently and blinded to each otherâ&#x20AC;&#x2122;s assessments. The inter-rater reliability between the two raters was excellent (ICC (2,1) = 0.98). After confirming inter-rater reliability, the remaining subject videos were analyzed. INJURY SURVEILLANCE Subjects consented to a retrospective and prospective medical record review. Sub-clinical injury

surveillance (injuries for which medical treatment was not sought) was performed by collecting semimonthly email self-report injury surveys. Clinical injury surveillance (injuries for which medical treatment was sought) was performed via full medical record review using the Armed Forces Health Longitudinal Technology Application (AHLTA), a secure and closed DoD medical documentation system. AHLTA was used to query lower extremity injury diagnoses related to hip, knee, ankle, foot and low back. This was done eight to 10 months after the initial running assessment. AHLTA medical records are available DoD wide, therefore if a subject moved during the study year their medical records were still able to be reviewed. All participants received a simple email survey every other month asking them to provide their weekly running mileage and if they had pain and/ or had limited their activity due to pain or an injury for seven or more days12 during the survey reporting period. If the answer was yes, the runner was deemed as having a sub-clinical injury and received additional questions regarding the location, severity, and nature of the injury. The email surveys were necessary to maximize accuracy of weekly running

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mileage and injury information for which the runners did not seek medical attention. A sub-clinical injury was defined as an injury reported on one of the surveys, and not documented in AHLTA (an injury for which medical treatment was not sought). STATISTICAL ANALYSIS All data were entered into Microsoft Excel and analysed by the statistical package, SPSS V 24 (SPSS Inc; Chicago, IL). Descriptive statistics were calculated to describe the socio-demographic (age, sex, etc.) and health characteristics of the entire sample. Means and standard deviations were computed for continuous data and frequency distributions were analysed for categorical data. To assess the influence of running step rate on injury, the step rate of participants who did not develop a clinical or sub-clinical musculoskeletal injury during the observation period was compared with the running step rate of participants who did develop an injury during the observation period utilizing a two tailed t-test. Effect size utilizing Cohenâ&#x20AC;&#x2122;s d (small; d=0.2, medium; d=0.5, large; d=0.8) was also calculated between the participants who did not develop a clinical or sub-clinical musculoskeletal injury and those runners who did develop an injury during the observational period. RESULTS Over the course of nine months 7% (25 out of 381) of runners sustained a clinical injury for which medical treatment was sought. Of these injuries 64% (16 out of 25) were overuse in nature. A total of 15 runners or 16% reported a sub-clinical injury via email

survey (15 out of 95). Total number of injuries and the corresponding average step rate per body region are presented in Table 2. Descriptive statistics of step rates in clinically non-injured and clinically overuse injured runners, as well as the sub-clinical non-injured and sub-clinical injured runners are presented in Table 3; step rate distributions by groups are represented in Figure 4. Mean step rate for non-injured runners was 172 steps/minute and mean step rate for clinically injured runners was 173 steps/minute. An independent t-test comparing step rate of clinically injured and non-injured runners demonstrated that these rates were not statistically significantly different (p=0.77). Only one subject was excluded from the clinical injury analysis due to being unable to find them in AHLTA. Ninety-five out of 381 runners (25%) completed all four sub-clinical injury surveys. Nineteen out of those 95 runners sustained a clinical (n=4) or sub-clinical injury (n=15). An independent t-test comparing step rate of sub-clinically injured and non-injured runners in this sub group demonstrated that these rates were not statistically significantly different (p=0.08), with a mean of 174 steps/minute for the uninjured group and a mean step rate of 170 steps/minute for those in the combined injury group. A small effect size was observed between both the clinically injured and non-injured runners (0.08) and the sub-clinically injured and non-injured runners (0.41). DISCUSSION The primary purpose of this study was to observe if step rate influenced lower extremity injury rates in

Table 2. Overuse Injuries and Step Rate by Body Region.

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Table 3. Step Rate Statistics in Non-Injured and Injured Runners.

Figure 4. Box plots showing the distributions of step rates between the injured and non-injured runners. The upper and lower margins of the box indicate the interquartile range, demarcating the 25th and 75th percentiles. The center line represents the median score (ie. 50th percentile). The outer bars indicate the range of scores at each end of the distribution, with circles indicating outliers beyond 3 standard deviations from the mean.

Department of Defense personnel. This relationship was analyzed by examining self-selected step rate during a timed two-mile run test or a 5K, and then collected injury data prospectively for an average of nine months. Overall, results of this study suggest that step rate did not have a significant impact on lower extremity injury rates in this population.

Running injuries can be complex and multifactorial. There are several internal and external risk factors to consider in regards to running injuries. Intrinsic risk factors include: sex, body mass index, previous injuries, weekly running distance, and/or lack of running experience.13 Extrinsic risk factors to consider include: training frequency, ground stiffness,

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always running on the same side of the road, and/or running shoe.13 One or a combination of these internal and external risk factors could also contribute to a running related injury. Though step rate has been proposed as a method to decrease load to the lower extremity while running, there have been few prospective studies observing preferred step rate and its relationship to lower extremity injury rates. To the authorsâ&#x20AC;&#x2122; knowledge Luedke et al9 is the only other published study to observe this relationship in high school cross country runners. In Luedke et al9 study, it was reported that runners with a step rate less than or equal to 164 were 6.7 times more likely to sustain a shin injury compared to runners who ran greater than or equal to 174 steps per minute. Luedke et al9 reported 63.6% of their injuries were classified as minor and resulted in only 1-7 days lost of running. In the current study, injury was defined as pain limiting running for seven or more days. Therefore, minor injuries were not captured in this study that limited running for less than seven days, which represented a majority of the injuries reported in Luedke et alâ&#x20AC;&#x2122;s study9. Analysis included all lower extremities injuries whereas, Luedke et al9 analyzed step rate separately for knee or shin pain. In the current study, both the shin and knee injured body regions had lower mean step rates (169 and 170 steps/minute) when compared to the other lower extremity injured body regions (Table 2). This could potentially indicate that these specific body regions, the shin and knee, might have a higher relative risk in regards to lower step rates as compared to other lower extremity body regions such as the hip and foot. This would be consistent with Luedke et al9 who reported cross country runners with a step rate less than or equal to 164 were 6.67 times more likely to sustain a shin injury compared to runners who ran greater than or equal to 174 steps per minute. In an attempt to capture injuries sustained over the course of the year that participants did not seek medical care for, four online surveys were sent out in total. Unfortunately, survey compliance rate was only 25%. Therefore, all injuries where runners could self-select not to run may not have been

captured. This could explain the low rate of injury over the course of one year. However, though the compliance rate of the surveys over all was low, of our 31 overuse injuries reported, 15 or 48% were reported only via survey. Preferred step rate was calculated using the 10s method. Though this method made it feasible to count step rate during a two-mile-run, it may have limited the sensitivity of step rate calculations. Utilizing this method, the minimal detectable difference in step rate was six steps. Luedke et al9 utilized the Polar S3+ Stride Sensor which has been shown to be an accurate and reliable tool to measure step rate with a 1.4% error rate (2-3 steps per minute). Presently, there are several reliable wearable technologies available to measure step rate that would negate this limitation. This study captured step rate during the Army Physical Fitness Test two-mile run event. This is a timed and graded event for cadets or active duty soldiers. Currently, it has not been reported in the literature whether step rate varies between a maximal effort two-mile run and a recreationally paced two-mile run. Luedke et al9 captured step rate during two separate 400 meter runs, one self-paced and one with a pace set at 3.3 m/s performed with a pacer. For the self-selected pace, runners were instructed to run with 80% of their 5K pace effort or 15 of 16 points on the Borg Rating of Perceived Exertion. Self-paced step rate of the sample was 171.3 steps per minute, and step rate at the set 3.3 m/s would be 169.7 steps per minute, which is most likely not a clinically meaningful difference.9 Step rate is often manipulated in runners undergoing gait retraining, but only one study to date has demonstrated that cross country runners with greater step rate experienced fewer anterior shin injuries.9 In the current study, running with a greater step rate was not protective of running related injuries in recreational runners. Injury was defined as pain limiting running for seven or more days, and therefore did not capture more minor injuries. In laboratory settings as little as a 5% increase in step rate significantly decreases the load to the lower extremity.2 This would represent approximately an eight steps per minute increase. Therefore, though step

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rate modifications may still be effective at treating running related injuries, self-selected step rate was not predictive of those runners who will sustain a running injury in this population. CONCLUSIONS The results of the current study indicate that selfselected step rate in DoD runners did not influence subclinical (self-reported) or clinically documented lower extremity injury rates. Future studies are needed to further investigate the relationship of step rate and lower extremity injuries, further examine step rate by specific injury locations, and whether step rate can be a useful screening tool to prevent lower extremity injuries in runners. REFERENCES 1. Hauret KG, Bedno S, Loringer K, Kao TC, Mallon T, Jones BH. Epidemiology of exercise- and sportsrelated injuries in a population of young, physically active adults: A survey of military servicemembers. Am J Sports Med. 2015;43(11):2645-2653. 2. Heiderscheit BC, Chumanov ES, Michalski MP, Wille CM, Ryan MB. Effects of step rate manipulation on joint mechanics during running. Med Sci Sports Exerc. 2011;43(2):296-302. 3. Lenhart RL, Thelen DG, Wille CM, Chumanov ES, Heiderscheit BC. Increasing running step rate reduces patellofemoral joint forces. Med Sci Sports Exerc. 2014;46(3):557-564. 4. Willson JD, Sharpee R, Meardon SA, Kernozek TW. Effects of step length on patellofemoral joint stress in female runners with and without patellofemoral pain. Clin Biomech. 2014;29(3):243-247.

5. Boyer E. Select injury-related variables are affected by stride length and foot strike style during running. Am J Sports Med. 2015;43. 6. Thompson MA, Gutmann A, Seegmiller J, McGowan CP. The effect of stride length on the dynamics of barefoot and shod running. J Biomech. 2014;47(11):2745-2750. 7. Lenhart R, Thelen D, Heiderscheit B. Hip muscle loads during running at various step rates. J Orthop Sports Phys Ther. 2014;44(10):766-774, A761-764. 8. Willson JD, Ratcliff OM, Meardon SA, Willy RW. Influence of step length and landing pattern on patellofemoral joint kinetics during running. Scand J Med Sci Sports. 2015;25(6):736-743. 9. Luedke LE, Heiderscheit BC, Williams DS, Rauh MJ. Influence of step rate on shin injury and anterior knee pain in high school runners. Med Sci Sports Exerc. 2016;48(7):1244-1250. 10. Miller E, Morris J., Watson D., Goss D. A reliability comparison of different methods for detecting step rate and foot strike pattern in runners using twodimensional video. Univ J Pub Health. 2018;6(6): 366-371. 11. Malone D, Ridgeway, K., Nordon-Craft, A., Moss, P., Schenkman, M., and Moss M. Physical therapist practice in the intensive care unit: results of national survey. Physl Ther. 2015;95(10):1335-1344. 12. Yamato TP, Saragiotto BT, Lopes AD. A consensus definition of running-related injury in recreational runners: a modified Delphi approach. J Orthop Sports Phys Ther. 2015;45(5):375-380. 13. Gijon-Nogueron G, Fernandez-Villarejo M. Risk factors and protective factors for lower-extremity running injuries. J American Podiatric Medical Association. 2015; 105(6):532-540.

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ORIGINAL RESEARCH

COMPARATIVE ANALYSIS OF HIP MUSCLE ACTIVATION DURING CLOSED-CHAIN REHABILITATION EXERCISES IN RUNNERS Christopher M. Connelly, MS1 Matthew F. Moran, PhD1 Jason K. Grimes, PhD1

ABSTRACT Background: Increased hip adduction and internal rotation during the early stance phase of running have been linked to an increased risk of lower extremity injury. Both the gluteus maximus (GMAX) and gluteus medius (GMED) eccentrically control these motions. GMAX and GMED activation levels during commonly used rehabilitation exercises requires further exploration. Hypothesis/Purpose: The purpose of this study was to compare peak surface electromyography (sEMG) amplitudes of GMAX and GMED between three closed-chain rehabilitation exercises: bilateral hip external rotation with resistance band (BER), forward lunge with resistance band (FL), and single-leg rotational squat (SLS). It was hypothesized that the FL would elicit greater peak amplitude in the GMAX and GMED than SLS and BER. Study Design: Descriptive, observational cohort study. Methods: Twenty-two healthy runners (14 male, 8 female) had sEMG electrodes placed bilaterally on GMAX and GMED. Participants completed three repetitions each of BER, FL, and SLS exercises with sEMG data normalized to the maximal amplitude recorded at each muscle during the running trial (% MRC). Seven inertial measurement units affixed to the lower extremity measured joint kinematics to enable the exercises to be split into eccentric and concentric phases respectively. Results: There were no significant differences between exercises during the eccentric phases with all peak amplitudes for GMAX and GMED being less than < 30% MRC. Both the SLS (GMAX: 48.2 ± 45.2% MRC, p = 0.019; GMED: 39.3 ± 24.8% MRC, p <.001) and FL (GMAX: 65.8 ± 58.9% MRC, p <.001; GMED: 52.2 ± 34.9% MRC, p<.001) elicited significantly greater peak amplitudes than BER (GMAX: 21.7 ± 22.3% MRC; GMED: 22.8 ± 21.2% MRC) during the concentric phase. Conclusion: Running related injuries have been linked to deficits in GMAX and GMED activation and strength. When averaged bilaterally across 22 healthy runners, peak GMAX and GMED amplitudes during three weight bearing exercises were less than 70% MRC. All three exercises had comparable eccentric peak amplitudes; however, the BER exercise produced a significantly reduced GMAX and GMED amplitude during the concentric phase versus the FL and SLS. The FL and SLS appear equally effective at eliciting peak GMAX and GMED activation. Level of Evidence: 3 Key Words: running, gluteus maximus, gluteus medius, muscle activation

Motion Analysis Laboratory, Sacred Heart University, Fairﬁeld, CT, USA

Conﬂicts of Interest and Source of Funding: There are no conﬂicts of interest and no sources of funding declared.

CORRESPONDING AUTHOR Christopher M. Connelly MS Sacred Heart University, 5002 Corner Rock Dr. Rolesville NC E-mail: moranm@sacredheart.edu

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INTRODUCTION Hip muscle recruitment and activation is an important topic and is widely researched in many different contexts.1–4 Proper hip muscle recruitment can potentially reduce injury risk in a variety of movements.4–8 Both the gluteus maximus (GMAX) and gluteus medius (GMED) are heavily recruited during running1,5,8,9 and may assist with limiting biomechanical flaws linked with running-related injuries.1,6,9–11 The GMAX and GMED also stabilize the pelvis during dynamic activity while eccentrically controlling femoral adduction and internal rotation.11 Previous authors also have suggested that the main biomechanical factors that may put a runner at increased risk for iliotibial band syndrome (ITBS) are excessive hip adduction and internal rotation, and knee internal rotation and abduction during the stance phase.12–15 Clinically, GMED dysfunction has been implicated in numerous musculoskeletal disorders including low back pain, patellofemoral pain syndrome (PFPS) and other lower limb injuries.6,7,10 Maximizing hip muscle recruitment during rehabilitation exercises may increase treatment efficacy, improve lower limb kinematics, assist in injury prevention, improve athletic performance and result in decreased pain.4,8,16 Two of the most common running-related injuries are PFPS and ITBS.17,18 Deficiencies in GMAX and GMED activation are potential etiological factors in injured runners who demonstrate biomechanical flaws linked to possible muscle weakness and/ or inactivation.1,4,6,9,11 Souza & Powers reported that runners with PFPS had greater peak hip internal rotation angles, reduced hip torques, lower GMAX and GMED isotonic strength and greater GMAX activation compared to pain-free runners.1 It has also been reported that female runners with PFPS had significantly less GMAX activation and hip extensor endurance which they speculated led to the observed increase in internal rotation.19 Several authors have investigated the influence of hip muscle strengthening and its effects on participants’ lower limb kinematics; however, the results have been equivocal.7,16,20,21 Snyder et al. investigated the effects of a six-week strengthening program which included closed-chain hip rotation exercises on lower extremity biomechanics.16 They reported a trend towards

reduced peak hip internal rotation angles and a significant decrease in knee abduction moment. This could possibly lead to altered joint loading which may reduce injury risk.16 Earl & Hoch investigated the effects of an eight-week hip and core strengthening program on lower extremity dynamic malalignment.20 They reported significant improvements in lateral core, hip abductor and hip extensor strength along with a significant reduction of knee abduction moment during running.20 Willy & Davis investigated the effect of a six-week hip strengthening and movement re-education program for the single-leg squat on running mechanics.21 They reported improvements in single-leg squat mechanics but not running mechanics. They concluded that a hip strengthening and movement re-training program that is not running specific does not alter abnormal running mechanics. There has been minimal research that has investigated GMAX and GMED activation during functional hip external rotation exercises in a weight-bearing position. During loading response, the initial portion of the stance phase of running gait, eccentric control from the GMAX and GMED is likely important to prevent excessive hip internal rotation.14,19 Runners with excessive internal rotation may be at greater risk of injury which could be caused by insufficiencies of the GMAX and GMED.1,14,19 Although Willy & Davis21 advocated for hip strengthening that more closely resembles the demands of running, there has been no research comparing GMAX and GMED activity during such exercises. Hip muscle activation during weight bearing exercises that challenge frontal and transverse plane control of the hip are lacking in the literature. The purpose of the study was to investigate differences in GMAX and GMED peak surface electromyography (sEMG) amplitudes during both the concentric and eccentric phases of three functional closed-chain exercises: standing bilateral hip external rotation with resistance band (BER), rotational single-leg squat (SLS), and forward lunge with resistance band (FL). It was hypothesized that there would be a significant difference in GMAX and GMED activation between exercises, specifically greater GMAX and GMED activation during FL compared to BER and SLS as that exercise best replicated the first half of the stance phase during running.

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METHODS To compare the influence of three closed-chain rehabilitation exercises on hip muscle activation, twenty-two healthy runners were recruited and tested in a cross-sectional study design. This study was approved by Sacred Heart University’s human subjects committee and all participants granted informed consent prior to enrollment. Purposive sampling was used to recruit participants from the local area using e-mail solicitation. Participants were recreational runners between the ages of 18 and 50 years, completing ≥ 24 km per week, with no reported lower extremity injuries in the prior 12 months. A lower extremity injury was defined as an injury to either lower extremity that resulted in the participant missing at least one day of running. Twenty-two participants (14 males, 8 females; 21.6 ± 2.3 years, 60.7 ± 7.1 kg, running volume: 66.6 ± 17.7 km∙wk-1) volunteered for this study. Cohort size was established a priori at ≥ 20 participants based on previous investigations utilizing similar methods reporting a range of 15-23 participants.22–27 Following informed consent, all participants were assessed for maximal isometric hip abductor strength via a handheld dynamometer (HHD) (Lafayette Instrument 01165; Lafayette Instruments, Lafayette, IN, USA) based on a previously reported method.28 The HHD was placed 5-cm proximal to the lateral malleolus with the participant in a side lying position. The top leg was positioned with the hip and knee neutral while the bottom leg was positioned with the hip at 45° of flexion and the knee at 90° of flexion. Participants performed a maximal isometric contraction against the resistance of one of the primary investigators. The HHD force was then normalized by body weight (BW) and hip abductor torque was computed as the product of normalized force (kg) times the HHD distance to the greater trochanter (cm). Normalized hip abductor torques were used to prescribe resistance band stiffness (TheraBand® CLXTM Resistance Band; Akron, OH, USA). Participants with hip abductor torque <9% BW were assigned a resistance band with minimal resistance from one set of three different bands ( yellow - 9.8N per 100% elongation, green – 20.5N, blue – 25.8N), between 9-11.9% BW were assigned a resistance band with moderate resistance (20.5N

Table 1. Resistance band (Theraband® CLXTM ; Akron, OH, USA) prescription based on hip abduction torque normalized to body weight (BW) [normalized force (kg) times the HHD distance to the greater trochanter (cm)].

per 100% elongation), and ≥12% BW were assigned a resistance band with maximum resistance (25.8N per 100% elongation) (Table 1). Resistance bands were placed approximately 5-cm above the superior border of the patella for both BER and FL exercises. Participants then had bipolar wireless sEMG electrodes (Noraxon U.S.A. Inc.; Scottsdale, Arizona USA) placed bilaterally on the GMAX and GMED in previously reported locations.29 This was preceded by shaving the area if necessary and then abrading and cleaning the skin with alcohol. The GMAX sEMG electrode was placed exactly one-third the distance between the second sacral vertebrae and greater trochanter starting at the second sacral vertebrae.29 The GMED sEMG electrode was placed exactly onethird the distance between the lateral midline of the iliac crest and greater trochanter, starting from the greater trochanter.29 Seven inertial measurement units (IMUs; Noraxon U.S.A. Inc.; Scottsdale, Arizona USA), synced with sEMG data, were firmly attached to the sacrum between the posterior superior iliac spines, lateral mid-thigh between the greater trochanter and lateral epicondyle, lateral mid-shank between the head of the fibula and the lateral malleolus, and on the dorsal surface of the feet bilaterally (Figure 1). A standing calibration trial was utilized to define anatomical neutral position and allow the subsequent determination of lower extremity kinematics during both running and exercise trials. Hip kinematics were computed via Noraxon myoMotionTM software (Noraxon U.S.A. Inc.; Scottsdale, Arizona USA) and used to partition exercise trials into respective eccentric and concentric phases. Transition between phases was determined via maximal knee flexion during the FL and SLS exercises and maximal hip external rotation for the BER exercise. Subsequent

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peak amplitudes were then assigned to eccentric and concentric phases, respectively. Participants then ran on a treadmill (Desmo; Woodway USA, Inc.; Waukesha, WI USA) at a self-selected comfortable pace (5-6/10 effort) for five minutes.

Figure 1. Participant in the starting (A) and ending (B) positions for the bilateral external rotation (BER) with resistance band. A resistance band was approximately placed 5-cm proximal to the superior patellar border and band stiffness was prescribed based on hip abductor strength. Seven inertial measurement units (IMUs) (Noraxon U.S.A. Inc.; Scottsdale, Arizona USA) were placed on the sacrum and bilaterally on the feet, shank, and thighs.

Both sEMG and IMU data were collected for 30 seconds at the four-minute mark. Following the fiveminute running trial, participants performed the BER, SLS, and FL bilaterally in one of the following two counter-balanced orders: (1) BER, SLS, FL; (2) FL, SLS, BER. The starting leg for the FL and SLS was self-selected by each participant and was held consistent for each exercise. Each exercise was performed for three repetitions bilaterally with a twominute rest period between exercises to minimize fatigue. A digital metronome (Pro Metronome; EUM Lab, Hangzhou, China) set at 60 beats per minute was utilized to standardize movement speed for all exercises. For BER, participants were instructed to start in a slightly internally rotated position with knees and hips slightly flexed, and perform a concentric external rotation at the hips (Figure 1). Participants were then instructed to return their hips to a slightly internally rotated position in a controlled manner. The exercise was performed going out (concentric phase) for one beat and coming back (eccentric phase) for three beats with the metronome (Table 2). For SLS, participants were instructed to start with one leg off the ground. They were then instructed to squat down until the femur was as close to parallel

Table 2. Instructions given to participants for performing the three hip exercises.

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to the floor as possible on their stance leg, while keeping their non-stance leg back and reaching their opposite arm across their body, rotating their trunk toward the stance leg about 90° and thereby internally rotating the stance hip (Figure 2). Participants were instructed to return to the starting position in a controlled manner. The exercise was then repeated for the opposite leg. The exercise was performed going down (eccentric phase) for two beats and coming up for two beats (concentric phase) with the metronome (Table 2). For FL, participants were instructed to stand normally and then perform a forward lunge without allowing their knee to move anterior to the toes (Figure 3). They were also instructed to prevent their knee from “moving inward” throughout the lunge movement due to the resistance from the band. Participants were then told to return to the starting position in a controlled manner. The exercise was then repeated for the opposite leg. The exercise was performed going down (eccentric phase) for two beats and coming up (concentric phase) for two beats with the metronome (Table 2). Electromyography data were collected at 1500 Hz (Noraxon 87-8M 8 Channel DDTS; Noraxon; Scottsdale, Arizona USA), band-pass filtered at 20-450 Hz, full-wave rectified, smoothed via 50ms root mean square algorithm. The peak amplitudes recorded during each of five consecutive running strides that

Figure 3. Participant in the starting (A) and ending (B) positions for the forward lunge (FL). A resistance band was approximately placed 5-cm proximal to the superior patellar border and band stiffness was prescribed based on hip abductor strength. A metronome set at 60 beats per minute controlled the speed of the down (eccentric) phase and up (concentric) phase. The same IMUs were worn during this exercise.

occurred after the 4 minute mark, were averaged and used to normalize amplitudes collected during the three exercises. This was used to determine the maximal contraction for the running trial (% MRC). This functional normalization method was chosen because it has been reported to decrease the variability between individuals compared to either using raw EMG data or normalizing to maximum voluntary contractions for dynamic tasks.30–32 STATISTICAL METHODS Data analysis was performed using four univariate analyses of variance (ANOVA) followed by a Bonferroni post-hoc analysis (PASW Statistics; SPSS, HongKong, China) to assess for differences in peak sEMG magnitudes between both phases of the BER, SLS, and FL respectively. For all participants, data from both legs were included within the statistical analysis. Significance level was set a priori at α=0.05.

Figure 2. Participant in the starting (A) and ending (B) positions for the rotational single leg squat (SLS). A metronome set at 60 beats per minute controlled the speed of the down (eccentric) phase and up (concentric) phase. The same IMUs were worn during this exercise.

RESULTS Analysis of GMAX peak amplitudes across all participants during the concentric phase revealed a significant main effect of exercise (BER, FL, SLS) on peak amplitude (F2,131=10.850, p<.001). For the concentric phase, post-hoc comparisons demonstrated that the FL (65.8 ± 58.9% MRC; p<.001) and SLS (48.2 ± 45.2% MRC; p=0.019) resulted in significantly

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greater peak amplitudes than the BER (21.7 ±22.3% MRC), however there was no significant difference between the FL and SLS (p>0.05). For the eccentric phase no exercise resulted in peak amplitudes > 25% MRC and there was not a significant main effect of exercise on peak GMAX amplitude (Figure 4). Analysis of GMED peak amplitudes across all participants during the concentric phase revealed a significant main effect of exercise (BER, FL, SLS) on peak amplitude (F2,131=12.505, p<.001). For the concentric phase, post-hoc comparisons demonstrated that the FL (52.2 ± 34.9% MRC; p<.001) and SLS (39.2 ± 24.8% MRC; p<.001) resulted in significantly greater peak amplitudes than the BER (22.8 ± 21.3% MRC), however there was no significant difference between the FL and SLS (p>0.05). For the eccentric phase no exercise resulted in peak amplitudes > 30% MRC and there was not a significant main effect of exercise on peak GMED amplitude (Figure 5). DISCUSSION The aim of the current study was to evaluate differences in GMAX and GMED activity between three functional closed-chains rehabilitation exercises designed to simulate demands during the stance phase of running. When averaged across 22 active runners and bilaterally, peak GMAX and GMED amplitudes during three weight bearing activities were less than 70% MRC. All three exercises had comparable eccentric peak amplitudes; however,

Figure 4. Peak normalized gluteus maximus EMG amplitude during three exercises (bilateral external rotation, single leg squat, and forward lunge). Statistically signiﬁcant differences (p<0.05) between BER and SLS denoted with * and BER and FL with ƒ.

Figure 5. Peak normalized gluteus medius EMG amplitude during three exercises (bilateral external rotation, single leg squat, and forward lunge). Statistically signiﬁcant differences (p<0.05) between BER and SLS denoted with * and BER and FL with ƒ.

the BER exercise produced a significantly reduced GMAX and GMED amplitude during the concentric phase versus the FL and SLS. Although all three rehabilitation exercises produced comparable GMAX and GMED contractions during the eccentric phase, the BER stimulated significantly lower peak GMAX and GMED activation during the concentric phase. Potential explanations for this finding may be due to a lower exercise difficulty of the BER or the bilateral nature of the exercise. Both of the other exercises included within this study were more unilateral in design. In general, exercises that are bilateral in nature will produce lower muscle activity than unilateral exercises that use the same muscle groups.33,34 However, both of these previous reports investigated concentric contractions, so the results of the current study are interesting in that deficits were not noted during the eccentric phase. Clinically, utilizing a stiffer resistance band or performing unilateral resisted hip external rotation may result in increased concentric phase GMAX and GMED activation and improve overall exercise efficacy. Exercise progression is a common prescriptive design utilized by clinicians. As suggested by Boren et al., percentage of maximal voluntary isometric contraction may be used to rank order exercises to improve strength building effectiveness.35 Although

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all three exercises had similar eccentric amplitudes, the FL and SLS may be more effective for building muscular strength for both the GMAX and GMED than the BER. Despite the fact that these exercises produced substantially lower peak amplitudes as compared to running, they should still be taken into consideration when developing a rehabilitation program for runners returning from injury or seeking to gain improved pelvic control. All of the exercises are functional in nature as they are performed in a weight bearing position similar to the stance phase of running gait. Additionally, SLS and FL are performed unilaterally, which improves the runningspecificity of each exercise possibly improving the transfer to single limb support in running. As stated previously, peak eccentric amplitudes for all three exercises fell substantially below (<30% MRC) the peak activations measured during running. A potential reason why this may have occurred was because the eccentric phases of each exercise was performed at a controlled speed as prescribed by the researchers and controlled by the metronome. While this did improve the methodological design, it did not approximate the speed of loading response during the stance phase. Muscle activity has been positively associated with running speed.36 Specifically, Kyrolainen et al. suggested that with higher running speeds, GMAX muscle activations are higher due to greater contribution from stretch reflexes and preactivation of muscle fibers.36 The purposefully slow eccentric motion during the exercises may have limited peak muscle activity when compared to the faster speeds occurring during the loading response with running. There are several limitations to the current study. In an attempt to standardize the exercise difficulty for the BER and FL, a resistance band was prescribed for each runner based on their normalized hip abductor muscle group strength. In an effort to improve the methodological design and increase the clinical applicability of study, the study was delimited to three resistance bands of varying stiffness, however, this could explain why inter-participant variations were large for the BER and FL. The current study only assessed differences in peak amplitudes and not the onset of activations. Female runners with PFPS have been shown to demonstrate a delayed

gluteal muscle response during running,37 however, it is unknown if the timing of GMAX and GMED peak activations are different between the three tested exercises. Additionally, this study was delimited to healthy runners so it is challenging to draw conclusions on the efficacy of these exercises in a runner rehabilitating from injury. CONCLUSIONS Due to the high prevalence of running-related injuries and the potential role of the GMAX and GMED in reducing these injuries, identifying exercises that effectively activate the gluteal muscles in runners is of great importance. Although none of the exercises investigated in this study approached the peak activation levels obtained with running, the results indicate that the FL with resistance band and SLS were superior to the BER exercise for concentric activation of the GMAX and GMED. All three exercises produced similar results in terms of eccentric activation of the GMAX and GMED. The ability to analyze the concentric and eccentric phases of these exercises is clinically meaningful as the muscle activity required to reduce the excessive hip adduction and internal rotation often observed in risky running posture is eccentric. In that regard, it is recommended that all three exercises may be used in a program focused on improving dynamic hip strength and control in runners rehabilitating from injury or hoping to potentially reduce lower extremity injury risk. Clinicians should also consider these exercises in a recommended progression, beginning with the BER exercise and then transitioning to the SLS and FL with resistance band. Future research is needed to investigate the efficacy of functional closed-chain hip exercises within a population of injured runners and if their adoption transfers to an alteration of running mechanics. REFERENCES 1. Souza RB, Powers CM. Differences in hip kinematics, muscle strength, and muscle activation between subjects with and without patellofemoral pain. J Orthop Sports Phys Ther. 2009;39(1):12-19. 2. Youdas JW, Adams KE, Bertucci JE, Brooks KJ, Nelson MM, Hollman JH. Muscle activation levels of the gluteus maximus and medius during standing hip joint strengthening exercises using elastic tubing resistance. J Sport Rehabil. 2014;23(1):1-11.

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3. Willcox EL, Burden AM. The inﬂuence of varying hip angle and pelvis position on muscle recruitment patterns of the hip abductor muscles during the clam exercise. J Orthop Sports Phys Ther. 2013;43(5): 325-331. 4. Mascal CL, Landel R, Powers C. Management of patellofemoral pain targeting hip, pelvis, and trunk muscle function: 2 case reports. J Orthop Sports Phys Ther. 2003;33(11):647-660. 5. Bazett-Jones DM, Cobb SC, Huddleston WE, O’Connor KM, Armstrong BSR, Earl-Boehm JE. Effect of patellofemoral pain on strength and mechanics after an exhaustive run. Med Sci Sports Exerc. 2013;45(7):1331-1339. 6. Fredericson M, Cookingham CL, Chaudhari AM, Dowdell BC, Oestreicher N, Sahrmann SA. Hip abductor weakness in distance runners with iliotibial band syndrome. Clin J Sport Med 2000;10(3):169-175.

15. Noehren B, Scholz J, Davis I. The effect of real-time gait retraining on hip kinematics, pain and function in subjects with patellofemoral pain syndrome. Br J Sports Med. 2011;45(9):691-696. 16. Snyder KR, Earl JE, O’Connor KM, Ebersole KT. Resistance training is accompanied by increases in hip strength and changes in lower extremity biomechanics during running. Clin Biomech. 2009;24(1):26-34. 17. Hootman JM, Macera CA, Ainsworth BE, Addy CL, Martin M, Blair SN. Epidemiology of musculoskeletal injuries among sedentary and physically active adults. Med Sci Sports Exerc. 2002;34(5):838-844. 18. Taunton JE, Ryan MB, Clement DB, McKenzie DC, Lloyd-Smith DR, Zumbo BD. A retrospective casecontrol analysis of 2002 running injuries. Br J Sports Med. 2002;36(2):95-101.

7. Nadler SF, Malanga GA, Bartoli LA, Feinberg JH, Prybicien M, Deprince M. Hip muscle imbalance and low back pain in athletes: inﬂuence of core strengthening. Med Sci Sports Exerc. 2002;34(1):9-16.

19. Souza RB, Powers CM. Predictors of hip internal rotation during running, an evaluation of hip strength and femoral structure in women with and without patellofemoral pain. Am J Sports Med. 2009;37(3):579-587.

8. Niemuth PE, Johnson RJ, Myers MJ, Thieman TJ. Hip muscle weakness and overuse injuries in recreational runners. Clin J Sports Med. 2005;15(1):14-21.

20. Earl JE, Hoch AZ. A proximal strengthening program improves pain, function, and biomechanics in women with patellofemoral pain syndrome. Am J Sports Med. 2011;39(1):154-163.

9. Willson JD, Petrowitz I, Butler RJ, Kernozek TW. Male and female gluteal muscle activity and lower extremity kinematics during running. Clin Biomech. 2012;27(10):1052-1057.

21. Willy RW, Davis IS. The effect of a hip-strengthening program on mechanics during running and during a single-leg squat. J Orthop Sports Phys Ther. 2011;41(9):625-632.

10. Ekstrom RA, Donatelli RA, Carp KC. Electromyographic analysis of core trunk, hip, and thigh muscles during 9 rehabilitation exercises. J Orthop Sports Phys Ther. 2007;37(12):754-762.

22. DiStephano L, Blackburn JT, Marshall S, Padua D. Gluteal muscle activation during common therapeutic exercises. J Orthop Sports Phys Ther. 2009;39(7):532-540.

11. Homan KJ, Norcross MF, Goerger BM, Prentice WE, Blackburn JT. The inﬂuence of hip strength on gluteal activity and lower extremity kinematics. J Electromyogr Kinesiol. 2013;23(2):411-415.

23. Bolgla LA, Uhl TL. Electromyographic analysis of hip rehabilitation exercises in a group of healthy subjects. J Orthop Sports Phys Ther. 2005;35(8): 487-494.

12. Brindle RA, Milner CE, Zhang S, Fitzhugh EC. Changing step width alters lower extremity biomechanics during running. Gait Posture. 2014;39(1):124-128.

24. Norris B, Trudelle-Jackson E. Hip- and thigh-muscle activation during the star excursion balance test. J Sport Rehabil. 2011;20(4):428-441.

13. MacMahon JM, Chaudhari AM, Andriacchi TP. Biomechanical injury predictors for marathon runners: striding towards ilitibial band syndrome injury prevention. ISBS - Conf Proc Arch. 2000;1(1). https://ojs.ub.uni-konstanz.de/cpa/article/ view/2485. 14. Miller RH, Lowry JL, Meardon SA, Gillette JC. Lower extremity mechanics of iliotibial band syndrome during an exhaustive run. Gait Posture. 2007;26(3):407-413.

25. Ayotte N, Stetts D, Keenan GS, Greenway E. Electromyographical analysis of selected lower extremity muscles during 5 unilateral weight-bearing exercises. J Orthop Sports Phys Ther. 2007;37(2):48-55. 26. O’Sullivan K, Smith SM, Sainsbury D. Electromyographic analysis of the three subdivisions of gluteus medius during weight-bearing exercises. BMC Sports Sci Med Rehabil. 2010;2(1):17. 27. Lubahn AJ, Kernozek TW, Tyson TL, Merkitch KW, Reutemann P, Chestnut JM. Hip muscle activation and knee frontal plane motion during weight bearing

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theraputic exercises. Int J Sports Phys Ther. 2011;6(2):92-103. Kendall F, McGreary E, Provance P. Muscles: Testing and Function, 4th Ed. Baltimore: Williams & Wilkins; 1993. Rainoldi A, Melchiorri G, Caruso I. A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Methods. 2004;134(1):37-43. Chapman AR, Vicenzino B, Blanch P, Knox JJ, Hodges PW. Intramuscular ďŹ ne-wire electromyography during cycling: repeatability, normalisation and a comparison to surface electromyography. J Electromyogr Kinesiol. 2010;20(1):108-117. Allison GT, Marshall RN, Singer KP. EMG signal amplitude normalization technique in stretchshortening cycle movements. J Electromyogr Kinesiol. 1993;3(4):236-244.

32. Yang JF, Winter DA. Electromyographic amplitude normalization methods: improving their sensitivity as diagnostic tools in gait analysis. Arch Phys Med Rehabil. 1984;65(9):517-521.

33. Cresswell A, Ovendal A. Muscle activation and torque development during maximal unilateral and bilateral isokinetic knee extensions. J Sports Med Phys Fitness. 2002;42:19-25. 34. Van Dieen JH, Ogita F, De Haan A. Reduced neural drive in bilateral exertions: a performance-limiting factor?: Med Sci Sports Exerc. 2003;35(1):111-118. 35. Boren K, Conrey C, Le Coguic J, Paprocki L, Voight M, Robinson TK. Electromyographic analysis of gluteus medius and gluteus maximus during rehabilitation exercises. Int J Sports Phys Ther. 2011;6(3):206-223. 36. Kyrolainen H, Avela J, Komi PV. Changes in muscle activity with increasing running speed. J Sports Sci. 2005;23(10):1101-1109. 37. Willson JD, Kernozek TW, Arndt RL, Reznichek DA, Straker JS. Gluteal muscle activation during running in females with and without patellofemoral pain syndrome. Clin Biomech. 2011;26(7):735-740.

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IJSPT

ORIGINAL RESEARCH

RELIABILITY AND VALIDITY OF THE HIP ABDUCTOR ISOMETRIC ENDURANCE TEST: A NEW METHOD TO ASSESS THE ENDURANCE OF THE HIP ABDUCTORS Joachim Van Cant, PT, PhD1,2 Christine Detrembleur, PT, PhD3 Philippe Mahaudens, PT, PhD3 Véronique Feipel, PT, PhD2

ABSTRACT Background: Substantial deficits in the performance of the hip abductor muscles are reported in females with common lower extremity conditions. In this context, the hip abductor isometric test (HAIE) test has been developed to assess the endurance of the hip abductors. Purposes: The aims of the study were: 1) to assess the test-retest reliability of the HAIE test and 2) to determine if the HAIE test is valid for the measuring hip abductor muscle fatigue. Design: Diagnostic accuracy of clinical tests; test retest reliability and validity Methods: Fifty-two healthy females, aged 18-30 years, were recruited. In two identical sessions, spaced by seven days, the participants performed the HAIE test and the test-retest reliability (ICC, SEM and MDC) was calculated. In ten subjects, surface EMG was used during the test in order to observe the change in the median frequency of EMG output of the gluteus medius and to determine if decrease of the median frequency is correlated with performance on the test, in order to discern validity. Results: The HAIE test demonstrated good test-retest reliability (ICC = 0.84, SEM = 11.5 seconds and MDC = 32.8 seconds). Significant differences were noted between the average median frequency of participants for the last four fifteen second intervals (p= 0.02). Moderate correlation between MFslope and endurance time (r = 0.56, p = 0.008) and strong correlation between MFslope75s and endurance time (r = 0.71, p = 0.001) were found. Conclusion: The results from this study support that the HAIE test is a reliable test for evaluating the endurance of the hip abductors. Further investigations should continue to explore the validity of the test, especially to determine which muscles limit the endurance time in healthy and unhealthy subjects. Level of evidence: 2b Key words: Hip abductor endurance, reliability, validity

Department of Physical Therapy, Institut Parnasse-ISEI, Brussels, Belgium. 2 Laboratory of Functional Anatomy, Faculty of Motor Sciences, Université Libre de Bruxelles, Brussels, Belgium. 3 Institute of Neuroscience, Faculty of Motor Sciences, Université Catholique de Louvain, Brussels, Belgium. Statement of financial disclosure and conflict of interest: The authors report no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

CORRESPONDING AUTHOR Joachim Van Cant, PT, PhD Department of Physical therapy, Institut Parnasse-ISEI, Avenue Mounier 85, 1200 Brussel, Belgium. jvancant@yahoo.fr

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 238 DOI: 10.26603/ijspt20200238

INTRODUCTION Substantial deficits in the performance of the hip abductor muscles, mainly in women, are reported in patients with common lower extremity conditions, such as patellofemoral pain (PFP), iliotibial band syndrome, anterior cruciate ligament injuries, and hip osteoarthritis.1,2 Several authors have suggested that endurance deficit of the hip abductors could affect lower extremity movements in frontal plane and, therefore, increase joint stress during prolonged dynamic movements, like running.3,4,5 However, while numerous tests are commonly used to assess the endurance capacity of specific muscles in healthy and symptomatic subjects (e.g. trunk extensors, neck flexors or ankle plantar flexors),6,7,8 there are few tests that have been developed to assess the endurance of the hip abductors.9 Thus, the hip abductor isometric endurance test (HAIE test) was developed to provide a standardized, easy to use evaluation of the endurance of the hip abductors. In a clinical or research context, it is important to determine whether a specific endurance test is a reliable method for assessing muscle endurance. The test-retest reliability of a clinical test refers to the extent to which the test is consistent across time.7 It is also crucial to determine the validity of an endurance test or, in other words, to identify whether muscle fatigue limits performance in terms of test endurance time or repetitions. Enoka and Duchateau10 define muscle fatigue as the gradual decrease in the force capacity of muscle or the endpoint of a sustained activity and suggest to evaluate it by measuring a reduction in muscle force, a change in electromyographic activity or an exhaustion of contractile function.10 In this respect and even if, at this stage, no consensus exists on the best way to evaluate muscle fatigue, the electromyographic (EMG) spectrum analysis is a specific way to assess this muscle impairment.11,12,13,14 In the case of EMG, fatigue is defined as a decrease of the median frequency of the EMG power spectrum.11 Thus, the aims of the present study were: 1) to assess the test-retest reliability of the HAIE test and 2) to determine if the HAIE test is a valid test for the measuring hip abductor muscle fatigue. In this context, surface EMG was used during the test in order to observe the change in the median frequency of

the gluteus medius (Gmed) and to determine if decrease of the median frequency is correlated with performance of the test (endurance time) in order to establish validity. Because previous studies suggest that hip muscle impairments are more prevalent in females than in males,3,15 only females were recruited to participate in this study. METHODS Subjects Fifty-two healthy females, aged 18-30 years, were recruited among students of the University of Louvain, Brussels, Belgium. The inclusion criteria were to be free of recent lower limb injuries (in the prior six months). The exclusion criteria were to have no history of orthopedic injury of or surgery performed on the lower limb or low back for in the prior 12 months and no cardiovascular, pulmonary, neurological, or systemic conditions. All subjects gave written consent to participation in the study, which was approved by the Hospital and Departmental Ethics Committee, Saint-Luc - UCL (Brussels). Procedures The participants attended two assessment sessions, separated by seven days, and conducted by the same investigators (two physical therapists, under the direct supervision of a physical therapist with over 10 years of clinical experience). For procedural standardization, each investigator performed the same tasks in both sessions for all participants. At the second session, the investigators were not blinded to prior data. In both sessions, all subjects performed a five-minute sub-maximal warm-up on a stationary cycle and then performed the HAIE test with the dominant limb (defined as the limb used for kicking a soccer ball). At the first session, participant demographics and characteristics including age, weight, body mass, and physical activity levels were collected. To assess physical activity levels, the French version of the Baecke Activity Questionnaire (BAQ), validated by Bigard and Dufaurez,3 was completed. The BAQ is a short questionnaire including a total of 16 questions classified into three domains receiving a score from one to five: work, sports, and non-sports leisure activity.3 At the second session,

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Table 1. Demographic and clinical characteristics of the study sample (n=52).

in order to assess the validity of the HAIE test, the EMG activity of the GMed was recorded during the test in ten subjects, randomly selected from among all the participants. Demographic and clinical data are presented in Table 1. The HAIE test The subject was placed in a side lying position on the examination table with the hip to be evaluated placed superiorly in neutral alignment and with the pelvis stabilized by straps. The opposite limb was flexed at the hip and knee. The hand of the ipsilateral upper limb was placed on the pelvis. (Figure 1). Considering that previous studies showed that the muscle contractions elicited by tests evaluating isometric endurance, such as the “Sorensen test”, were found to be equal to 40–52% of the maximal voluntary contractile force,11,12 external weight, corresponding to 7.5% of body mass, was placed on the ankle of the evaluated limb.9 Given that maximal isometric strength of hip abductors in side lying position ranges from 14% to 22% of body mass, 7.5% of BW corresponds to a percentage ranging from 34 % to 53% of the maximal voluntary contractile force.16 Upon verbal command, the subject was instructed to isometrically hold the limb in a horizontal position, aligned with the trunk, knee extended and to stabilize the pelvic and scapular girdles in a neutral position. In order to control for the horizontality of the leg, a horizontal bar, fixed to vertical bars, was placed 5 cm underneath the malleolus. Moreover, a mirror was positioned close to the examination table so that the participants could control the horizontal position of the limb during the test. Every 15 s and at the end of the test, the subject was asked to give an overall perception about how hard the exercise felt according to the Borg Rating of Perceived Exertion Scale (Borg RPE), a 15-point single-item scale

Figure 1. The Hip Abduction Isometric Endurance (HAIE) test.

ranging from 6 to 20 (with anchors ranging from 6 “No exertion” to 20 “Maximum exertion”).17 The time during which the subject held the limb straight and the test was stopped when the participant could no longer control the horizontal posture (sustained contact with the bars for more than 5 s) despite investigator warnings or until she reached the limit of fatigue. Standardized instructions and verbal encouragement were given by the same investigator to all participants. Verbal encouragement consisted of the investigator giving positive verbal commands, every 15 s, encouraging the subject to hold the limb in a horizontal position and included the following sentence: “come on, let’s keep going”. Equipment The EMG signals of GMed were recorded by a telemetry EMG system (Telemg, BTS, Milan, Italy). One pair of circular surface electrodes (Medi-Trace, Graphic Controls Corporation, NY, USA) with an electrical surface contact of 100 mm2 were attached using tape to the GMed. The electrodes were placed midway between the iliac crest and the greater trochanter with an inter-interelectrode distance of

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20 mm.11 Before attaching the electrodes, the skin cleaning of with alcohol on the electrode positions. The signal was digitized at 1,000 Hz, full-wave rectified, and filtered (bandwidth 25–300 Hz). Each recorded EMG signal was divided in intervals of 15 s. The median frequency of the EMG power spectrum was calculated with fast Fourier transforms (FFT) using the EMG SMART software, which allowed to transform the EMG signal in the timedomain to the frequency-domain.11 The median frequency was defined as the frequency that divided the spectrum into two equal areas.11 Linear regression analyses were performed for each subject on the calculated median frequencies as a function of time (Figure 2). The median frequency slope (MFs) was determined as the slope of the regression lope line. Moreover, similarly to Kankaanpää et al14 who analyzed participants in a similar period of time, linear regression analyses were also performed for each subject in the first 75 seconds of the test. The median frequency slope for this period (MFslope 75s) was determined as the slope of the regression line. Statistical analysis The test-retest reliability of the HAIE test was calculated with a two-way random model intraclass correlation coefficient (ICC2,1). Reliability coefficients was considered to be poor for an ICC less than 0.51, moderate between 0.51 and 0.70, good between 0.70 and 0.90 and very good for an ICC greater than 0.90.7 To determine consistency of measurements,

the standard error of measurement (SEM) was calculated as SD×√1-ICC, where SD is the standard deviation of all scores from the participants.8 The minimal detectable change (MDC) was calculated as SEM×1.96×√2 to construct a 95% CI.8 The Wilcoxon test was used to assess systematic difference in the rate of perceived exertion between both sessions. Concerning the validity of the HAIE test, a one-way analysis of variance with repeated measures design (ANOVA) was conducted to determine if the average median frequency (AMF) of participants decreased significantly over time. In order to have the same number of observations in each group, only the last four intervals of 15 seconds were compared. Tukey’s post hoc test was used to examine differences between AMF of intervals. Pearson correlation coefficients were calculated between MFslope and endurance time and between MFs75s and endurance time. Correlation was defined as lope weak (< 0.3), moderate (0.3-0.5) and strong (> 0.7).12 The statistical analyses were performed using IBM SPSS 23 software (IBM Corp, Armonk, NY, USA) with a significance level of p < 0.05. RESULTS Test-retest reliability Descriptive statistics and data for the test-retest reliability (ICC, SEM and MDC) are presented in Table 2. The HAIE test demonstrated good test-retest reliability (ICC = 0.84). The SEM was 11.5 seconds for isometric endurance test and the MDC was 32.8 seconds. No statistically significant differences were found in Borg RPE at the end of the test between two sessions (p = 0.49). Validity Descriptive statistics are reported in Table 3. Significant differences were noted between the AMF of participants for the last four 15s intervals (p= 0.02). The AMF of intervals 1 and 3 were significantly different (p>0.05) and the AMF of interval 4 was significantly different from the AMF of the intervals 1, 2 and 3 (p< 0.001) (Figure 3).

Figure 2. Median EMG frequency (transformed from timedomain via EMG START software) of the gluteus medius plotted as a function of time for one subject (Subject 3).

Moderate correlation between MFslope and endurance time (r = 0.56, p = 0.008) and strong correlation

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Table 2. Descriptive statistics and data for the test-retest reliability of the Hip Abductor Isometric Endurance (HAIE) test (n=52).

Table 3. Descriptive statistics for subjects on the Hip Abductor Isometric Endurance (HAIE) test, rates of perceived exertion, and median frequency slopes (n=10).

between MFslope75s and endurance time (r = 0.71, p = 0.001) were found. DISCUSSION The HAIE test is derived from a previous test described by Van Cant et al.9 These authors assessed its test-retest reliability and the test demonstrated good intraclass correlation coefficient (ICC = 0.73). However, standard error of measurement (SEM) and minimal detectable change (MDC) were 19.8 and

54.9 seconds, respectively. Thus, the clinical utility of the previously described test for therapists who want to evaluate endurance of hip abductor was questionable, taking account of the MDC. Therefore, in order to increase the test-retest reliability, a few methodological differences were incorporated between the endurance test used in the previous study9 and the currently described HAIE test: the pelvis was stabilized by straps and in order to control for the horizontality of the leg; a horizontal bar, fixed

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fatigue become fatigued and more emphasis is placed on slow-twitch fibers.5 At this stage, only two studies have evaluated the fatigability characteristics of Gmed during a fatigue protocol.5,15 Jacobs et al5 reported higher AMF than previously reported values associated with trunk extensor muscle. These authors hypothesized that Gmed has larger proportion of fast-twitch fibers than the primarily tonic trunk extensor muscle. In our study, the AMF of the first interval of 15 seconds (142.2 +/- 16.8 Hz) was comparable with AMF of the initial epoch reported by Jacobs et al (2) (146.2 +/- 24.2 Hz). In comparison, Elfving et al18 found lesser AMF values associated with the trunk extensors muscle (53.2 Hz).

Figure 3. Average median frequencies of the gluteus medius of the participants for the last four intervals of 15 seconds (intervals 1, 2, 3 and 4). * p < 0.05.

to vertical bars, was placed underneath the malleolus and a mirror was positioned close to the examination table so that the participants could monitor and attempt to control the horizontal position of the limb during the test. These modifications could explain the better test-retest reliability of the HAIE test and, therefore, the use of this inexpensive equipment is strongly recommended (bars, straps and mirror) in order to complete the test as accurately as possible in clinical practice. One of the purposes of this study was to assess the validity of the HAIE test. The results of the present study showed significant decrease of the median frequency of the GMed during the hip abductor isometric endurance test, confirming that fatigue occurs in the Gmed during the test. Changes in median frequency have been quite frequently used to quantify muscles fatigability in the literature.5,11,12,13,14 Bigland-Ritchie et al3 argued that slow-twitch muscle fibers have low-frequency signals, whereas fast-twitch fibers have higher-frequency signals. During fatiguing efforts, fast-twitch

In the present study, similarly to Jacobs et al5, analyses of hip abductor muscles fatigue have relied on EMG data collected from the Gmed only. Nevertheless, the hip abductors are composed of several muscles that act synergistically to produce hip abduction. In a systematic review, Neumann19 analyzed the actions of the muscles of the hip and reported that the primary hip abductor muscles include all fibers of the Gmed and gluteus minimus, as well as the tensor fasciae latae. The piriformis, sartorius and rectus femoris are considered secondary hip abductors. Furthermore, Coorevits et al11 suggest that it is important to simultaneously measure several muscle locations in order to avoid an oversimplified view of the EMG muscle performance. Moreover, during the test it was also possible that the trunk muscles and the contralateral hip abductor muscles were activated. Widler et al16 reported that there is considerable activation of the contralateral-to-ipsilateral Gmed when evaluated in three different testing positions designed to assess unilateral hip abductor muscle. This suggests that bilateral activation is inevitable during the test. Despite these considerations, the present study showed moderate and strong correlations between MFslope and endurance time. The MFslope values represent the shift from higher- to lower-frequency motor units.5 The correlation between MFslope and endurance time indicate that muscle fatigue of the Gmed can partially explain the test endurance time. In other words, if a subject demonstrated a steeper

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negative MFslope, the Gmed was fatigued at a faster rate during the test and endurance time was lower. MFslope was calculated throughout the entire test for each subject and, also, in the first 75 seconds of the test. According to Kankaanpää et al14, the hypothesis was that analyzing participants in a same period of time could a better way to discriminate test performance and, therefore, that the best performers should demonstrate a less-steep slope in the first 75 seconds rather than throughout the entire test. This may explain why moderate correlation was found between MFslope and endurance time and strong correlation between MFslope75s and endurance time. Further research is needed to determine if the analyze of participants in a same period of time rather than throughout the entire test is more appropriate. The validity and the reliability of the EMG spectrum analysis to monitor muscle fatigue has been evaluated in several studies. Mutchler et al15 sought to determine the reliability of the median frequency measure between two sessions of a 60 s standing isometric endurance protocol. The ICC-values demonstrated that median frequency measurements of hip muscles, including Gmed, were found to have suitable reliability. Mannion et al 20 concluded that measurement of the rate of decline in median frequency of the surface EMG power spectrum provides an excellent technique for objectively monitoring the fatigability of the trunk extensors. The present study must be considered in the light of several limitations. First, the participants assessed were healthy females and the results should not be generalized to males or unhealthy or injured females. Second, at the second session, the investigators were not blinded from prior data and bias might have been introduced during evaluation. Third, analyses of muscle fatigue have relied on EMG from the Gmed only. Thus, it is possible that other hip abductor muscles also contribute to abduction endurance and may account for performance during the HAIE test. Finally, at this stage, no consensus exists on the best way to evaluate muscle fatigue using EMG spectrum analysis and validity of the measure used herein has not been evaluated in Gmed. This may constitute the object of future studies.

CONCLUSION The results from this study support that the HAIE test is a reliable test for evaluating the endurance of the hip abductors. Further investigations should continue to explore the validity of the test, especially to determine which muscles limit the endurance time in healthy and unhealthy/injured subjects. REFERENCES 1. Prins MR, van der Wurff P. Females with patellofemoral pain syndrome have weak hip muscles: a systematic review. Aust J Physiother. 2009;55:9-15. 2. Van Cant J, Pineux C, Pitance L, Feipel V. Hip muscle strength and endurance in females with patellofemoral pain: a systematic review with meta-analysis. Int J Sports Phys Ther. 2014;9:564-82. 3. Bigland-Ritchie B, Cafarelli E, Vøllestad NK. Fatigue of submaximal static contractions. Acta Physiol Scand Suppl. 1986;556:137-48. 4. Bolgla LA, Malone TR, Umberger BR, Uhl TL. Hip strength and hip and knee kinematics during stair descent in females with and without patellofemoral pain syndrome. J Orthop Sports Phys Ther. 2008;38:12-8. 5. Jacobs C, Uhl TL, Seeley M, Sterling W, Goodrich L. Strength and fatigability of the dominant and nondominant hip abductors. J Athl Train. 2005;40:203-6. 6. Demoulin C, Vanderthommen M, Duysens C, Crielaard J-M. Spinal muscle evaluation using the Sorensen test: a critical appraisal of the literature. J Bone Spine Rev Rheum. 2006;73:43-50. 7. Harris KD, Heer DM, Roy TC, Santos DM, Whitman JM, Wainner RS. Reliability of a measurement of neck flexor muscle endurance. Phys Ther. 2005;85:1349-55. 8. Sman AD, Hiller CE, Imer A, Ocsing A, Burns J, Refshauge KM. Design and reliability of a novel heel rise test measuring device for plantarflexion endurance. Biomed Res Int. 2014;2014:391646. 9. Van Cant J, Dumont G, Pitance L, Demoulin C, Feipel V. Test-retest reliability of two clinical tests for the assessment of hip abductor endurance in healthy females. Int J Sports Phys Ther. 2016;11:24-33. 10. Enoka RM, Duchateau J. Muscle fatigue: what, why and how it influences muscle function. J Physiol. 2008;586:11-23. 11. Hermens HJ, Freriks B, Merletti R, Stegeman D, Blok J, Rau G, et al. European recommendations for surface electromyography. SENIAM Project. Roessingh Research and Development; 1999.

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12. Dedering A, Németh G, Harms-Ringdahl K. Correlation between electromyographic spectral changes and subjective assessment of lumbar muscle fatigue in subjects without pain from the lower back. Clin Biomech. 1999;14:103-11. 13. Dedering A, Roos af Hjelmsäter M, Elfving B, Harms-Ringdahl K, Németh G. Between-days reliability of subjective and objective assessments of back extensor muscle fatigue in subjects without lower-back pain. J Electromyogr Kinesiol. 2000;10:151-8. 14. Kankaanpää M, Taimela S, Webber CL, Airaksinen O, Hänninen O. Lumbar paraspinal muscle fatigability in repetitive isoinertial loading: EMG spectral indices, Borg scale and endurance time. Eur J Appl Physiol. 1997;76:236-42. 15. Mutchler JA, Weinhandl JT, Hoch MC, Van Lunen BL. Reliability and fatigue characteristics of a standing hip isometric endurance protocol. J Electromyogr Kinesiol. 2015;25:667-74.

16. Widler KS, Glatthorn JF, Bizzini M, Impellizzeri FM, Munzinger U, Leunig M, et al. Assessment of hip abductor muscle strength. A validity and reliability study. J Bone Joint Surg Am. 2009;91:2666-72. 17. Muyor JM. Exercise Intensity and Validity of the Ratings of Perceived Exertion (Borg and OMNI Scales) in an Indoor Cycling Session. J Hum Kinet. 2013;39:93-101. 18. Elfving B, Németh G, Arvidsson I, Lamontagne M. Reliability of EMG spectral parameters in repeated measurements of back muscle fatigue. J Electromyogr Kinesiol. 1999;9:235-43. 19. Neumann DA. Kinesiology of the hip: A focus on muscular actions. J Orthop Sports Phys Ther. 2010;40:82-94. 20. Mannion AF, Connolly B, Wood K, Dolan P. The use of surface EMG power spectral analysis in the evaluation of back muscle function. J Rehabil Res Dev. 1997;34:427-39.

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IJSPT

ORIGINAL RESEARCH

ECCENTRIC HAMSTRING STRENGTH IS ASSOCIATED WITH AGE AND DURATION OF PREVIOUS SEASON HAMSTRING INJURY IN MALE SOCCER PLAYERS Jordi Vicens-Bordas, MSc1-3 Ernest Esteve, PT, MSc1,2 Azahara Fort-Vanmeerhaeghe, PhD4 Mikkel Bek Clausen, PT, PhD5,6 Thomas Bandholm, PT, PhD7 David Opar, PhD8 Anthony Shield, PhD9 Kristian Thorborg, PT, PhD5,7

ABSTRACT Background: Eccentric hamstring strength seems important in reducing the odds of future hamstring injuries. While age and previous injury are well-known risk factors for future hamstring injuries, the association of age and previous hamstring injury with eccentric hamstring strength in the following season is unknown. Purpose: To investigate the association of age and previous hamstring injury with preseason eccentric hamstring strength in soccer players, and to investigate the association between previous hamstring injury duration and preseason eccentric hamstring strength. Study design: Descriptive, cross-sectional study Methods: A convenience sample of 284 male amateur soccer players (age 18-38 years) was included in the analyses. Self-reported information about previous season hamstring injury and its duration (three weeks or less; more than three weeks) was collected. Preseason eccentric hamstring strength was obtained during the Nordic hamstring exercise using a field-based device. Results: Age had a negative association with preseason eccentric hamstring strength with 0.9% reduction per year. Players with a previous hamstring injury duration of more than three weeks (n=27) had 13% lower preseason eccentric hamstring strength compared to players without previous hamstring injury. Conclusion: Older players have lower preseason eccentric hamstring strength than younger players. Players with a previous hamstring injury duration of more than three weeks have lower preseason eccentric hamstring strength than the rest of the players. These results highlight the need to monitor and address the identified weaknesses in eccentric hamstring strength in amateur soccer players, with specific emphasis on older players with a previous hamstring injury of longer duration. Level of evidence: 2b Keywords: knee-flexor, muscle injuries, hamstrings, performance, football

Sportclinic. Physiotherapy and Sports Training Centre. Girona, Catalonia, Spain 2 School of Health and Sport Sciences (EUSES), Universitat de Girona, Salt, Catalonia, Spain. 3 Research Group of Clinical Anatomy, Embriology and Neuroscience (NEOMA), Department of Medical Sciences, Universitat de Girona (UdG), Girona, Catalonia, Spain. 4 Faculty of Psychology, Education Sciences and Sport (FPCEE) and School of Health Sciences (FCS) Blanquerna, Universitat Ramon Llull, Barcelona, Catalonia, Spain 5 Sports Orthopedic Research Center - Copenhagen (SORC-C), Department of Orthopedic Surgery, Amager-Hvidovre Hospital, University of Copenhagen, Denmark 6 Bachelor’s Degree Programme in Physiotherapy, Department of Physiotherapy and Occupational Therapy, Faculty of Health and Technology, Metropolitan University College, Denmark 7 Physical Medicine and Rehabilitation Research – Copenhagen (PMR-C), Clinical Research Center, Department of Physical and Occupational Therapy, Department of Orthopedic Surgery, Amager-Hvidovre Hospital, Copenhagen University Hospital, Denmark 8 School of Exercise Sciences, Australian Catholic University, Melbourne, Australia 9 Faculty of Health, School of Exercise and Nutrition Science, Queensland University of Technology, Brisbane, Australia; and Institute of Health and

Biomedical Innovation, Queensland University of Technology, Brisbane, Australia Statement of the sources of grant support: No external financial support was provided for this research project. Conflicts of interest: J. Vicens-Bordas reports no financial or other interest in the product or distribution of the product. Anthony Shield and David Opar are listed as co-inventors on a patent filed for the device employed here to assess eccentric hamstring strength (PCT/ AU2012/001041.2012) as well as being shareholders in a company responsible for commercializing the device. Neither of these authors were involved in data collection or analysis in the present study.

CORRESPONDING AUTHOR Jordi Vicens-Bordas School of Health and Sport Sciences (EUSES), Universitat de Girona. Carrer de Francesc Macià, 65, 17190 Salt (Girona), Catalonia, Spain. E-mail: jvicens@euses.cat

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INTRODUCTION Eccentric hamstring weakness has been identified as a risk factor for future hamstring strain injury (HSI) in sports with high intensity running demands, such as soccer1 and Australian rules football (AFL).2 Recently, a device has been developed to measure eccentric hamstring strength during the Nordic hamstring exercise (NHE).3 In a large prospective study including 152 professional soccer players assessed using the NHE device, those with eccentric hamstring strength below 4.35 N·kg-1 were 4.4 times more likely (RR; 95% CI 1.1 to 17.5) to sustain an HSI in the following season compared to stronger players.1 In contrast, no association between eccentric hamstring weaknessess and hamstring injury risk was found in a cohort of 413 professional Qatari soccer players who were assessed using the NHE device.4 Univariate analysis of eccentric hamstring strength may not predict future HSI,4 but it seems that multivariate analyses including age, previous hamstring injury, and reduced levels of eccentric hamstring strength may identify players at a greater risk of future HSI.1 Measuring preseason eccentric hamstring strength in amateur soccer players and identifying those with poorer results may have some merit. Age4–6 and previous hamstring injury7 have often been linked to future HSI. Professional soccer players older than 23 years have been reported to be at an elevated risk of sustaining an HSI6 and each year of age has been reported to increase the risk of sustaining an HSI up to 1.8-fold (OR; 95% CI 1.2 to 2.7) in English Premier League soccer players.5 This apparent effect of age on injury risk could, at least in part, be due to age related changes in hamstring strength. However, the impact of age on eccentric hamstring strength has not previously been investigated in soccer players at any level. While the effects of a previous HSI on eccentric hamstring strength have been addressed in the literature,8 most of the studies have been performed in mixed groups of athletes, with small sample sizes and have used isokinetic dynamometry to examine strength. Furthermore, previous studies have not accounted for injury severity.8 Players with previous HSI may present persistent biceps femoris long head muscle atrophy,9,10 and neuromuscular inhibition.7,11 This may limit the effectiveness of the rehabilitation

process and thereby increase the risk of re-injuries,7 due to persistent inadequate muscle structure and/ or function. Accordingly, the observed activation and strength deficits during eccentric actions remain present despite apparently successful rehabilitation and return to pre-injury levels of training and match play.12 As a consequence, it is plausible that a hamstring injury sustained in the previous season could negatively influence eccentric hamstring strength at the beginning of the next season. Presently, however, the association of a previous hamstring injury with eccentric hamstring strength in the following season is unknown. The purpose of the present study was to investigate the association of age and previous hamstring injury with preseason eccentric hamstring strength in soccer players. The secondary purpose was to investigate the association between previous hamstring injury duration and preseason eccentric hamstring strength. MATERIALS AND METHODS Design and participants This study employed a cross-sectional exploratory and descriptive design and includes data from a large cohort study investigating hamstring and groin injuries, self-reported outcome and muscle strength in amateur male soccer players.13 The reporting of the present study follows the “Strengthening the Reporting of Observational Studies in Epidemiology” (STROBE) statement, using the checklist for cross-sectional studies.14 Male players (n=363) from a convenience sample of 17 sub-elite soccer teams from the northeast of Spain, competing in the 3rd national and the 1st and 2nd regional divisions (4th to 6th tier), were screened for eligibility. Players from those teams performed the baseline testing during the preseason (July-August 2015). Players were included if they were over 18 years of age, were free from current hamstring injury, were able to participate in a training session on the day of testing, could understand Catalan or Spanish, provided written informed consent and completed all testing procedures. This study was approved by a regional ethics committee (Consell Català de l’Esport, approval number = 08/2015CEICEGC).

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Testing procedure Three members of the research team who were trained in the measurement procedures, one physiotherapist (EE) and two sport scientists JVB and LS performed all the baseline measurements at the respective team facilities. Team physiotherapists, physical trainers and members of the technical staff of the respective teams collaborated in the assessments, providing questionnaires and forms and helping to conduct the standardized warm-up, which consisted of low intensity shuttle runs and active lower limb mobility exercises. Players were asked to arrive 90 minutes before the start of a regular preseason training session to perform the test battery. Using a standardized form, players provided personal information (date of birth) and data on current hamstring injury (Yes; No), previous season hamstring injury (Yes; No), previous season hamstring injury duration in week ranges (three weeks or less; more than three weeks; as a possible surrogate measure of injury severity), side of injury (right; left). Additionally, weight and height were measured and registered for each player. The NHE device, previously assessed for reliability (0.83-0.90 ICC and 5.8-8.5% CV),3 was used for the assessment of eccentric hamstring strength. Participants knelt on a padded board, with the ankles secured superior to the lateral malleolus by individual ankle braces attached to custom-made uniaxial load cells (Delphi Force Measurement, Gold Coast, Australia). Immediately before testing, players were provided with a demonstration of the NHE by the investigators. After a three-repetition warm-up set and one minute of rest, participants were asked to perform one set of three maximal repetitions of the NHE. Participants were instructed to gradually lean forward at the slowest possible speed while maximally resisting this movement with both limbs while keeping the trunk and hips in a neutral position throughout, and the hands held across the chest.3 Standardized verbal encouragement was given throughout the range of motion to ensure maximal effort. The investigators closely monitored all trials to ensure proper technique, which, if considered invalid, additional trials were allowed. The results were only visible to the outcome assessor during

the testing and were shown to the player after the completion of all testing. All eccentric strength testing was performed in a rested state before the team training session. Data analysis Force data for both limbs during the NHE were logged to a personal computer at 100Hz through base station receiver (Mantracourt, Devon, UK). Peak force for each of the three repetitions was averaged for all statistical comparisons. Average of both legs was analyzed and reported normalized to body weight (NÂˇkg-1). Inter-limb asymmetry was analyzed using the formula: (strongest limb-weakest limb)/ Total (sum of both limbs); noting that this has been suggested as an appropriate method for computing inter-limb differences from bilateral tests.15 Statistical analysis For descriptive statistics, means and standard deviations (SD) were used for continuous variables, while numbers (percentages) were used for dichotomous variables. Simple linear regression models were performed to investigate the differences in preseason eccentric hamstring strength on soccer players including 1) age, 2) previous season hamstring injury, and 3) hamstring injury duration of three weeks or less and more than three weeks. Preseason eccentric hamstring strength was included as the dependent variable, while age, previous season hamstring injury and hamstring injury duration, respectively, were included as the independent variables of interest. Moreover, two standard multiple regressions were performed for previous season hamstring injury and hamstring injury duration, including age as covariate. Confidence intervals were set at 95% for all analyses. All the assumptions for all regression models were met. Estimates of the differences in eccentric hamstring strength were presented as absolute mean differences and percentages â&#x20AC;&#x201C;by dividing the absolute mean difference by the estimated mean of the reference group. All statistical analyses were performed using SPSS v22.0.0.1 (IBM Corporation, Chicago, IL). Players with incomplete data, due to time constraints during testing or not completing three valid repetitions for other reason were not included in the analyses. Hence, data were analyzed as complete cases (no imputation of

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missing data). Information regarding missing data are provided in Figure 1. RESULTS In total, 284 amateur male players were included in the analyses (age=23±4years; weight=74.0±7.8kg; height=178.3±6.4cm; see Table 1 and Figure 1). Twenty-two players did not complete testing and were not included in the analyses. From the 284 players, 56 (19.7%) had sustained a hamstring injury in

the previous season. From those injured players, 29 (51.8%) reported having a hamstring injury duration of three weeks or less, whereas 27 players (48.2%) reported having a hamstring injury of more than three weeks. Between limb asymmetry was present in both injured and uninjured groups (Table 1). Age had a significant negative association with preseason eccentric hamstring strength with a mean reduction of 0.9% per year increase in player’s

Figure 1. Flowchart of participants.

Table 1. Descriptives (Mean ± SD) for age, weight, height and eccentric hamstring strength.

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Table 2. Estimates from simple linear regressions of age, previous hamstring injury and hamstring injury duration.

age (Table 2, 1a; Figure 2). Players with previous hamstring injury had 7% lower preseason eccentric hamstring strength compared to players with no previous hamstring injury (Table 2, 1b). When adjusting for age (Table 3, Model A), players with a previous hamstring injury had a non-significant difference (5%) in preseason eccentric hamstring strength compared to players with no previous hamstring injury. Players with hamstring injury duration of more than three weeks had 13% lower preseason eccentric hamstring strength compared to players with no previous hamstring injury (Table 2, 1c). When adjusting for age (Table 3, Model B), players with a hamstring injury duration of more than three weeks had 9% lower preseason eccentric hamstring strength compared to players with no previous hamstring injury. Players with a hamstring injury duration of three weeks or less had no difference in preseason eccentric hamstring strength compared to players with no previous hamstring injury in any of the analyses (Table 2, 1c; and Table 3, Model B). DISCUSSION This study is the first to investigate how age and previous season hamstring injury are associated with preseason eccentric hamstring strength in a large cohort of male amateur soccer players using an on-field and time-efficient testing device (the NHE device). The most important findings of this study are the negative association of age and previous hamstring injury duration (more than three weeks) with preseason eccentric hamstring strength.

Figure 2. Scatter plot of age (years) and eccentric hamstring strength (NÂˇkg-1). Triangles represent individual players without previous hamstring injury; circles represent individual players with previous hamstring injury.

Estimates revealed that a 0.9% decrease in strength could be expected for a year increase in player age. This is a small but important association, considering that in 10 years of age difference, a reduction of 9% on preseason eccentric hamstring strength may be present (0.5NÂˇkg-1 or 37N for a 74kg soccer player). Moreover, players with a hamstring injury duration of more than three weeks had 9% lower preseason eccentric hamstring strength compared to players with no previous hamstring injury. Taking these results together, older and previously injured soccer players had even lower preseason eccentric hamstring strength compared to younger and noninjured counterparts. These results are relevant since prospective studies have shown that higher

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Table 3. Estimates from multiple regressions of previous hamstring injury and duration including age as a covariate.

levels of eccentric hamstring strength were important in older and previously injured soccer1 and AFL2 players to reduce the odds of sustaining future HSI injuries. Hamstring strength deficits after a hamstring injury have been addressed in the literature before,8 however, those studies were performed in a mixed group of athletes, with smaller sample sizes, and using other testing devices such isokinetic dynamometry. Furthermore, previous studies have not accounted for any possible impact of prior injury severity. The current data showing the negative association of age with preseason eccentric hamstring strength in amateur soccer players is a novel finding. Although increasing age has been identified as a potential risk factor for HSI in soccer players5,6 no convincing explanation has been given as to why older players are at significantly greater risk than younger players.7 The results of the present study, showing a decrease in strength related to increasing age, may partly explain the increased risk of future HSI in older soccer players.5,6 Also, this relationship between reduced eccentric hamstring strength and age could be also explained by a longer exposure to soccer or history of several HSIs (preceding the previous season), which has not been recorded in this study. Furthermore, the impact of age on eccentric hamstring strength may be greater in amateur than professional soccer players given that the former are less likely to engage in frequent and supervised strength training. Future investigations should consider prioritising serial monitoring of hamstring eccentric strength during the season to establish

trends and the relationship between strength other variables such as training load. Previous hamstring injury duration of more than three weeks was associated with low preseason eccentric hamstring strength, regardless of player age in the present study. Conversely, previous hamstring injuries of shorter duration did not affect eccentric hamstring strength. This finding is supported by previous studies linking injury duration, which is likely a surrogate measure for injury severity, to a higher degree of neuromuscular maladaptation (neuromuscular inhibition, selective hamstring atrophy, and shifts in the torque-joint angle relationships) and consequently an increased deficit in eccentric hamstring strength.7,9â&#x20AC;&#x201C;11 Hence, looking at hamstring injury duration instead of previous hamstring injury may be a more relevant approach to classify amateur soccer players with suspected lower levels of eccentric hamstring strength and greater propensity to sustain future HSI in the new season. The existing evidence regarding the deficits in eccentric hamstring strength after an HSI is mixed,8 perhaps partly because a diversity of methods are used and heterogeneous populations are compared. One previous study has used the NHE device to measure eccentric hamstring strength in professional AFL players.16 Players with previous HSI displayed higher eccentric hamstring strength compared to players without HSI at preseason testing.16 The differences between these findings may be related to training practices, as professional AFL players may have more strictly supervised rehabilitation programs than amateur soccer players. We would assume that

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a vast majority of professional AFL players might be performing intense eccentric hamstring strength exercises during rehabilitation17 while most amateur soccer players may not. Eccentric hamstring strength can be improved through strength exercises18 and intervention studies suggest that eccentric hamstring exercises are effective at improving strength,19,20 hamstring muscle volume and cross-sectional area20 and fascicle length in the long head of the biceps femoris.20 Performing eccentric hamstring exercises such as the NHE reduces the risk of future HSI in both amateur21,22 and professional soccer players,21 possibly as a consequence of increased eccentric hamstring strength and also neuromuscular and architectural adaptations. Those studies revealed that HSI incidence, but not severity, can be reduced to approximately one-third of those in control teams by an NHE intervention.21,22 Moreover, previously injured players who employed the NHE were approximately six times less likely to suffer a recurrence than previously injured players from control teams.21 These results may give an insight into previous findings, since a decrease in eccentric hamstring strength following a hamstring injury duration of more than three weeks is likely to be carried into the following season unless it is countered by the implementation of adequate reconditioning. Considering that training loads may also be a crucial component for injury risk management,23 it seems that stronger and fitter players better tolerate high increases in training load24 which highlights the importance of assessing players strength levels at the beginning of the season. Interestingly, the present study found that amateur soccer players with a previous history of hamstring injury of more than three weeks had reduced eccentric hamstring strength at the beginning of a soccer season, while eccentric hamstring strength was also lower in older amateur soccer players. Importantly, those two factors are not exclusive, meaning that older soccer players with a history of hamstring injury will present with even more accentuated decrements in eccentric hamstring strength. Altogether, those findings highlight the importance of monitoring eccentric strength and implementing adequate conditioning emphasising older players and players with a more severe hamstring injury history.

It should be acknowledged that some limitations are present in the current study. First, the retrospective recollection of injury history limits the accuracy of the data on injury duration. Recall bias associated with the use of a self-reported injury history questionnaire from the previous season may be present. However, in order to minimize recall bias, the injury form comprised a small number of simple questions including a clear definition of injury and also details in relation to anatomical regions, which has shown to result in better recall.25 Furthermore, we also limited the time-frame of injury reporting to 12 months, since this has been shown to reduce the impact of recall bias.26 CONCLUSIONS Amateur soccer players with a hamstring injury of more than three weeks in the previous season present with lower eccentric hamstring strength at the beginning of the soccer preseason. Moreover, increasing age is associated with a decrease in eccentric hamstring strength in amateur soccer players. These results highlight the need to monitor and consequently address identified weaknesses in eccentric hamstring strength in amateur football players, with specific emphasis on older players with a previous hamstring injury of longer duration. REFERENCES 1. Timmins RG, Bourne MN, Shield AJ, Williams MD, Lorenzen C, Opar DA. Short biceps femoris fascicles and eccentric knee ďŹ&#x201A;exor weakness increase the risk of hamstring injury in elite football (soccer): a prospective cohort study. Br J Sports Med. 2015;bjsports-2015-095362. 2. Opar DA, Williams MD, Timmins RG, Hickey J, Duhig SJ, Shield AJ. Eccentric hamstring strength and hamstring injury risk in Australian footballers. Med Sci Sports Exerc. 2015;47(4):857-865. 3. Opar DA, Piatkowski T, Williams MD, Shield AJ. A novel device using the Nordic hamstring exercise to assess eccentric knee ďŹ&#x201A;exor strength: a reliability and retrospective injury study. J Orthop Sports Phys Ther. 2013;43(9):636-640. 4. van Dyk N, Bahr R, Burnett AF, et al. A comprehensive strength testing protocol offers no clinical value in predicting risk of hamstring injury: a prospective cohort study of 413 professional football players. Br J Sports Med. 2017;51(23):16951702.

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5. Henderson G, Barnes CA, Portas MD. Factors associated with increased propensity for hamstring injury in English Premier League soccer players. J Sci Med Sport. 2010;13(4):397-402. 6. Woods C, Hawkins RD, Maltby S, et al. The Football Association Medical Research Programme: an audit of injuries in professional football -analysis of hamstring injuries. Br J Sports Med. 2004;38(1):36-41. 7. Opar DA, Williams MD, Shield AJ. Hamstring strain injuries: factors that lead to injury and re-injury. Sport Med. 2012;42(3):209-226. 8. Maniar N, Shield AJ, Williams MD, Timmins RG, Opar DA. Hamstring strength and ﬂexibility after hamstring strain injury: a systematic review and meta-analysis. Br J Sports Med. 2016;50(15):909-920. 9. Croisier J-L. Factors associated with recurrent hamstring injuries. Sport Med. 2004;34(10):681-695. 10. Silder A, Heiderscheit BC, Thelen DG, Enright T, Tuite MJ. MR observations of long-term musculotendon remodeling following a hamstring strain injury. Skeletal Radiol. 2008;37(12):1101-1109. 11. Fyfe JJ, Opar DA, Williams MD, Shield AJ. The role of neuromuscular inhibition in hamstring strain injury recurrence. J Electromyogr Kinesiol. 2013;23(3):523-530. 12. Bourne MN, Opar DA, Williams MD, Al Najjar A, Shield AJ. Muscle activation patterns in the Nordic hamstring exercise: Impact of prior strain injury. Scand J Med Sci Sport. 2016;26(6):666-674. 13. Esteve E, Rathleff MS, Vicens-Bordas J, et al. Preseason adductor squeeze strength in 303 Spanish male soccer athletes: a cross-sectional study. Orthop J Sport Med. 2018;6(1):232596711774727. 14. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008;61(4):344-349. 15. Bishop C, Read P, Lake J, Chavda S, Turner A. Effects of inter-limb asymmetries on physical and sports performance: A systematic review. Strength Cond J. 2018;36:1135-1144.

16. Opar DA, Williams MD, Timmins RG, Hickey J, Duhig SJ, Shield AJ. The effect of previous hamstring strain injuries on the change in eccentric hamstring strength during preseason training in elite Australian footballers. Am J Sports Med. 2015;43(2):377-384. 17. Pizzari T, Wilde V, Coburn P. Management of hamstring muscle strain injuries in the Australian Football League (AFL): A survey of current practice. J Sci Med Sport. 2010;13:e76. 18. Bourne MN, Timmins RG, Opar DA, et al. An evidence-based framework for strengthening exercises to prevent hamstring injury. Sport Med. 2017. 19. Askling C, Karlsson J, Thorstensson A. Hamstring injury occurrence in elite soccer players after preseason strength training with eccentric overload. Scand J Med Sci Sport. 2003;13(4):244-250. 20. Bourne MN, Duhig SJ, Timmins RG, et al. Impact of the Nordic hamstring and hip extension exercises on hamstring architecture and morphology: implications for injury prevention. Br J Sports Med. 2016:bjsports-2016-096130. 21. Petersen J, Thorborg K, Nielsen MB, BudtzJørgensen E, Hölmich P. Preventive effect of eccentric training on acute hamstring injuries in men’s soccer: a cluster-randomized controlled trial. Am J Sports Med. 2011;39(11):2296-2303. 22. van der Horst N, Smits D-WW, Petersen J, Goedhart EA, Backx FJG. The preventive effect of the Nordic hamstring exercise on hamstring injuries in amateur soccer players: a randomized controlled trial. Am J Sports Med. 2015;43(6):1-8. 23. Gabbett TJ. The training-injury prevention paradox: should athletes be training smarter and harder? Br J Sports Med. 2016:1-9. 24. Malone S, Hughes B, Doran DA, Collins K, Gabbett TJ. Can the workload–injury relationship be moderated by improved strength, speed and repeatedsprint qualities? J Sci Med Sport. 2018;22(1):29-34. 25. Askling C, Lund H, Saartok T, Thorstensson A. Self-reported hamstring injuries in student-dancers. Scand J Med Sci Sports. 2002;12(4):230-235. 26. Gabbe BJ. How valid is a self reported 12 month sports injury history? Br J Sports Med. 2003;37(6):545-547.

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IJSPT

ORIGINAL RESEARCH

ANALYSIS OF TIMING OF SECONDARY ACL INJURY IN PROFESSIONAL ATHLETES DOES NOT SUPPORT GAME TIMING OR SEASON TIMING AS A CONTRIBUTOR TO INJURY RISK Jun Zhou1,2 Nathan D. Schilaty1,3,4 Timothy E. Hewett5,6 Nathaniel A. Bates1,3,4

ABSTRACT Background: Anterior cruciate ligament (ACL) injuries are a common cause of time loss in sports. Approximately one-third of ACL reconstructed athletes who return to sport suffer secondary injury. The presence of fatigue during athletic performance has been hypothesized to increase susceptibility to ACL injury. However, the relative role of fatigue in secondary ACL failures remains unexplored. Purpose: To assess how time elapsed within a game and within a season associate with secondary ACL injury occurrence in international professional athletes and American collegiate athletes. Study Design: Retrospective cohort analysis Methods: The public domain was searched for secondary ACL injuries that occurred during competitive matches between 2000-2018. Demographics (age, height, weight), side of injury, type of injury (contact, noncontact), and timing of injury within competition and within season were determined for each case. Results: Sixty-seven secondary ACL injuries were identified. Within-game, there were no differences in the distribution of ACL injures across each quarter of game time (p = 0.284). This was consistent between sport (p = 0.1200.448). Within-season, there were no differences in the distribution of secondary ACL injures across each quarter of the season (p = 0.491). This was again consistent between sport (p = 0.151-0.872). Relative risk was not found to be significantly greater for any combination of season and game. Conclusion: The results of the current study indicate that the occurrences of secondary ACL injuries were equally distributed with respect to in-game and in-season timing. Both in-game and in-season timing were not significantly different across each individual sport examined. These results implicate that overall there is not an association between fatigue and secondary ACL injury occurrence in professional athletes. Level of Evidence: 3 Keywords: anterior cruciate ligament injury, fatigue, knee, professional athletes, sports injury

Department of Orthopedic Surgery, Mayo Clinic, Rochester, MN, USA; 2 Department of Orthopedic Surgery, The First Afﬁliated Hospital of Soochow University, Suzhou, Jiangsu, China. 3 Sports Medicine Center, Mayo Clinic, Rochester, MN, USA; 4 Department of Physiology & Biomedical Engineering, Mayo Clinic, Rochester, MN, USA; 5 Sparta Science, Menlo Park, CA, USA 6 The Rocky Mountain Consortium for Sports Research, Edwards, CO, USA Acknowledgements: We acknowledge grant funding from NIH R01-AR055563, NIH K12-HD065987, and the Jiangsu Health International Exchange Program (JSH-2018-004).

Conflict of Interest: There are no conflicts of interest of financial relationships to disclose for any of the authors in preparation of this manuscript.

CORRESPONDING AUTHOR Nathaniel A. Bates, PhD 200 First St SW Rochester, MN 55905 E-mail: batesna@gmail.com Telephone: 507-538-6953 Fax: 507-284-5392

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 254 DOI: 10.26603/ijspt20200254

INTRODUCTION Anterior cruciate ligament (ACL) injury is a common sports injury with an estimate in excess of 200,000 annual incidents per year in the United States.1,2 These injuries are particularly prevalent among young athletes, between the ages of 15 and 25,3 and females, who are 2-10 times more likely to experience ACL failure than their male counterparts.4-7 It is estimated that ACL injuries account for 14-17% of all sports-related lower extremity injuries.8 9 Athletes who desire to return to their preinjury activities typically undergo ACL reconstructions (ACLR) to re-establish mechanical knee stability.10 However, these ACLRâ&#x20AC;&#x2122;s fail to fully restore the mechanics of the native knee,11 and between 16-33% of athletes who return to their previous level of sport with ACLR suffer additional ACL ruptures, known as a secondary injuries.12-14 Secondary ACL injures can entail re-tear of the previously injured ACL or subsequent injury to the contralateral ACL.15 A retrospective cohort study that evaluated 17,436 ACLRâ&#x20AC;&#x2122;s found that 4.9% experienced ipsilateral ACL re-injury and 4.2% experienced contralateral ACL injury within five years.16 However, this study population was limited in that athletic activity and subsequent return to athletic activity were not tracked. The higher physical demands on professional athletes put them at a greater risk of injury than the general population;17 therefore, higher rates of injury are expected, and have been observed, in athletic-specific populations that return to sport after ACLR. 12-14 In addition, athletic exposures during competitive game scenarios present considerably higher risk for ACL injury than training sessions.18 Athletes involved in competitive sports activities prior to surgery have an increased risk of revision ACL surgery compared with those not involved in competitive sports.19 Therefore, professional athletes who return to high levels of sport from ACL injuries are highly susceptible to a second ACL injury.14,20,21 Despite growing interest in the relationship between fatigue and ACL injury, the nature of this association, especially with relation to secondary ACL injuries in professional athletes, remains inconclusive. Athletes who participate in high-impact, cutting, and pivoting sports are at risk of sustaining multiple

ACL injuries.22 In general, professional athletes are assumed to be more fatigued in the second half of a game and the second half of a season than in the first halves, respectively. However, this is not a comprehensive interpretation as fatigue can be generated by a sudden spike of activity within a particular game or as a neuromuscular response to cumulative playing time over an extended period, both of which may increase vulnerability to injury.23 Several authors have purported that fatigue propagates deleterious biomechanics as fatigue onset has been associated with increased knee abduction angles and moments,24-28 decreased range of flexion excursion,23,25,26,28-30 increased asymmetry in frontal and sagittal plane knee moments,30 delayed hamstrings neuromuscular activation,31,32 and increased vertical ground reaction and knee joint forces.23,30,33-35 These changes would be indicative of stiffer landing mechanics and decreased energy absorption that correspond with increased ACL injury risk.23,29 However, these principles are not universally accepted as contrarian findings have identified that extended exercise and fatigue increase flexion,24,35-37 increase muscle activation,38 do not influence frontal plane mechanics,23,39 decrease vertical ground reaction forces,40 and decrease load on the ACL.41 Collectively, fatigue-related findings have exhibited limited congruency relative to motion mechanics;23,42 thus, it remains inconclusive as to how fatigue influences injury incidence within athletic exposures. Therefore, the purpose of this investigation was to assess how time elapsed within a game and within a season associate with secondary ACL injury occurrence in international professional athletes and American collegiate athletes. The hypothesis tested was that the occurrence of secondary ACL injuries would be equally distributed with respect to in-game and in-season timing. It was further hypothesized that in-game and in-season timing would exhibit differences between sports. METHODS For this investigation, an internet search was conducted in order to identify professional and American collegiate athletes who had suffered a public and video-documented secondary ACL injury in a game, match, or contest between 2000 - 2018. Game

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scenario ACL injuries were selected for analysis because it allowed the raters to determine the precise timing of injury occurrence and because competitive game scenarios expose a considerably higher risk of ACL injury than training.18 Secondary ACL injures were classified as any additional ACL injuries that occurred after the date of an athlete’s primary ACL injury, and included ipsilateral injuries of an ACLR graft as well as additional ACL injuries contralateral to a previously-injured ACL. The search engines used in this investigation were the news article feature on Google, ESPN, and the ACL Recovery Club’s Twitter feed. Two investigators used the search terms “ACL injury” and “ACL injured” coupled with the major national sports leagues (NFL, NBA, AFL, etc.) to find documented instances of ACL ruptures. For each ACL injury identified, that athlete was subsequently searched for history of prior ACL injury. Inclusionary criteria were restricted to those secondary ACL injuries that occurred within a game, such that the precise time of injury could be documented. Athlete demographics (age, height, weight), side of injury (contralateral, re-tear), and type of injury (contact, noncontact) were also recorded. Type of injury was determined either from recorded video of the injury event and visual observation of whether a direct blow of force was delivered to the knee, or from interpretation of written description. Language such as “when landing” or “while making a cut” was interpreted as noncontact, while language such as “was hit at the knee” or “collided with another player” was interpreted as contact. The injury data search was concluded December 2018. Once an athlete was determined to have sustained multiple ACL injuries, their secondary injuries were investigated to discern in what game of the season and what time point within the game their injury occurred. Any injury event where these two data points could not be extracted was excluded from analysis. Dependent variables included tear location, tear type, number of games played, percentage of season completed, quarter of the game at time of injury, and percentage of game completed prior to injury. For sports that were not pre-divided into quarters based on standard regulations, each quarter of the competition was determined by a percentage of the total time elapsed on the game clock or total innings completed.

Student t-tests were used to assess demographic differences between tear types and sports played (α < 0.05). Bonferroni correction for multiple comparisons were applied when differences between sports were assessed. Sport specific differences were only assessed for those sports that expressed a minimum of seven secondary ACL tears (American football, Australian football, basketball, soccer). Chi-Squared tests of the distribution (α < 0.05) were used to determine if ACL injuries were evenly dispersed within-game and within-season (based on quarters). A relative risk was used to assess the risk for second ACL injury between half-of-season and half-of-game. RESULTS A total of 67 secondary ACL injuries (63 males, 4 females) were identified in professional athletes that participated in Australian Rules Football (AFL), Baseball, Basketball, American Football (Football), Hockey, Rugby, or Soccer at the time of injury (Table 1). Of the secondary injuries documented, 55% were re-tears and 93% occurred in noncontact scenarios. For secondary ACL athletes, the mean age was 26.4 ± 4.6 years, height was 188 ± 9 cm, and weight was 98.3 ± 18.5 kg. There were no differences in age or weight between contralateral and ipsilateral injury presentations (p ≥ 0.569); however, athletes who suffered re-tears were generally 4 cm taller than those who suffered contralateral injury (Pp= 0.033). There were an insufficient number of contact-based secondary ACL injuries to assess demographic differences between contact and noncontact tears. There were also significant demographic differences between sport as basketball athletes with secondary ACL tears were 10 ± 4 cm taller than soccer athletes (p = 0.014) and 8 ± 3 cm taller than American football athletes (p = 0.009). Basketball athletes also weighed 16.5 ± 8.0 kg more than soccer athletes, but 12.8 ± 5.9 kg less than American football athletes (p = 0.035) who were 17.2 ± 5.4 kg and 29.3 ± 6.8 kg heavier than Australian football (p < 0.001) and soccer athletes (p = 0.002), respectively. Within-game there were no differences in the distribution of ACL injuries across each quarter of a game (p = 0.284). These results remained unchanged within each individual sport (p = 0.120-0.448, Figure 1). Timing of second ACL injury within-game

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Table 1. Secondary ACL ruptures identiďŹ ed in professional athletes by sport and type of tear. Data is presented as number of injuries (percentage of population) for the sport speciďŹ ed in each column.

and within-season was consistent between injury type (p = 0.364 & 0.407; Table 2) and sport played (p = 0.736 & 0.555). Within-season, there were no differences in the distribution of second ACL injures across each quarter of the season (p = 0.491, Figure 2). These results remained unchanged within each individual sport (p = 0.151-0.872). Timing of

second ACL injury within-game and within-season was consistent between injury type (p = 0.728 & 0.487) and sport played (p = 0.491 & 0.679). Relative risk between half-of-season and half-of-game where second ACL injury occurred was not found to be significantly greater for any single category (Table 3).

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DISCUSSION The objective of this investigation was to assess how time elapsed within a game and within a season associate with secondary ACL injury occurrence in professional and American collegiate athletes. The primary hypothesis that second injury would be equally distributed across time points in game and across a sports season was supported by the lack of difference in injury incidence recorded between each quarter of athletic competition. The incidence distribution observed in the present investigation supports a prior meta-analysis that found no effect of season or game time on the occurrence of ACL, groin, or hamstring injuries.40 Additional prior reviews also found inconclusive effects of fatigue on motion mechanics.23,42 Inconsistent behavioral Table 2. Timing of secondary ACL rupture by sport (with standard deviations where multiple subjects were observed).

adaptations from fatigue would consequently not be expected to bias injury incidence toward a particular timing aspect of a game or season. Indeed a soccerspecific investigation found that 17 of 78 (22%) ACL injuries occurred within 15 minutes of kickoff (17% of game time).18 This indicates a relatively even distribution of injury incidence compared to the time elapsed and echoes the findings of the present investigation. The demographic data of this study, suggest that a higher center of gravity is more likely to affect the involved side as athletes with ipsilateral re-injury were 4 cm taller than athletes with contralateral tears. Indeed, taller center of mass has been observed in landings with larger vertical ground reaction forces, frontal plane angles, and frontal plane moments,43,44 all of which are known risk factors associated with ACL injury.45 In addition, the differences in athlete height and weight observed between sports may be

Table 3. Relative risk for groups.

Figure 2. (A) Absolute number of ACL injuries that occurred within each quarter of a season separated by sport. (B) Percentage of ACL injuries that occurred within each quarter of a season separated by sport. The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 258

related to center of gravity and balance control, or to sport-specific demands. Therefore, these demographic data may have limited clinical significance, or at least necessitate investigation with a larger dataset to results with greater power. Younger age and a return to high levels of activity following primary ACLR are salient factors associated with secondary ACL injury.14 Professional athletes exhibit higher levels of activity than the general population and often experience sport-specific fatigued conditions due to year-round participation in workouts, practices and games.46 Fatigue and overtraining may compromise coordination as well as athlete awareness, which can subsequently increase the risk of ACL injury.47 Physical fatigue has been tied to mental (i.e. cognitive) fatigue as it might influence oneâ&#x20AC;&#x2122;s abilities to focus on important cues around him/ her, compromise cognitive processing, and impair decision-making.42,48,49 Decreased cognitive function following concussion has been associated with increased ACL injury incidence;50 therefore, cognitive fatigue that results from physical fatigue could also influence ACL incidence rates. However, such a concept was not examined in the present study. Game-context athletic exposures generate considerably higher ACL injury incidence rates than training situations.18 Athletes may experience fatigue as a results of a sudden activity spike during the game or as neuromuscular fatigue because of extended playing time.23 For athletes with prior history of ACL reconstruction, decreases in movement quality were noted with the onset of fatigue, while no such changes were documented in healthy control subjects.51 However, if these deleterious motion changes occurred in the present cohort, they did not influence a biasing of ACL occurrence relative to game time or season time elapsed. Following the onset of fatigue, athletes demonstrate greater vertical ground reaction forces (vGRFs) during landing, regardless of sex.52 As noted, increased frontal plane hip and knee moments and angles, as well as increased hip and knee internal rotation, have been documented as side-effects of fatigue in some investigations.53 Each of these factors are a component of dynamic valgus which is associated with increased risk of non-contact ACL injury in vivo45,54 and increased ACL loading in vitro.55-57 Furthermore, as the body

absorbs vGRFs during movement, if neuromuscular control surrounding the joints is altered due to fatigue, it may increase ligament susceptibility to rupture.58 The present study was unable to estimate specific kinetic and kinematic biomechanical variables during documented injury events. Therefore, the authors were unable to document whether these traits were observed in this cohort of professional athletes. In accordance with the present results, study of male youth elite soccer players showed that soccer-specific fatigue did not increase the risk of ACL or hamstring injury.59 A second soccer-specific study echoed these findings in that no consistent relationship was identified between fatigue, playing time, and injury.18 A third cross-sectional study examined quadriceps muscle fatigue in 17 high-performance soccer players between 5.5 and 7 months after ACL reconstruction.17 The results showed no significant difference between involved and uninvolved limbs regarding local muscle fatigue. As ACL loading and injuries are multi-factorial events across multiple planes of motion,45,56,57,60,61 fatigue as a single factor, may not be sufficient to reliably induce secondary ACL injury in professional athletes. In addition, as professional athletes consistently participate in training and competition, they may be better adapted to functional performance under fatigued conditions than the general population. However, further investigation would be required to confirm or refute this theory. The primary limitation of the present study was that individual participant fatigue was not objectively measured or controlled for. As injury incidence was documented from the public domain, there was no reliable or accurate method available to document individual participant fatigue at the time of injury occurrence. It was generally assumed that as game time and season duration progressed, an athleteâ&#x20AC;&#x2122;s potential level of fatigue would subsequently increase. Based on the reasonable consideration that professional athletes are more overall fatigued in the second half of a game and the second half of a season than in the first half of the game and the first half of the season, only the timing of secondary ACL injury that occurred during the game and the season was analyzed. However, due to large variability in substitution patterns, relative use patterns, positional responsibilities, and individual fitness

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associated with professional sports, the assumption of fatigue onset is not comprehensive or quantifiable. Accordingly, it is difficult to draw direct associations between game time, season time, and player fatigue. If this investigation were to be repeated as a prospective, controlled laboratory study, individual levels of fatigue should be documented and quantified. Such an investigation would still be limited though as fatigue evaluations on an injured player would likely have to be subjective in nature as injury would compromise the integrity and performance of the musculoskeletal system. Alternatively, the establishment of a comprehensive evaluation that could be converted to a quantitative scale for the documentation of relative fatigue in an athlete would be a useful tool to both research and clinical assessment. Similarly, mental fatigue status also went undocumented in the present investigation. Further, while the accuracy of each secondary ACL injury recorded for the present study was verified by two independent observers, it is possible that additional incidences may exist that went undocumented. Identification and inclusion of additional data points always affords the potential to impact the outcomes of statistical analysis. CONCLUSIONS The present results indicate that secondary ACL injury incidence was relatively equally distributed with respect to in-game and in-season timing, as there was a lack of timing differences for athletes who participated in Australian Rules Football, Baseball, Basketball, American Football, Hockey, Rugby and Soccer. The hypothesis was supported, which implied that time elapsed within a match or across a season may not be associated with onset of secondary ACL injuries in professional athletes. REFERENCES 1. Mather RC, 3rd, Koenig L, Kocher MS, et al. Societal and economic impact of anterior cruciate ligament tears. J Bone Joint Surg Am. 2013;95(19):1751-1759. 2. Kim S, Bosque J, Meehan JP, Jamali A, Marder R. Increase in outpatient knee arthroscopy in the united states: A comparison of national surveys of ambulatory surgery, 1996 and 2006. J Bone Joint Surg Am. 2011;93(11):994-1000. 3. Nessler T, Denney L, Sampley J. Acl injury prevention: What does research tell us? Curr Rev Musculoskelet Med. 2017;10(3):281-288.

4. Mihata LC, Beutler AI, Boden BP. Comparing the incidence of anterior cruciate ligament injury in collegiate lacrosse, soccer, and basketball players: Implications for anterior cruciate ligament mechanism and prevention. Am J Sports Med. 2006;34(6):899-904. 5. Stanley LE, Kerr ZY, Dompier TP, Padua DA. Sex differences in the incidence of anterior cruciate ligament, medial collateral ligament, and meniscal injuries in collegiate and high school sports: 20092010 through 2013-2014. Am J Sports Med. 2016. 6. Prodromos CC, Han Y, Rogowski J, Joyce B, Shi K. A meta-analysis of the incidence of anterior cruciate ligament tears as a function of gender, sport, and a knee injury-reduction regimen. Arthroscopy. 2007;23(12):1320-1325, e1326. 7. Fältström A, Kvist J, Gaufﬁn H, Hägglund M. Female soccer players with anterior cruciate ligament reconstruction have a higher risk of new knee injuries and quit soccer to a higher degree than knee-healthy controls. Am J Sports Med. 2018;47(1):31-40. 8. Hootman JM, Helmick CG, Schappert SM. Magnitude and characteristics of arthritis and other rheumatic conditions on ambulatory medical care visits, united states, 1997. Arthritis Rheum. 2002;47(6):571-581. 9. Hootman JM, Dick R, Agel J. Epidemiology of collegiate injuries for 15 sports: Summary and recommendations for injury prevention initiatives. J Athl Train. 2007;42(2):311-319. 10. Frobell RB, Roos HP, Roos EM, Roemer FW, Ranstam J, Lohmander LS. Treatment for acute anterior cruciate ligament tear: Five year outcome of randomised trial. BMJ. 2013;346:f232. 11. Bates NA, Myer GD, Shearn JT, Hewett TE. Anterior cruciate ligament biomechanics during robotic and mechanical simulations of physiologic and clinical motion tasks: A systematic review and metaanalysis. Clin Biomech. 2015;30(1):1-13. 12. Holm I, Oiestad BE, Risberg MA, Gunderson R, Aune AK. No differences in prevalence of osteoarthritis or function after open versus endoscopic technique for anterior cruciate ligament reconstruction: 12-year follow-up report of a randomized controlled trial. Am J Sports Med. 2012;40(11):2492-2498. 13. Paterno MV, Rauh MJ, Schmitt LC, Ford KR, Hewett TE. Incidence of second acl injuries 2 years after primary acl reconstruction and return to sport. Am J Sports Med. 2014;42(7):1567-1573. 14. Wiggins AJ, Grandhi RK, Schneider DK, Stanﬁeld D, Webster KE, Myer GD. Risk of secondary injury in younger athletes after anterior cruciate ligament reconstruction: A systematic review and metaanalysis. Am J Sports Med. 2016;44(7):1861-1876.

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15. Schilaty ND, Nagelli C, Bates NA, et al. Incidence of second anterior cruciate ligament tears and identiﬁcation of associated risk factors from 2001 – 2010 using a geographic database. Ortho J Sports Med. 2017;5(8): DOI: 10.1177/2325967117724196.

27. Lessi GC, Silva RS, Serrao FV. Comparison of the effects of fatigue on kinematics and muscle activation between men and women after anterior cruciate ligament reconstruction. Phys Ther Sport. 2018;31:29-34.

16. Maletis GB, Inacio MC, Funahashi TT. Risk factors associated with revision and contralateral anterior cruciate ligament reconstructions in the kaiser permanente aclr registry. Am J Sports Med. 2015;43(3):641-647.

28. Mejane J, Faubert J, Romeas T, Labbe DR. The combined impact of a perceptual–cognitive task and neuromuscular fatigue on knee biomechanics during landing. The Knee. 2019;26(1):52-60.

17. Cavalcante ML, Teixeira PR, Sousa TC, Lima PO, Oliveira RR. Index of fatigue quadriceps in soccer athletes after anterior cruciate ligament reconstruction. Rev Bras Ortop. 2016;51(5):535-540. 18. Walden M, Hagglund M, Magnusson H, Ekstrand J. Anterior cruciate ligament injury in elite football: A prospective three-cohort study. Knee Surg Sports Traumatol Arthrosc. 2011;19(1):11-19. 19. Yabroudi MA, Bjornsson H, Lynch AD, et al. Predictors of revision surgery after primary anterior cruciate ligament reconstruction. Ortho J Sports Med. 2016;4(9): DOI: 10.1177/2325967116666039. 20. Anand BS, Feller JA, Richmond AK, Webster KE. Return-to-sport outcomes after revision anterior cruciate ligament reconstruction surgery. Am J Sports Med. 2016;44(3):580-584. 21. Webster KE, Feller JA, Leigh WB, Richmond AK. Younger patients are at increased risk for graft rupture and contralateral injury after anterior cruciate ligament reconstruction. Am J Sports Med. 2014;42(3):641-647. 22. Webster KE, Feller JA, Kimp AJ, Whitehead TS. Low rates of return to preinjury sport after bilateral anterior cruciate ligament reconstruction. Am J Sports Med. 2019;47(2):334-338. 23. Benjaminse A, Webster KE, Kimp A, Meijer M, Gokeler A. Revised approach to the role of fatigue in anterior cruciate ligament injury prevention: A systematic review with meta-analyses. Sports Med. 2019;49(4):565-586. 24. Shultz SJ, Schmitz RJ, Cone JR, et al. Changes in fatigue, multiplanar knee laxity, and landing biomechanics during intermittent exercise. J Athl Train. 2015;50(5):486-497. 25. Collins JD, Almonroeder TG, Ebersole KT, O’Connor KM. The effects of fatigue and anticipation on the mechanics of the knee during cutting in female athletes. Clin Biomech. 2016;35:62-67. 26. Barber-Westin SD, Noyes FR. Effect of fatigue protocols on lower limb neuromuscular function and implications for anterior cruciate ligament injury prevention training: A systematic review. Am J Sports Med. 2017;45(14):3388-3396.

29. O’Connor KM, Johnson CP, Benson LC. The effect of isolated hamstrings fatigue on landing and cutting mechanics. J Appl Biomech. 2015;31(4):211-220. 30. Briem K, Jonsdottir KV, Arnason A, Sveinsson T. Effects of sex and fatigue on biomechanical measures during the drop-jump task in children. Ortho J Sports Med. 2017;5(1): DOI: 10.1177/2325967116679640. 31. De Ste Croix MBA, Priestley AM, Lloyd RS, Oliver JL. Acl injury risk in elite female youth soccer: Changes in neuromuscular control of the knee following soccer-speciﬁc fatigue. Scand J Med Sci Sports. 2014;25(5):e531-e538. 32. Behrens M, Mau-Moeller A, Wassermann F, Plewka A, Bader R, Bruhn S. Repetitive jumping and sprinting until exhaustion alters hamstring reﬂex responses and tibial translation in males and females. J Orthop Res. 2015;33(11):1687-1692. 33. Dickin DC, Johann E, Wang H, Popp JK. Combined effects of drop height and fatigue on landing mechanics in active females. J Appl Biomech. 2015;31(4):237-243. 34. Khalid AJ, Harris SI, Michael L, Joseph H, Qu X. Effects of neuromuscular fatigue on perceptualcognitive skills between genders in the contribution to the knee joint loading during side-stepping tasks. J Sports Sci. 2015;33(13):1322-1331. 35. Schmitz RJ, Kim H, Shultz SJ. Neuromuscular fatigue and tibiofemoral joint biomechanics when transitioning from non-weight bearing to weight bearing. J Athl Train. 2015;50(1):23-29. 36. Frank BS, Gilsdorf CM, Goerger BM, Prentice WE, Padua DA. Neuromuscular fatigue alters postural control and sagittal plane hip biomechanics in active females with anterior cruciate ligament reconstruction. Sports Health. 2014;6(4):301-308. 37. Xia R, Zhang X, Wang X, Sun X, Fu W. Effects of two fatigue protocols on impact forces and lower extremity kinematics during drop landings: Implications for noncontact anterior cruciate ligament injury. J Healthc Eng. 2017;2017:5690519. 38. Lessi GC, Serrao FV. Effects of fatigue on lower limb, pelvis and trunk kinematics and lower limb muscle activity during single-leg landing after anterior

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cruciate ligament reconstruction. Knee Surg Sports Traumatol Arthrosc. 2017;25(8):2550-2558. 39. Tamura A, Akasaka K, Otsudo T, Shiozawa J, Toda Y, Yamada K. Dynamic knee valgus alignment inﬂuences impact attenuation in the lower extremity during the deceleration phase of a single-leg landing. PLoS ONE. 2017;12(6):e0179810. 40. Doyle TLA, Schilaty ND, Webster KE, Hewett TE. Time of season and game segment is not related to likelihood of lower-limb injuries: A meta-analysis. Clin J Sport Med. 2019. Epub ahead of print: DOI: 10.1097/JSM.0000000000000752. 41. Smith CM, Housh TJ, Hill EC, Keller JL, Johnson GO, Schmidt RJ. Co-activation, estimated anterior and posterior cruciate ligament forces, and motor unit activation strategies during the time course of fatigue. Sports (Basel). 2018;6(4) : DOI: 10.3390/ sports6040104.

50. McPherson AL, Nagai T, Webster KE, Hewett TE. Musculoskeletal injury risk after sport-related concussion: A systematic review and meta-analysis. Am J Sports Med. 2018:036354651878590. 51. van Melick N, van Rijn L, Nijhuis-van der Sanden MWG, Hoogeboom TJ, van Cingel REH. Fatigue affects quality of movement more in acl-reconstructed soccer players than in healthy soccer players. Knee Surg Sports Traumatol Arthrosc. 2019;27(2):549-555. 52. Brazen DM, Todd MK, Ambegaonkar JP, Wunderlich RE, Peterson C. The effect of fatigue on landing biomechanics in single-leg drop landings. Clin J Sport Med. 2010;20(4):286-292. 53. Borotikar BS, Newcomer R, Koppes R, McLean SG. Combined effects of fatigue and decision making on female lower limb landing postures: Central and peripheral contributions to acl injury risk. Clin Biomech. 2008;23(1):81-92.

42. Almonroeder TG, Tighe SM, Miller TM, Lanning CR. The inﬂuence of fatigue on decision-making in athletes: A systematic review. Sports Biomech. 2019;14:1-14.

54. Myer GD, Heidt RS, Waits C, et al. Sex comparison of familial predisposition to anterior cruciate ligament injury. Knee Surg Sports Traumatol Arthrosc. 2014;22(2):387-389.

43. Bates NA, Ford KR, Myer GD, Hewett TE. Impact differences in ground reaction force and center of mass between the ﬁrst and second landing phases of a drop vertical jump and their implications for injury risk assessment. J Biomech. 2013;46(7):1237-1241.

55. Kiapour AM, Demetropoulos CK, Kiapour A, et al. Strain response of the anterior cruciate ligament to uniplanar and multiplanar loads during simulated landings: Implications for injury mechanism. Am J Sports Med. 2016;44(8):2087-2096.

44. Bates NA, Ford KR, Myer GD, Hewett TE. Timing differences in the generation of ground reaction forces between the initial and secondary landing phases of the drop vertical jump. Clin Biomech. 2013;28(7):796-799.

56. Bates NA, Nesbitt RJ, Shearn JT, Myer GD, Hewett TE. Knee abduction affects greater magnitude of change in acl and mcl strains than matched internal tibial rotation in vitro. Clin Orthop Relat Res. 2017;475:2385-2396.

45. Hewett TE, Myer GD, Ford KR, et al. Biomechanical measures of neuromuscular control and valgus loading of the knee predict anterior cruciate ligament injury risk in female athletes: A prospective study. Am J Sports Med. 2005;33(4):492501.

57. Bates NA, Schilaty ND, Nagelli CV, Krych AJ, Hewett TE. Multiplanar loading of the knee and its inﬂuence on acl and mcl strain during simulated landings and noncontact tears. Am J Sport Med. 2019;47(8):1844-1853.

46. Dodson CC, Secrist ES, Bhat SB, Woods DP, Deluca PF. Anterior cruciate ligament injuries in national football league athletes from 2010 to 2013: A descriptive epidemiology study. Ortho J Sports Med. 2016;4(3): DOI: 10.1177/2325967116631949. 47. Elliot DL, Goldberg L, Kuehl KS. Youngwomen’s anterior cruciate ligament injuries: An expanded model and prevention paradigm. Sports Med. 2010;40(5):367-376. 48. Ivarsson A, Johnson U, Lindwall M, Gustafsson H, Altemyr M. Psychosocial stress as a predictor of injury in elite junior soccer: A latent growth curve analysis. J Sci Med Sport. 2014;17(4):366-370. 49. Chaudhari A, Behan PO. Fatigue and basal ganglia. J Neurol Sci. 2000;179:34-42.

58. Myer GD, Ford KR, Hewett TE. Rationale and clinical techniques for anterior cruciate ligament injury prevention among female athletes. J Athl Train. 2004;39(4):352-364. 59. Lehnert M, Croix MDS, Xaverova Z, et al. Changes in injury risk mechanisms after soccer-speciﬁc fatigue in male youth soccer players. Journal of Human Kinetics. 2018;62(1):33-42. 60. Boden BP, Sheehan FT, Torg JS, Hewett TE. Noncontact anterior cruciate ligament injuries: Mechanisms and risk factors. J Am Acad Orthop Surg. 2010;18(9):520-527. 61. Bates NA, Schilaty ND, Nagelli CV, Krych AJ, Hewett TE. Validation of non-contact anterior cruciate ligament tears produced by a mechanical impact simulator against the clinical presentation of injury. Am J Sport Med. 2018;46(9):2113-2121.

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IJSPT

CASE SERIES

AN EXPLORATORY CASE SERIES ANALYSIS OF THE USE OF PRIMAL REFLEX RELEASE TECHNIQUE™ TO IMPROVE SIGNS AND SYMPTOMS OF HAMSTRING STRAIN Erica S. Albertin, DAT, AT, PES1 Maisie Walters, DAT, AT, CSCS2 James May, DAT, LAT, ATC3 Russel T Baker, Ph.D, LAT, ATC4 Alan Nasypany, Ed.D., LAT, ATC5 Scott Cheatham, Ph.D., DPT, PT, OCS, ATC, CSCS6

ABSTRACT Background/Purpose: Hamstring strain (HS), a common condition found among the injured physically active population, is often treated with rest, stretching, and modalities. Primal Reflex Release Technique™ (PRRT™) is a manual therapy technique used to treat pain caused by over-stimulation of the body’s primal reflexes. The purpose of this case series was to explore the immediate effects of PRRT™ for treating hamstring strains. Description of Cases: A multi-site case series approach was used to report on the treatment of six patients with HS using PRRT™. The Numeric Pain Rating Scale (NPRS), Patient Specific Functional Scale (PSFS) and range of motion (ROM) measurements were collected, as well as evaluation of symmetry of the sacroiliac joints, reported as sacroiliac dysfunction(SJD). Outcomes: Primal Reflex Release Technique™ (PRRT™) was an effective treatment for subjects with HS. Subjects reported a significant decrease in pain on the NPRS, averaging five points over the course of the treatment (95% CI of 3.374, 6.626). Functional measures on the PSFS were significantly improved following treatment (post-treatment mean = 7.8 ± 1.84, pre-treatment mean = 4.8 ± .97, p< .001; CI: -2.1, -3.9). The mean change on the Passive Knee Extension Test (PKE) (mean = 8.20° ± 3.96°) and ASLR (mean = 10.333° ± 8.98°) indicated statistically significant improvements of post-treatment ROM (mean change = 8.20° ± 3.96°, p= .01). The presence of SJD was observed in all subjects prior to treatment and resolved in all subjects when reassessed after treatment. Discussion: In this case series, the use of PRRT™ resulted in decreased pain, increased function, and increased range of motion, as well as resolved SJD. The Primal Reflex Release Technique™ may be useful in decreasing symptoms of HS acutely, but long-term effects are unknown at this time. Clinicians should consider using a treatment which targets the autonomic nervous system when addressing pain associated with HS. Level of Evidence: Level 4 - case series Keywords: Autonomic nervous system, primal reflex, sacroiliac joint dysfunction, up-regulation

Goshen College, Goshen, IN, USA Carroll College and Helena Orthopedic Clinic, Helena 3 University of Idaho, Moscow, ID, USA 4 University of Idaho, Moscow, ID, USA 5 University of Idaho, Moscow, ID, USA 6 California State University Dominguez Hills in Carson, California, USA 2

The authors have no ﬁnancial or proprietary interest in the materials presented herein.

CORRESPONDING AUTHOR Erica Albertin 1700 S Main Street Goshen, IN, 46526 574-535-7417 E-mail: erica.albertin@outlook.com

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 263 DOI: 10.26603/ijspt20200263

INTRODUCTION The incidence and re-injury rates of hamstring strain (HS) in the physically active have not improved over the past thirty years.1 The hamstrings continue to be the most commonly strained multi-joint muscle group in the active population.2-5 For example, Serner et al. reported that 8-18% of all soccer injuries are HS related.6 Although researchers currently debate the primary cause of HS, possible contributing factors include decreased hamstring length, previous HS injury, and/or muscle imbalances between the hamstring and quadriceps muscles.7 Diagnosis of HS severity is traditionally based on clinical signs and symptoms collected from the history and physical examination.8,9 The physical examination includes palpation for tenderness, swelling, and/or deformity, manual muscle testing, and bilateral range of motion assessment.8 Generally, clinicians utilize the grading scale to classify a first, second or thirddegree strain based on signs and symptoms found during the clinical exam (Table 1).9 The presence of pelvic abnormalities in soccer players has been linked to hamstring dysfunction and muscle strain.10-14 Previously, Cibulka, Rose, Delitto, and Sinacore15 reported participants diagnosed with HS also commonly present with sacroiliac joint dysfunction (SJD), which was defined as asymmetrical innominates. Treatment incorporating manipulation of the sacroiliac (SI) joint with a high velocity manipulation (HVLA) resulted in increased ability to create force in the hamstrings (as indicated by increased peak hamstring torque) and also resolved SJD.15 Asymmetrical iliac bones or malalignment of the innominates (i.e., SJD) may add tension to muscles that are attached to the pelvic girdle,16 which

may predispose a patient to mechanical injury at the hamstrings.17 After injury, the autonomic nervous system (ANS) may remain in a heightened state of sensitivity in order to protect from further injury. This state may be referred to as “up-regulated” and can be associated with pain, muscle spasm, muscle guarding, and altered motor behavior.18 An intervention aimed at down regulation of the nerves innervating the hamstring muscles may be helpful in addressing the symptoms of up-regulation and HS compared to traditional treatments that address tissue healing through lengthening or strengthening the hamstring muscle. The Primal Reflex Release Technique™ (PRRT™) is a treatment paradigm theorized to decrease pain and muscle spasm by targeting, resetting reflexes, and using reciprocal inhibition to “down regulate” the autonomic nervous system (ANS).18 Reflexes can produce protective muscle contraction during the fight or flight response after injury.19 The ANS enacts a release of messenger chemicals including acetylcholine20 and serotonin19 which reinforces the protective spasm or trigger points while the patient’s pain continues. The overactive neurons create a cutaneous or nociceptive stimulus affecting the muscle spindles that in turn affect the length and tension of a muscle.21 When mechanical tension is present, as a result of up-regulated areas of facilitated muscle(s), stimulation of reflexes may be beneficial as a treatment because as the “the agonist muscle receives a nerve impulse to contract, its antagonist simultaneously receives an impulse to relax.”22 Targeting reflexes to stimulate a contraction of the antagonist muscle can be used to produce a signal from the ANS to relax the protective mechanisms in the

Table 1. Muscle grading.9

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agonist muscle.23 The Primal Reflex Release Technique™ utilizes the relationship between agonist and antagonist muscles to increase the afferent activity gained from the mechanoreceptors, resulting in a neurological downregulation of the muscles.23 The Primal Reflex Release Technique™ may be suited for patients diagnosed with HS because PRRT™ utilizes reflexive stimulation to downregulate the protective response of the ANS to treat both pain in the musculoskeletal system and address possible upregulation or protective muscle contractions.18 A cluster protocol of five PRRT™ techniques has been introduced as a recommended treatment for the hamstring muscles, addressing the reflexes along the sciatic nerve pathway.24 The purpose of this case series was to explore the immediate effects of PRRT™ for treating hamstring strains. METHODS Description of Cases: Subject History and Systems Review Ethical approval was obtained from the Institutional Review Board prior to beginning data collection; signed informed consent was collected from each participant prior to study inclusion. The study was conducted using six patients who presented to the athletic training clinics at two locations (Clinic A had three patients, Clinic B had three patients) with hamstring pain. Patient histories are presented in Table 2. Subjects were excluded if any overt neurologic signs/conditions, such as sensory paresthesia or motor paresis, present during the initial evaluation or if the patient had a medical history of recent fracture, previously diagnosed neurological condition, or previous spinal surgery. Clinical Impression #1 Subjects were included in the study if they had the presence of signs and/or symptoms of HS, all subjects presented with grade one HS (Table 1).9 The signs and symptoms of a HS matched those used in the previous study assessing SJD and hamstring strains and were defined as pain and/or ecchymosis localized to involved muscle, pain on resistive isometric position (knee flexion with hip extension),

and/or pain on passive range of motion (PROM) of the involved muscle (hip flexion with the knee flexed and extended).15 Examination and Reliability The initial examination included an extensive history relating to pain location, intensity, and mechanism of injury. All subjects (N = 6) presented to the athletic training clinic within 72 hours after feeling pain in their hamstring during activity (pain was not reported prior to the activity). The examination also included an assessment of SJD defined as an examination of innominate alignment.15, 25 Both investigators utilized the same protocol for assessing the level of the anterior superior iliac spine (ASIS).25 The subjects were assessed in supine and standing positions and the SI joint at the posterior superior iliac spine (PSIS) with movement during weight bearing forward flexion of the hips, standing hip and knee flexion (marching) alternating legs, and supine leg-length assessments.25 Sacroiliac joint dysfunction was noted with positive or negative results on these three special tests pre and postintervention, a negative result was only recorded if all three tests were negative.25 If one, two, or three of the tests were positive, the result recorded was positive.25 Assessment of SJD was categorized as asymmetrical (positive) or symmetrical (negative).15,25 Each investigator collected passive knee extension test (PKET) and active straight leg raise (ASLR) measurements at their respective clinics, and intrarater reliability was established for each rater prior to data collection (Table 3). Reliability in assessing SJD is reported to range between excellent reliability (Kappa coefficient of .88)26 and poor reliability (kappa range of .11 to .23).27 Importantly, reliability increases with cluster testing of pain provocation tests (five positive tests resulted in a specificity of .88).28 In cases where pain may originate away from the site of dysfunction (known as regional interdependence),29 identifying the presence of SJD even when pain is not present may be helpful. The first investigator had seven years of athletic training experience. The second investigator had 11 years of athletic training experience. Both investigators completed the PRRT™ home-study course24 and a levelone PRRT™ course prior to completing the study.30

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Table 2. Narrative summary of initial ďŹ ndings.

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Table 3. Intra-rater reliability for range of motion.

In this case series, the researchers used PRRT™, and collected outcomes for pain, function, range of motion and SJD. Patient outcomes were collected using the Numeric Pain Rating Scale (NPRS) and the Patient Specific Functional Scale (PSFS). Clinicianrated outcomes were collected in the form of rangeof-motion (ROM) measurements for PKET and ASLR along with SJD. Clinical Impression #2 The subjects all were within normal limits for manual muscle testing (knee flexion, knee extension, hip flexion). Two of the six subjects had decreased ASLR results compared to normal ranges prior to treatment while PKET measurements were all limited compared to reported norms (Table 2). All six subjects were categorized as asymmetrical SJD (positive tests) prior to treatment. INTERVENTION Outcome Measures The NPRS and PSFS were collected at initial evaluation and following the first treatment. Patients were asked to rate their pain on a scale of 0-10 (0 = no pain; 10 = worst pain imaginable).31 An improved change in score of 2 points (or more) on the NPRS indicate a minimally clinically important difference (MCID).32 The clinicians used the PSFS score to determine the functional status of the patient.33 The patient self-selected two to three functional measures (tasks) and rated their ability to complete each task (0 = unable to perform an activity; 10 = able to perform an activity at the same level as before the injury).33 The minimal detectable change (MDC) is three points for an average of the three functions and is two points for a single function.34 The clinician-rated outcomes obtained were PKE and ASLR range-of-motion measurements at initial evaluation and following the first treatment. The clinician

recorded the outcome of SJD on all tests (standing flexion test, sitting forward flexion test, and prone knee flexion test). Treatment Procedure Each subject, after consenting and meeting inclusion criteria, was treated using similar methods as Cibulka, et al,15 however, in the current study, the use of PRRT™ treatment replaced the HVLA manipulation. Prior to treatment, each patient used a moist heat pack for 10 minutes on the involved hamstring in order to replicate the Cibulka study.15 The following techniques of PRRT™ were then completed: plantar reflex (primal), SI/Lumbar and L1 release, hamstring release, gastrocnemius release and eversion release as recommended in the PRRT guidelines.30 This cluster protocol of five PRRT™ techniques were chosen to focus on downregulating musculature of the posterior chain and targeting the specific release of the sciatic nerve.30 Each technique was applied for 12 seconds exept for the planar reflex which was held for one minute. All patients were treated following the same protocol. The plantar reflex is used to treat lower quarter pain conditions from the lumbar area down to the foot.18 The patient, was positioned supine with the foot over the edge of the plinth (Figure 1), and was asked to hold a pencil between his toes while maintaining full plantar flexion and the motion of inversion to eversion for one minute. The SI/Lumbar and L1 release was used to address an upregulation of the ANS specific to the coccyx, SI, Lumbar, or L1 areas.18 The patient was positioned supine on the plinth (Figure 2). The patient was asked to bend their affected-side knee to 90 degrees and move the knee over the unaffected-side leg. The clinician stood on the unaffected side and provided static resistance as the patient contracted

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Figure 1. Plantar Release PRRT™: Patient plantar-ﬂexes ankle and holds pen with toes for 1 minute.

Figure 2. S1/Lumbar Release PRRT™: Patient adducts leg with hip ﬂexion. The clinician resists against abduction of the hip.

hip abductors. The patient was then asked to hold isometric abduction and external rotation against the clinician with the affected side while hiking the opposite hip upward.18 The patient slowly exhaled while performing the technique for 12 seconds for one application.18 The hamstring release was used to address an upregulation of the ANS for the hamstring area.18 The patient was positioned in supine, and the involved hip was flexed to 45 degrees (Figure 3). The knee was flexed to 20 degrees. The Simultap technique was then applied for 12 seconds: The clinician tapped (i.e., stimulate deep tendon reflex) on two separate

Figure 3. Hamstring Release PRRT™: Patient hip ﬂexes to 90 degrees, knee ﬂexed Simultaps hamstring tendons and patellar tendon.

Figure 4. Patient hip-flexes and knee-flexes; clinician to 90 degrees; clinician simultaps on patellar tendon and on dorsiflexors of ankle.

areas at the same time. In this case, the Simultap was used for the mid-belly of the hamstring (involved) and the patellar tendon. The gastrocnemius release was applied as a fourth PRRT™ component to treat lower quarter pain (Figure 4).18 The patient was positioned in supine, and the hip and knee were flexed (45 degrees and 90 degrees respectively) with the ankles in 90 degrees of dorsiflexion. A Simultap was used on the ankle dorsiflexors and the patellar tendon.18 For consistency with the Cilbulka et al. case report, following the PRRT™ treatment the clinician began passive stretching of the patient’s hamstring (Figure 5). The clinician completed three

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Pain: Numeric Pain Rating Scale Pain scores on the NPRS (N=6) averaged 5.7 pretreatment and .67 immediately following the PRRT™ treatment. A statistically significant difference from the pre- (5.67 ± .33) to post-test measurement (.67 ± .33) was found (t(6) = 7.91 p = .001, two-tailed). The Cohen’s d value of 6.1 suggests a large effect size from the NPRS rating pre-treatment to post-treatment.35 The mean decrease in pain was 5.0, which exceeds the MCID of 2.0 and is clinically significant.32

Figure 5. Stretching Passive Hamstring Technique: Clinician moves leg to hip ﬂexion and knee extension and holds at end; patient stretches for 30 seconds.

repetitions of 30-second holds at the patient’s point of comfort. RESULTS AND OUTCOMES Both clinician and patient rated outcomes were assessed prior to and following treatment to the six patients treated with PRRT™. Outcomes of NPRS, PSFS and range of motion were both clinically and statistically significant different compared to pre-treatment measurements with an a priori alpha level set at .05 and 95% confidence intervals (Table 4). Paired t-tests of pre-treatment and post-treatment measurements were performed on range of motion (both PKET and ASLR). Cohen’s d effect sizes were calculated using the formula d = (M2 - M1) ⁄ SDpooled where M equals the mean and SD is the pooled standard deviation (Table 4).35

Function: Patient Speciﬁc Functional Scale and Range of Motion The mean functional score of 7.8 was calculated for the six subjects indicating a high level of function was present after the PRRT™ treatment compared to a mean score of less than five (4.8) for the scores prior to treatment. A statistically significant difference from the pre- (4.8 ± .94) to post-test measurement (7.8 ± 1.86) was found (t(6) = 3.526, p = .000, two-tailed). Analysis of the change in mean PSFS scores from pretreatment to post treatment scores 35, 36 resulted in a Cohen’s d of 1.9, suggesting a large effect size from the treatment.35 Five of the six patients exceeded a large change MCID of 2.7 in total PSFS mean score. 34 All PSFS results, including specific tasks for each subject, can be seen in Table 5. Passive Knee Extension Test An immediate increase in the mean range of motion measurement of PKET was found from pre to posttreatment (mean of 8.20 degrees). A statistically significant difference between the pre-PKET (mean = 58.40° ± 8.82°) and the post-PKET (mean = 66.60°

Table 4. Change in overall patient and clinician outcomes from initial evaluation to post-treatment.

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Table 5. Patient speciﬁc functional scale: pre and post-treatment information.

± 11.26°) was found (p = .01; Table 4). The mean change (mean = 8.20° ± 3.96°) suggests that the treatment was nearly effective enough to produce a clinically significant difference (MDC of 8.60°) and the Cohen’s d value of .81 suggests a large effect size from the treatment.35 Active Straight Leg Raise An increase in ASLR range of motion was found when comparing pre-treatment to post-treatment measurements (10.3 degrees). A statistically significant difference between the pre-ASLR (mean = 69.83° ± 16.27°) and the post-ASLR (mean = 80.17° ± 14.39°) was found (p = .037; 95% CI: .908, 19.759; Table 4). The mean change (mean = 10.33° ± 8.98°) suggests that the treatment was clinically significant, surpassing the MCID (5.9°) after one visit and the Cohen’s d value of .67 suggests a medium effect size from the treatment.35 Sacroiliac Joint Dysfunction A resolution of SJD occurred after one treatment for 100% of the patients (N = 6). Resolution of previously assessed SJD was observed in all six patients. DISCUSSION The purpose of this case series was to examine the immediate effects of a PRRT treatment on subject’s symptoms following a HS including pain, function, and presence of SJD. The results provide preliminary evidence that the use of the PRRT protocol can

produce immediate changes that are clinically and statistically significant following a first-degree HS (N=6). The single PRRT treatment produced substantial improvement in measures of pain (NRS) and function (PSFS and ROM). The results of this case series are unique as the treatment used which focuses on the proposed mechanism of downregulating the neuromuscular system is not commonly used. The results of this case series provide initial support that this type of treatment may be effective for reducing pain and dysfunction following a first degree HS. In two additional case series assessing the use of PRRT™, both Hansberger36 and Honeycutt37 reported immediate changes in pain and function using PRRT™, although their studies were focused on patients complaining of plantar fasciitis36 and breathing pattern dysfunctions.37 Pain was assessed using the NPRS and in each study a decrease in pain was reported (mean change score 5.0 points,36 and 3 points37). Hansen-Honeycutt et al.,37 reported that the decrease in pain may have been attributed to either restoring normal movement patterns or diminishing associated tender areas. When using PRRT™ to treat HS similar assumptions could apply; improvements to function (measured by the PSFS and range of motion) could be attributed to decreasing pain in the area or decreasing protective muscle spasm to improve motor control and recruitment of the hamstring muscle group.

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In this case series, high functional levels were reported after PRRT™ treatment. In the case study performed by Cilbulka et al.15 immediate changes in function were assessed using HS torque values. Positive changes in function was reported in both the current case series as well as the Cilbulka et al.15 study (mean PSFS change of 3 points and mean torque change of 8.1 foot pounds). Addressing neuromuscular dysfunction (i.e., downregulating muscles of the posterior chain) in patients diagnosed with a Grade 1 HS may allow for quick resolution of symptoms as compared to the time it takes in the standard tissue healing model. The standard tissue healing model includes three overlapping phases: inflammatory response, fibroplastic repair, and maturation-remodeling phase.37 Symptoms caused by damage to the soft tissue can take up to three years to resolve during the maturation-remodeling phase.37 However, it should be noted that this case series did not follow subjects for the timeframe associated with the standard tissue healing model. Perhaps a treatment focused on restoring motor control and muscle recruitment is a possible addition or alternative to traditional treatments for hamstring strains to induce meaningful outcomes. Up to 70% of MRI clinically diagnosed hamstring injuries include no evidence of fibrous tissue damage after examination. 38 Therefore, it may benefit clinicians to evaluate and treat grade one HS from a perspective where tissue damage is not the only cause of pathology. Theoretically, the symptoms reported in the grade one HS population may indicate dysfunction within the neuromuscular system. Primal Reflex Release Technique™ has been successful in resolving these symptoms immediately by targeting the downregulation of the posterior chain, which is in line with the idea that the dysfunction is occurring at the neurological level.38,40 By downregulating the muscles of the posterior chain, decreased hamstrings muscle tension may be attributed to the presence of a neurological dysfunction rather than a disruption of hamstring tissue. Faster symptom resolution in patients would be seen with treatments affecting the neurological system if the healing process is not needed to repair damaged tissue. To track patient recovery, both patient-rated and clinician-rated outcomes can be measured with a focus on down regulating the nervous system resulting to influence the musculature. Two out of the six subject’s

measurements of active straight leg raise were less than the reported normal range of motion pre-treatment,41 while six out of six subjects were within normal range (65 degrees or more) post-treatment. All five subjects (one subject was not tested due to time constraints) with pre-treatment PKET measurements, demonstrated measures less than the reported normal range of motion (70-80 degrees).42 Following the single treatment of PRRT™, three of five subjects met normal ranges of motion on the PKET (Table 4). Although the change in PKET after PRRT™ was statistically significant (mean change = 10 degrees), the comparison group in Cibulka’s study utilizing heat and stretching alone was reported to have a PKET change of 12 degrees. Range of motion measurements (ROM) alone appear to indicate comparable changes to isolated treatments of heat and stretching, but the control groups ROM mean prior to treatment was less than normal (42 degrees) and remained less than normal ranges after treatment (54 degrees) indicating that, while change occurred, resolution of the deficient ROM was not seen in the control group. In the current study, three of the five subjects treated with PRRT™ had measurements within normal range after treatment. Furthermore, when combined with the significant changes in pain and function ratings a treatment including PRRT™ appears to have a positive effect on the patient’s symptoms as well as possible increases in range of motion. Further research comparing signs and symptoms of HS to the treatment of heat and stretch alone would allow for clearer comparisons of how PRRT™ effects HS. Treatment utilizing PRRT™ may also have positive effects on SJD. Faulty movement patterns may predispose active individuals to HS and SJD. Cluster testing can be used to determine whether a patient has SJD.26 The PRRT™ treatment was designed to downregulate the neuromuscular system at the posterior chain which likely positively affected the SI joint. Further consideration and research is warranted on the treatment of SJD with PRRT™. LIMITATIONS Several limitations occurred due to the choice of following the design of the case report by Cibulka et al.,15 including application of a heat pack before

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treatment and clinician-applied static stretching after treatment, which add to the variables to consider when assessing the results. Either of these two interventions could also have affected the results of the study. This case series lacked a control group, which did not allow for comparison to another intervention or to no intervention. The researchers accepted these limitations with the intent to compare to the outcomes of function and range of motion to the previously collected data in the Cibulka study.15 While intra-rater reliability of range of motion was established prior to data collection, however, no inter-rater reliability was established. A lack of inter-rater reliability data may result in measurement error if the study is duplicated as it cannot be verified that the clinicians were producing the same measurements. Additionally, both the researchers and patients were not blinded in this case series, which may have led to biasing the outcomes. The researchers also utilized a convenience sample of patients which may limit the applicability of study results to other patient populations. Finally, an a priori sample size calculation was not conducted, as is typical in case series research. A small sample size can affect power, but the post hoc analysis suggests adequate power (.85-1.0) was achieved given the effect sizes ranged from moderate (.61, .67) to high levels, (1.9, .81) and within pair correlations were high for most variables.36,42,43 The assessment of clinical significance was explored by comparing to the MDC or MCID which is important when analyzing a limited sample size.43,44 CONCLUSIONS The results of this case series suggest that PRRT™ is useful in decreasing pain and increasing function in patients presenting with symptoms of HS in the short term. Primal Reflex Release Technique™ is used for downregulating dysfunction of the protective response of the ANS by manual reflex stimulation. In this case series the novel treatment used resulted in immediate changes in pain, function, and normalization of SJD. Further research on the effects of PRRT™ on muscle strains and the effects of PRRT™ on pain and function over longer periods of time are warranted.

REFERENCES 1. Mendiguchia J, Alentorn-Geli E, Brughelli M. Hamstring strain injuries: are we heading in the right direction? Br J Sports Med. 2012;46(2):81-85. 2. Davis DS, Ashby PE, McCale KL, Mcquain JA, Wine JM. The effectiveness of three stretching techniques on hamstring ﬂexibility using consistent stretching parameters. J Strength Cond Res. 2005;19(1):27-32. 3. DeWeiger VC, Gorniak GC, Shamus E. The effect of static stretch and warm-up exercise on hamstring length over the course of 24 hours. J Orthop Sports Phys Ther. 2003;33(12):727-732. 4. Kage V, Ratnam, R. Immediate effect of Active Release Technique versus Mulligan bent leg raise in subjects with hamstring tightness: a randomized clinical trial. Int J Physiother Res. 2014;2(1):301-304. 5. Kuilart K, Woollam M, Barling E, Lucas, N. The active knee extension test and Slump test in subjects with perceived hamstring tightness. Int J Osteopath Med. 2005;8:89-97. 6. Serner A, Tol JT, Jomaah H, et al. Diagnosis of acute groin injuries: a prospective study of 110 athletes. Am J Sports Med. 2015;43(8):1857-1864. 7. Beijsterveldt AMC, Port IGL, Vereijken A, Backx FJG. Risk factors for hamstring injuries in male soccer players: a systematic review of prospective studies. Scand J Med Sci Sports. 2013;23(3):253-262. 8. Sherry MA & Best TM. A comparison of 2 rehabilitation programs in the treatment of acute hamstring strains. J Orthop Sports Phys Ther. 2004;34(3),116-125. 9. Craig TT. Comments in Sports Medicine. Chicago, IL: American Medical Association; 1973. 10. Gerhardt MB, Romero AA, Silvers HJ, Harris DJ, Watanabe D, Mandelbaum, BR. The prevalence of radiographic hip abnormalities in elite soccer players. Am J Sports Med. 2012;40(3):584–588. 11. Hölmich P, Hölmich L, Bjerg A. Clinical examination of athletes with groin pain: an intraobserver and interobserver reliability study. Br J Sports Med. 2004;38(4): 46-451. 12. Nilstad A, Andersen TE, Bahr R, Holme I, Steffen K. Risk factors for lower extremity injuries in elite female soccer players. Am J Sports Med. 2014; 42, 940-948. 13. Thorborg K, Branci S, Nielsen MP, Tang L, Nielsen MB, Hölmich, P. Eccentric and isometric hip adduction strength in male soccer players with and without adductor-related groin pain: an assessorblinded comparison. Orthop J Sports Med. 2014;2(2):2325967114521778. 14. Gilmore J. Groin pain in the soccer athlete: fact, ﬁction, and treatment. Clin J Sports Med. 1998;17:787–793.

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15. Cibulka MT, Rose SJ, Delitto A, Sinacore DR. Hamstring muscle strain treated by mobilizing the sacroiliac joint. Phys Ther. 1986;66(8):1220-1223. 16. Vleeming A, Schuenke M, Masi A, Careiro J, Danneels L, Willard, F. The sacroiliac joint: an overview of its anatomy, function and potential clinical implications. J Anat. 2012;221(6):537-567. 17. Liebenson C. Hip dysfunction and back pain. J Bodyw Mov Ther. 2007;11(2):111-115. 18. Iams J. When reflexes rule: a new paradigm in understanding why some patients don’t get well. Adv Phys Ther Rehab Med. 2005;16(3):41. 19. Kasprowicz DE. Understanding the autonomic nervous system–a missing piece in the treatment of chronic pain. ND. Retrieved from http://www.boernepti.com/ media/file/340330/Understanding%20the%20ANS. pdf. Accessed December 7, 2015. 20. Bertoti DB. Functional Neurorehabilitation Through the Life Span. Philadelphia, PA: F.A. Davis; 2004. 21. Hall JE. Guyton and Hall Medical Physiology. Elsevier Health Sciences; 2015. 22. Arey LB, Burrows W, Greenhill JP, Hewitt RM. Dorland’s illustrated medical dictionary. Am J Med Sci. 1957;234(6):733. 23. Hartman LS. Handbook of osteopathic technique. Springer: 2013. 24. Iams J. Primal Reflex Release Technique Home Study Course. October 2015. 25. Nasypany A. SI & Pelvic Girdle #1 Initial Assessment. https://www.youtube.com/watch?v=H26DmIrAuiQ. Published Oct. 15, 2014. Retrieved Aug 15, 2016. 26. Cibulka MT, Delitto A, Koldehoff RM. Changes in innominate tilt after manipulation of the sacroiliac joint in patients with low back pain. Phys Ther. 1988; 68(9), 1359-1363. 27. Riddle DL, Freburger JK. Evaluation of the presence of sacroiliac joint region dysfunction using a combination of tests: a multicenter intertester reliability study. Phys Ther. 2002;82(8):772-781. 28. Laslett M, Aprill CN, McDonald B, Young SB. Diagnosis of sacroiliac joint pain: validity of individual provocation tests and composites of tests. Man Ther. 2005;10(3):207-218. 29. Wainner RS, Whitman JM, Cleland JA, Flynn TW. (2007). Regional interdependence: a musculoskeletal examination model whose time has come. J Orthop Sports Phys Ther. 2007;37(11): 658-660. 30. Nasypany, A., Primal Reflex Release Technique: Level 1 Seminar. Presented at University of Idaho; July 2-3, 2016; Moscow ID.

31. Farrar JT, Pritchett YL, Robinson M, Prakash A, Chappell A. The clinical importance of changes in the 0 to 10 numeric rating scale for worst, least, and average pain intensity: analyses of data from clinical trials of duloxetine in pain disorders. J Pain. 2010;11(2):109–118. 32. Williamson A, Hoggart B. Pain: a review of three commonly used pain rating scales. J Clin Nurs. 2005;14(7):798–804. 33. Sterling M, Brentnall D. Patient specific functional scale. Aust J Physiother. 2007;53(1): 65. 34. Stratford P, Gill C, Westaway M, Binkley J. Assessing disability and change on individual patients: a report of a patient specific measure. Physiother Can. 1995;47(4): 258-264. 35. Hurley WL, Denegar CR, Hertel J. Research Methods: A Framework for Evidence-Based Clinical Practice. Baltimore, MD: Lippincott, Williams, & Wilkins; 2011. 36. Hansberger BL, Baker RT, May J, Nasypany A. A novel approach to treating plantar fasciitis - effects of primal reflex release technique - a case series. Int J Sports Phys Ther. 2015;10(5):690-699. 37. Prentice, William E. Arnheim’s Principles of Athletic Training : a Competency-Based Approach. New York, NY :McGraw-Hill, 2003. 38. Ekstrand J, Healy JC, Walden M, Lee JC, English B, Hagglund M. Hamstring muscle injuries in professional football: the correlation of MRI findings with return to play. Br J Sports Med. 2012;46(2):112-117. 39. Hansen-Honeycutt J, Chapman EB, Nasypany A, Baker RT, & May J. A clinical guide to the assessment and treatment of breathing pattern disorders in the physically active: part 2, a case series. Int J Sports Phys Ther. 2016;11(6): 971–979. 40. Orchard JW. Lumbar spine region pathology and hamstring and calf injuries in athletes: is there a connection? Br J Sports Med. 2004;38(4):502-504.. 41. Carregaro, R., Silva, L., & GilCoury, HJ. Comparison between two clinical tests for the evaluation of posterior thigh muscles flexibility. Revista Brasileira de Fisioterapia, 11(2):139-145. 42. Davis DS, Quinn RO, Whiteman CT, Williams JD, Young CR. Concurrent validity of four clinical tests used to measure hamstring flexibility. J Strength Cond Res. 2008; 22(2):583-8. 43. de Winter JC. Using the Student’s t-test with extremely small sample sizes. Pract Assess Res Eval. 2013;18(10):1-12. 44. Lachin JM. Introduction to sample size determination and power analysis for clinical trials. Contr Clin Trials. 1981;2(2):93-113.

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IJSPT

CASE REPORT

THE MANAGEMENT OF PLANTAR FASCIITIS WITH A MUSCULOSKELETAL ULTRASOUND IMAGING GUIDED APPROACH FOR INSTRUMENT ASSISTED SOFT TISSUE MOBILIZATION IN A RUNNER: A CASE REPORT Rob Sillevis, PT, DPT, PhD, OCS, FAAOMPT1 Eric Shamus, PhD, DPT, CSCS1 Brittany Mouttet, DPT1

ABSTRACT Background and Purpose: Musculoskeletal ultrasound imaging (MSK US) is an emerging diagnostic tool in physical therapy, which allows for dynamic visualization of tissues in real time. Plantar fasciitis is a common condition causing heel and arch pain and has been related with degenerative changes in the plantar fascia resulting in tissue thickening. Instrument Assisted Soft Tissue Mobilization (IASTM) is an intervention that allows clinicians deep penetration to treat tissues. The mechanical forces caused by IASTM might cause localized tissue trauma leading to stimulation of the body’s natural inflammation and healing processes. The purpose of this case report is to demonstrate the use of ultrasound imaging to guide the decision-making process and to discern the optimal location for the application of IASTM. Case description: The subject was a 46-year-old female yoga practitioner and runner, who presented with right foot pain. The clinical impression was formulated based on the combination of traditional physical therapy examination procedures and MSK US imaging findings of the plantar fascia demonstrating thickness and tendinosis like changes within the plantar fascia 3 cm distally from the calcaneus. Outcomes: The subject was seen for eight treatment sessions over four weeks, at which time the goals of normal ankle dorsiflexion, no pain with palpation of the plantar fascia, negative windlass test, and no reported pain during gait were achieved. Discussion: This case report illustrates the use of MSK US imaging as a method to objectively assess tissue quality and guide decision-making when managing patients with plantar fascia related pain. MSK US was used to determine the optimal location for the application of IASTM during the conservative management of a runner with plantar fasciitis Level of evidence: Therapy, Level 5 Key words: Instrument Assisted Soft Tissue Mobilization, Movement system, Musculoskeletal Ultrasound imaging, Plantar fasciitis

Florida Gulf Coast University, Fort Myers, FL, USA

Conﬂict of interest statement: The authors do not report any conﬂict of interest.

CORRESPONDING AUTHOR Rob Sillevis 10501 FGCU Boulevard south Marieb 428 Fort Myers, Florida 33965 Tel: 239-7454312 E-mail: rsillevis@fgcu.edu

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 274 DOI: 10.26603/ijspt20200274

BACKGROUND AND PURPOSE Foot and ankle injuries occur commonly in sports related activities, such as running, resulting in pathologies including Achilles tendinopathy, plantar fasciitis, and cortical stress fractures1 Diagnostic imaging is often used to diagnose conditions, however the value of imaging as it relates to the treatment of musculoskeletal system conditions has been controversial due to the fact that anatomical changes not necessarily correlate with pain and dysfunction.2 Clinical decision-making is dependent on the accuracy and reliability of clinical tests and should not be based on imaging alone. 3,4 However, when correlated with patient history and physical findings the likelihood of proper imaging related decisions and interventions increases.2 Musculoskeletal ultrasound imaging (MSK US) is an emerging diagnostic tool in medicine and physical therapy, which allows for dynamic visualization of tissues in real time with devices that are often portable. Recent advances in ultrasound technology and the development of highresolution ultrasound transducers has resulted in improved visualization of soft tissues and bony structures.5,6 MSK US can be used to evaluate tissue properties such as the orientation and volume of fibers, as well as the presence of inflammatory processes, therefore can be a valuable diagnostic and prognostic tool for the physical therapist.5-7 Based on these advances the use of MSK US in the management of athletes has been growing.8 MSK US is a safe noninvasive imaging technique. It is safe for all patients, including those with cardiac pacemakers and metal implants, without any contraindications.9 MSK US imaging can easily be repeated and is therefore an effective tool to monitor tissue changes over time. Scheel et al10 demonstrated that inter-tester reliability, sensitivity, and specificity of MSK US imaging performed by rheumatologists in comparison with MRI ranged from moderate to good. Based on the current evidence MSK US appears to be a valid and reliable tool to evaluate the musculoskeletal system and should be considered as a possible diagnostic tool. 6,9,11 Additionally, MSK US imaging is within the scope of practice of the physical therapist and can easily be integrated into clinical practice now as US units are becoming more affordable. Plantar fasciitis is a common condition causing medial heel and arch pain.12-14 Plantar fasciitis is the

most common foot condition seen in clinical practice, which affects about two million Americans annually. There is a life span incidence of plantar fasciitis of about 10%.1 It has been reported that the prevalence of plantar fasciitis is between 11 to 15% of all foot symptoms, with a higher occurrence between the ages of 40 and 60.1,15 Risk factors for the development of plantar fasciitis including obesity, prolonged standing, poor ankle biomechanics, a decreased medial arch height, leg length inequity, heel spurs, and sports activities such as running. Plantar fasciitis accounts for about 10% of all running related injuries.1,15 With conservative management it has been reported that 80% of the cases will have symptom resolution within 12 months.16 It is believed that plantar fasciitis is the result of prolonged loading resulting in adaptive changes in the fascia.1 It has been related to degenerative changes in the plantar fascia resulting in tissue thickening, which could include proliferation of fibroblasts and a perpetuating inflammatory cycle.15 The localized healing responses results in the production of new connective tissue, which is laid down in a disorganized fashion and will cause the formation of adhesions and thickening of the plantar fascia. 15 Toomey16 previously demonstrated that a decrease in plantar fascia thickness was positively related with a reduction of pain in subjects with plantar fasciitis. The 2014 revised clinical guidelines for heel pain and plantar fasciitis recommend conservative management of plantar fasciitis to include joint and soft tissue manipulation, triceps surae and plantar fascia muscle elongation, the short-term use of taping, foot orthosis to support the medial arch, short term use of iontophoresis, low level laser, and education and counseling on the use of exercise to achieve a better body mass index.1 Additionally, It has been reported that the use of instrument assisted soft tissue mobilization (IASTM) is beneficial.17 IASTM is a modality that allows clinicians to achieve a localized and deep penetration of tissues, while reducing stress placed on the hands and fingers of clinicians.18 Although the exact effects of IASTM remain elusive, mechanical forces caused by the IASTM might result in localized tissue trauma leading to stimulation of the bodyâ&#x20AC;&#x2122;s natural inflammation and healing processes.19 The proposed benefits of IASTM are at

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the molecular and cellular level.19,20 Loghmani and Warden20 examined the response to IASTM on the knee ligaments of rats and found that changes in the tissues appear to be the result of stimulation of the fibroblasts located within the myofascial tissue layers.20 This gives the tissue the opportunity to restart the fibroblastic healing and remodeling process so that it has an opportunity to restore appropriately.20-22 It has also been proposed that IASTM may decrease pain through the stimulation of mechanoreceptors within the tissues resulting in the inhibition of nociceptor activity.20 This decrease in localized pain may contribute to increased range of motion, reduction of tissue tension, increase in tissue extensibility and producing normalization of neuromuscular movement patterns.20 Typically, IASTM is used in combination with other interventions.21 Looney et al17 reported that IASTM followed by two repetitions of 30 seconds static stretching and 20 minutes of icing resulted in clinically meaning changes in active range of motion. The exact dosing of IASTM is not clear, however, recommended treatment time ranges from a few minutes up to 20 minutes.23

and was advised to increase her functional activities gradually and initiate self-stretching. She was not able to manage her condition independently and she remained functionally limited. She was not able to return to her normal running activities or participate in her normal yoga activities, for that reason she was referred to physical therapy.

Therefore, the purpose of this case report is to demonstrate the use of ultrasound imaging to guide the decision-making process and to discern the optimal location for the application of IASTM.

At the time of physical therapy evaluation, she described both her heel and arch pain using the Numeric Pain Rating Scale (NPRS). The NPRS is a frequently used tool to quantify subjective pain and it has been previously recommended for the selfreport of pain.24Â 25 The validity and reliability of the NPRS has been previously reported for patients with acute and chronic pain.26 She reported her pain at the heel at 3/10 and in the medial arch at 6/10. The Lower Extremity Functional Scale (LEFS) was used as a patient reported outcome measure. The Lower Extremity Functional Scale (LEFS) can be used to evaluate the functional impairment of a patient with a disorder of one or both lower extremities. It can be used to monitor the patient over time and to evaluate the effectiveness of an intervention.27 The LEFS is a 20-item self-reported measure with each item a possible score 0-4, resulting in a total maximum score of 80. Higher scores on the LEFS indicate greater disability levels. At the time of examination her score was 39/80, which indicates a moderate level of disability. The validity, reliability, and responsiveness of the LEFS has been previously shown in patients with plantar fasciitis.1,28 The

CASE DESCRIPTION: SUBJECT HISTORY AND SYSTEMS REVIEW The subject of this case report was an otherwise healthy 46-year-old mesomorphic female yoga practitioner and recreational runner, who was referred to physical therapy by a local podiatrist. She had developed pain in the arch of the right foot six months ago after a three-mile run. After three weeks of unsuccessful self-management, which included icing and stretching, she sought medical care. She underwent a comprehensive evaluation and a plain film radiograph displayed a heel spur at the plantar aspect of the calcaneus, but no evidence of OA or cortical fracture. She was diagnosed with plantar fasciitis. Her podiatrist recommended cortisone injections and placed the foot in a rigid brace to immobilize the tissue. In total, she received two cortisone injections and was immobilized for six weeks. Following this she was transitioned to a soft brace, night splint,

She reported that her pain was localized on the plantar medial aspect of the heel and medial arch. This pain was provoked with standing and walking. Especially, the first couple of steps were painful after not being on the feet for a while. She reported that taking her weight off the foot decreased her pain and after several minutes the pain typically was completely gone. At the time of the evaluation she reported heel pain, but her medial arch pain was worse. Her pain was typically contained to the foot region although occasionally she did experience pain along the medial shin region. She reported that after being on her feet for a while she developed pain in the lateral right hip region. The screen for yellow and red flags was negative and she denied the presence of numbness in lower extremity.

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minimal clinically significant difference of the LEFS is a 9-point change.27

dysfunctions, which include ankle/ foot pain, knee pain, hip pain, and lower back pain.35-37

Clinical Impression #1 The subject experienced a sudden onset of heel pain after a three-mile run. Her pain was typically worse with weightbearing and did result in pain of the hip region. Differential diagnosis consisted of calcaneal contusion, calcaneal stress fracture, inflammatory arthropathy of the mid tarsal or subtalar joints, and plantar fasciitis or plantar fascia rupture. Due to the fact that her plain radiographs were negative, and had been immobilized for six weeks, the likelihood of underlying cortical fractures seemed low. The fact that weightbearing/ loading activities continued to provoke her symptoms in the heel and medial arch led the authors to the discern that the plantar fascia was the underlying cause of the subject’s symptoms. She reported an unremarkable medical history with a negative general health screen for the presence of red or yellow flags; therefore, further examination of this subject was appropriate. Examination included ruling out cortical bone as the cause of symptoms with the use of MSK US and joint mobility assessment followed by soft tissue assessment to further identify related tissues contributing to the subject’s presentation.

Joint motion assessment Active range of motion of the hip, knee, ankle and foot (AROM) was assessed in supine using a goniometer. It has been previously suggested that AROM assessment using a goniometer is valuable when examining patients with ankle/ foot dysfunction in non-weghtbearing.38,39 She displayed decreased dorsiflexion of the right ankle both with the knee in extension and flexion. This could indicate either a capsular restriction or a soleus tightness contributing to her motion deficit. Arthrokinematic assessment of the talocural joint displayed a decreased posterior/ inferior glide of talus. There was an increased medial glide of the calcaneus in the subtalar joint, which correlates to the pronation of the calcaneus seen in standing. She also displayed an increased plantar glide of the navicular in the transverse tarsal joint line which supports the observation of a decreased medial arch in standing. The fact that she displayed hypermobility of the subtar and midtarsal joint ruled out inflammatory arthropathy as the underlying cause of her symptoms.

EXAMINATION Initial observation Upon arrival to the examination (Table 1), the subject ambulated with a shortened stance phase and a positive Trendelenburg on the right. This gait pattern could be indicative of gluteus medius weakness and might indicate the presence of a regional interdependent multifactorial issue in this case.29-32 However, it was considered that six weeks of boot usage could have resulted in talocural joint limitations and an altered neuromuscular firing patterns.33,34 She reported pain in the right foot during the first couple of steps. She appeared comfortable when seated during her intake interview. Visual inspection in standing revealed a forward head posture, an increased thoracic kyphosis, increased lumbar lordosis, minimal knee valgus on the right, pronation of the calcaneus R>L, pes planus valgus R>L, and minimal hallux valgus on the right. Poor postural positioning can be attributed to a variety of musculoskeletal

Neurological assessment She did not display any signs of neurogenic sensitivity in the lower extremity. There was a negative straight leg raise, and a negative Tinel test for the tarsal tunnel. She displayed normal lower extremity muscle stretch reflexes and normal myotomal strength in the lower quadrant. Palpation for position in standing revealed positive navicular drop compared to the left side and this likely contributed to her pes planus valgus and altered gait pattern.40 Palpation and tissue speciﬁc assessment Structural palpation revealed a painful plantar aspect of the calcaneus. There was hypertonicity of the plantar fascia R>L and there was pain upon palpation of the planar fascia in the region of the navicular. To further examine the structures of the foot and the quality and integrity of the plantar fascia MSK US imaging (GE Healthcare, Chicago Il, Venue 40) was used. The scanning protocol was based on the fact that the reliability of using MSK to evaluate plantar fascia thickness was previously reported as high

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Table 1. Summary of relevant examination and re-examination ďŹ ndings.

with good intertester agreement when using the longitudinal scanning method.41 Figure 1 displays the position of the probe when assessing the plantar fascia using the longitudinal scanning method. Figure 2 displays the MSK US image of a normal foot. When evaluating an MSK image the clinician will use the variance in tissue density displayed in a variance of the gray scale to identify normal and abnormal tissues. Denser tissues will present as hyper-echoic (white) signals and tissues with lower density, such as fluid, as hypo-echoic (black).42 The calcaneus is identified as the highly reflective hyper-echoic curved line with dark shadowing underneath as no

sound waves pass the cortical bone. The planar fascia presents with a hyper-echoic fibrillar pattern in which the thickness is the generally same throughout the structure. Figure 3 displays the image of the right plantar fascia of the subject. Imaging demonstrated intact cortical calcaneal bone without the presence of any signs of fluid around the cortical structures, thereby ruling out cortical bone as the cause of symptoms. MSK imaging did identify that there was thickening of the plantar fascia 3 cm distal from the calcaneal origination. Additionally, this region demonstrated a tendinosis type presentation with several areas of disruption (hypo-echoic areas

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within the hyper-echoic fibrillar pattern) appearance on imaging of collagenous fibers within the fascia.7 This would confirm the hypothesis that there is a chronic irritation of the planta fascia present in this case. Muscle strength/ length assessment Manual muscle testing revealed marked weakness of the tibialis posterior at 3+/5, weakness of the triceps surae at 4/5, and weakness of the toe flexors at 4/5. Muscle length testing demonstrated muscle

Figure 1. Position of the MSK US probe when assessing the plantar fascia.

shortening of the triceps surae complex on the right and she displayed a positive windlass test on the right.43 De Garceau et al44 report that the windlass test has a 100 % specificity and the inter-rated reliability had an ICC of .96, therefore this would confirm the presence of plantar fasciitis in this case. Based on the regional interdependence model the knee and hip joints were examined for active and passive range of motion. No significant differences were present between the right and left side. She did display a positive valgus stress test of the knee in 0 and 30 degrees of flexion (graded 1+), which seemed to correlate to the valgus knee during stance phase. Manual muscle testing revealed weakness of the right hip abductor group at 4/5 without provocation of any pain. Muscle length testing revealed some hamstring muscle tightness using the 90/90 test with tightness reported at 35 degrees of knee flexion on the right and 15 degrees on the left. Clinical Impression #2 The clinical impression in this case was based on the combination of traditional physical therapy examination procedures and the dynamic MSK US

Figure 2. Normal MSK US images of a plantar fascia (not actual patient). (a) Yellow arch on the image left is the hyperechoic cortical bone. (b) In the right image the yellow lines outline a normal plantar fascia with equal thickness at three measurement points. The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 279

Figure 3. MSK US images of the plantar fascia upon initial examination.White arrow indicates area of fascia thickening and hypoechoic changes.

imaging findings of the plantar fascia. Considering the fact that she had pain upon palpation of the plantar fascia, decreased ankle dorsiflexion with decreased posterior glide of the talus, a negative tarsal tunnel testing, a positive windlass test the findings were consistent with plantar fasciitis.1 This was further supported by the positive MSK US imaging findings of tissue thickness and tendinosis like changes within the plantar fascia. This led to the hypothesis that this subject could benefit from localized IASTM, joint manipulation, and muscle stretching and strengthening. Successful outcomes were considered as improved NPRS and LEFS scores, normalized AROM of the ankle, normalization of the plantar fascia on MSK imaging, and return to running without symptoms. Interventions and outcomes Following the examination, the initial treatment focused on normalizing ankle dorsiflexion, improving talocural joint mobility, and decreasing the tightness and hypersensitivity of the plantar fascia. Therefore, treatment included manipulation techniques targeting the talocural joint (Table 2). Both

the distraction manipulation and manipulation to improve dorsal glide of the talus were utilized. Ankle dorsiflexion improved from 5 to 11 degrees. Muscle stretching of the triceps surae was performed using a contract-hold-relax-stretch technique with a stretch hold time of 30 seconds and this was repeated 3 times.45 The stretch intensity was moderate which is considered beneficial and safe.46 To address the tone of the planar fascia an IASTM approach was utilized using the EDGEility tool (https://www.edgemobilitysystem.com/, Buffalo, NY). The MSK US imaging identified the exact location of the plantar fascia irritation and at this location a five-minute application of short stroking of the fascia was utilized. Initially the subject reported significant sensitivity using the tool however within 60 seconds this became pain free. After the initial manual therapy interventions, her pain upon standing in the arch had decreased from 6/10 to 3/10. This supported the thought that manual therapy techniques would be beneficial in this case. Based on her foot position in standing and the clinical practice guidelines she was recommended to obtain prefabricated arch supports that would position her calcaneus in less pronation.1 To maximize the carryover of manual therapy interventions the subject was instructed in an augmented exercise program, which included stretching of both the triceps surae and plantar fascia in standing. She was instructed to perform her stretching exercises ins such a way that a static stretch was maintained for 30 seconds and repeated three times. Stretching has been shown to be beneficial within the management of plantar fasciitis.1 Each treatment session started with assessment of the ankle mobility for dorsiflexion, palpation of the plantar fascia both for pain and tension, and the windlass test was utilized to determine fascia length. These three findings served as test-retest signs to determine the benefit of manual therapy interventions. She received the IASTM during all eight treatment sessions. After the fifth session, no pain was present while preforming the IASTM technique. The ankle manipulation techniques used during the course of treatment were performed as described by Hartman and were based on the presence of hypomobility in talocural joint.47 Based on the fact that the talocural joint was restricted in dorsal/ inferior

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Table 2. Interventions and augmented exercise.

glide the both general non-specific traction manipulation and the dorsal glide manipulation were used. Additional mobilization with movement was used to add and active component to the dorsal glide manipulation. At the third visit, the ankle dorsiflexion was 15 degrees with the knee flexed and no additional manipulative treatments were utilized in subsequent treatments. The tibialis posterior muscle plays a role in the overall stability of the ankle and supports the medial arch.48 Therefore, at the second visit, she was introduced to the strengthening exercises with a focus on standing tibialis posterior and triceps surae strengthening exercises. The focus was placed on eccentric strengthening. 49 At visit three, she initiated additional hip strengthening exercises and gait training to normalize her neuromuscular recruitment pattern. The eight session was four weeks after the initial treatment and, at that time, the she displayed normal ankle dorsiflexion, no pain with palpation of the plantar fascia, negative windlass test, and she

reported no pain during gait. MSK US displayed a normal presentation of the plantar fascia of the right foot (Figure 3). She was able to participate in normal yoga activities. She had initiated some running on a treadmill with the prefabricated arch supports in her shoes without symptoms arising. Due to the fact that treatment goals were achieved she was discharged with the instructions to continue to perform muscle stretching, strengthening exercises for the tibialis posterior and hip abductors, and to continue using her arch supports in her shoes. At the onemonth follow-up, she continued to be pain free and reported no functional limitations. DISCUSSION This case report describes how MSK US was used within the management of a 46-year-old otherwise healthy female subject presenting with heel and arch pain limiting her running ability. Based on a cluster of evaluation findings, including AROM, arthrokinematic motion assessment, muscle length

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and strength assessment, and MSK US imaging findings it appeared that this subject presented with plantar fasciitis. MSK US is a safe noninvasive imaging technique within the scope of physical therapy practice that provides the clinician with an easy, relatively low cost, portable, and dynamic real-time view of human tissues.9,50 It can easily be repeated and is therefore an appropriate tool to monitor tissue changes over time.7 The utilization of MSK US by physical therapists has been steadily growing. It not only aids in the diagnostic process it can also guide (real time) treatment interventions.6,50 Initially, MSK US was used by physical therapists to evaluate muscle contractions and as a biofeedback tool during interventions to improve isolated muscle action.51,52 Since than it has become useful for diagnosing many conditions such as cortical bone fractures, tendon and muscle morphology, ligament integrity and length, the presence of inflammation including synovitis, bursitis, and nerve related conditions such as carpal tunnel syndrome and Morton neuroma.5,8,50,53,54 MSK US has been demonstrated to be a reliable and valid method to assess the musculoskeletal system.5,54 Naredo et al55 demonstrated moderate to good inter-tester reliability when evaluating soft tissue and bony structures with MSK-US. Poltawski et al56 demonstrated test-retest reliability ranges from .70-.82 when measuring muscle thickness making this a relatively good method to evaluate the thickness of the plantar fascia. One of the disadvantages of MSK US is the fact that the quality of the image is greatly dependent of the experience of the sonographer.5 The clinician who performed the MSK US in this case report has more than six years of experience using MSK US in clinical practice. It appears that this is a modality even the novice practitioner can use after minimal training.56,57 Filippucci et al58 demonstrated that quality images can be obtained by a novice after a short two hour training by an experienced sonographer followed by 24 non-consecutive hours of active scanning. This concurs with the findings of Dâ&#x20AC;&#x2122;Agostino et al,59 who suggest that it takes at least 70 examinations to develop competence evaluating the MCP, PIP, and MTP joints. Based on current evidence it can be concluded that even the novice practitioner who undergoes training in MSK US can achieve the acceptable diagnostic accuracy compared to highly experienced

Figure 4. MSK US images of the plantar fascia upon discharge. White arrow indicates normal plantar fascia tissue.

sonographers. Based on the anatomical and biomechanical knowledge of the ankle/foot physical trained therapists should be able to produce reliable and repeatable MSK US images. The exact mechanism underlying the development of plantar fasciitis is not clear. There are several contributing factors that have been identified that could contribute to this syndrome.1 Such risk factors include age between 40 and 60 years, sudden increase in running distance, change in running surface, prolonged standing, foot pes planus, limitations in ankle dorsiflexion and sudden weight gain or obesity. 1,15 Age is considered a risk factor, as degenerative changes begin within the plantar fascia. MSK US imaging (Figures 2 and 3) demonstrated that the plantar fascia in this case had a tendinosis type presentation with areas of swelling and disruption of fibers about 3 cm distally of the calcaneal insertion. A characteristic presentation related to degenerative changes in the fascia is the presence of localized hyperemia. 60 This suggests that there could be a neurovascular in-growth which may contribute to foot pain when loading the tissues. McMillan et al60

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was able to demonstrate abnormal soft tissue vascularity in the plantar fascia with ultrasound imaging. This change in fiber consistency could have led to degradation and weakening of the connective tissue collagen and elastin fibers in the plantar fascia in this case, resulting in impaired shock absorption during running activities. A second consideration related to the findings of the tissue changes found with the MSK image in this case could be her anatomical presentation. The subject presented with pes planus valgus in both feet with the right greater than the left. In the case of pes planus, one could assume that the medial longitudinal arch is depressed, the subtalar joint is pronated, and the calcaneus assumes a valgus position during weight bearing and more dysfunctional during running activities. This repetitive stress on the plantar fascia to invert the calcaneus during the gait cycle predisposes the tissue to microtearing within the fascia, collagen necrosis, angiofibroblastic hyperplasia and pain.1 McNally and Shetty61 report that a thickening of the plantar fascia greater than 5 mm on MSK US is suggestive of plantar fasciopathy. The MSK US images in this case (Figure 3) clearly identified thickening and degenerative changes supporting the decision that there were structural changes in the fascia.62 This would also explain the fact that

her pain likely was not caused by an acute inflammatory processes. Therefore, IASTM would be an appropriate intervention to address these tissue changes within the plantar fascia clinically. One of the rationales explaining the therapeutical benefit of IASTM is based on the tissue friction effect by the tool believed to increase local blood flow. Additionally, the use of the tool could cause localized tissue trauma resulting in an inflammatory cascade within the tissue.20-22 Figure 5 A depicts an MSK US image prior to the five-minute IASTM intervention and an image of the same tissue directly after the intervention. The Doppler setting was used while creating these images. Doppler MSK US is commonly used to estimate the blood flow through blood vessels with higher flow indicated by more red discoloration within the image. No identifiable circulatory changes can be detected on the post intervention image (Figure 5B) implying that there was none. This observation does not support any circulatory benefits of IASTM to the plantar fascia in this case. Because no cause and effect relationships can be inferred from this case report, future studies should use MSK US to further evaluate the effect of IASTYM on the circulation in the different layers of human tissues in larger sample sizes.

Figure 5. MSK US Doppler images of the plantar fascia before and after IASTM. (a) Prior to intervention. (b) Post 5-minute intervention application. The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 283

CONCLUSIONS MSK US imaging allows the clinician real time visualization of different tissue layers in the human body which can assist the clinician in establishing a differential diagnosis and selecting appropriate treatment interventions. The results of this case report offer preliminary evidence that supports the use of MSK imaging within the evaluation process in the case of a runner with plantar fasciitis. The treatment combination of manual therapy, the use of IASTM directed by MSK US imaging, and stretching, strengthening, gait training, and proper footwear was beneficial. This subject was pain free and returned to full activity and running after eight visits over four weeks. Additional research is necessary to further validate MSK US imaging as a method to objectively assess tissue quality and guide decision-making when managing patients with musculoskeletal injuries. REFERENCES 1. Martin RL, Davenport TE, Reischl SF, et al. Heel pain-plantar fasciitis: revision 2014. J Orthop Sports Phys Ther. 2014;44(11):A1-33. 2. Doss A. Wording wisely: Including prevalence data and evidence based clinical outcomes of spinal and musculoskeletal degeneration in radiology reports. J Med Imaging Radiat Oncol. 2018;62(5):599-604. 3. Edwards I, Jones M, Carr J, Braunack-Mayer A, Jensen GM. Clinical reasoning strategies in physical therapy. Phys Ther. 2004;84(4):312-330; discussion 331-315. 4. Sizer PS, Jr., Mauri MV, Learman K, et al. Should evidence or sound clinical reasoning dictate patient care? J Man Manip Ther. 2016;24(3):117-119. 5. Rasmussen OS. Sonography of tendons. Scand J Med Sci Sports. 2000;10(6):360-364. 6. Smith J, Finnoff JT. Diagnostic and interventional musculoskeletal ultrasound: part 1. Fundamentals. PM R. 2009;1(1):64-75. 7. Zellers JA, Cortes DH, Pohlig RT, Silbernagel KG. Tendon morphology and mechanical properties assessed by ultrasound show change early in recovery and potential prognostic ability for 6-month outcomes. Knee Surg Sports Traumatol Arthrosc. 2018. 8. Yim ES, Corrado G. Ultrasound in sports medicine: relevance of emerging techniques to clinical care of athletes. Sports Med. 2012;42(8):665-680. 9. Blankstein A. Ultrasound in the diagnosis of clinical orthopedics: The orthopedic stethoscope. World J Orthop. 2011;2(2):13-24.

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39. Ness BM, Sudhagoni RG, Tao H, et al. The reliability of a novel heel-rise test versus goniometry to assess plantarﬂexion range of motion. Int J Sports Phys Ther. 2018;13(1):19-27. 40. Blasimann A, Eichelberger P, Lutz N, Radlinger L, Baur H. Intra- and interday reliability of the dynamic navicular rise, a new measure for dynamic foot function: A descriptive, cross-sectional laboratory study. Foot. 2018;37:48-53. 41. Cheng JW, Tsai WC, Yu TY, Huang KY. Reproducibility of sonographic measurement of thickness and echogenicity of the plantar fascia. J Clin Ultrasound. 2012;40(1):14-19. 42. Guermazi A, Roemer FW, Robinson P, Tol JL, Regatte RR, Crema MD. Imaging of muscle injuries in sports medicine: Sports imaging series. Radiology. 2017;282(3):646-663.

31. McPoil TG, Vicenzino B, Cornwall MW. Effect of foot orthoses contour on pain perception in individuals with patellofemoral pain. J Am Podiatr Med Assoc. 2011;101(1):7-16.

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33. McHenry BD, Exten EL, Cross JA, et al. Sagittal subtalar and talocrural joint assessment during ambulation with controlled ankle movement (CAM) boots. Foot Ankle Int. 2017;38(11):1260-1266. 34. Rabin A, Portnoy S, Kozol Z. The association of ankle dorsiﬂexion range of motion with hip and knee kinematics during the lateral step-down test. J Orthop Sports Phys Ther. 2016;46(11):1002-1009.

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48. Simpson MR, Howard TM. Tendinopathies of the foot and ankle. Am Fam Physician. 2009;80(10):11071114. 49. Nishikawa KC, Lindstedt SL, LaStayo PC. Basic science and clinical use of eccentric contractions: History and uncertainties. J Sport Health Sci. 2018;7(3):265-274. 50. Karel Y, Miranda A, Thoomes-de Graaf M, et al. Does the outcome of diagnostic ultrasound inﬂuence the treatment modalities and recovery in patients with shoulder pain in physiotherapy practice? Results from a prospective cohort study. Musculoskelet Sci Pract. 2019;41:28-35. 51. Amiri Arimi S, Ghamkhar L, Kahlaee AH. The Relevance of Proprioception to Chronic Neck Pain: A Correlational Analysis of Flexor Muscle Size and Endurance, Clinical Neck Pain Characteristics, and Proprioception. Pain Med. 2018;19(10):2077-2088. 52. Teyhen DS, Miltenberger CE, Deiters HM, et al. The use of ultrasound imaging of the abdominal drawing-in maneuver in subjects with low back pain. J Orthop Sports Phys Ther. 2005;35(6):346-355. 53. Situ-LaCasse E, Grieger RW, Crabbe S, Waterbrook AL, Friedman L, Adhikari S. Utility of point-of-care musculoskeletal ultrasound in the evaluation of emergency department musculoskeletal pathology. World J Emerg Med. 2018;9(4):262-266. 54. Smith J, Finnoff JT. Diagnostic and interventional musculoskeletal ultrasound: part 2. Clinical applications. PM R. 2009;1(2):162-177. 55. Naredo E, Moller I, Moragues C, et al. Interobserver reliability in musculoskeletal ultrasonography: results from a “Teach the Teachers” rheumatologist course. Ann Rheum Dis. 2006;65(1):14-19.

56. Poltawski L, Ali S, Jayaram V, Watson T. Reliability of sonographic assessment of tendinopathy in tennis elbow. Skeletal Radiol. 2012;41(1):83-89. 57. Kissin EY, Nishio J, Yang M, et al. Self-directed learning of basic musculoskeletal ultrasound among rheumatologists in the United States. Arthritis Care Res (Hoboken). 2010;62(2):155-160. 58. Filippucci E, Unlu Z, Farina A, Grassi W. Sonographic training in rheumatology: a self teaching approach. Ann Rheum Dis. 2003;62(6): 565-567. 59. D’Agostino MA, Maillefert JF, Said-Nahal R, Breban M, Ravaud P, Dougados M. Detection of small joint synovitis by ultrasonography: the learning curve of rheumatologists. Ann Rheum Dis. 2004;63(10): 1284-1287. 60. McMillan AM, Landorf KB, Gregg JM, De Luca J, Cotchett MP, Menz HB. Hyperemia in plantar fasciitis determined by power Doppler ultrasound. J Orthop Sports Phys Ther. 2013;43(12):875-880. 61. McNally EG, Shetty S. Plantar fascia: imaging diagnosis and guided treatment. Semin Musculoskelet Radiol. 2010;14(3):334-343. 62. Gibbon WW, Long G. Ultrasound of the plantar aponeurosis (fascia). Skeletal Radiol. 1999;28(1):21-26. 63. Arias-Buria JL, Martin-Saborido C, Cleland J, Koppenhaver SL, Plaza-Manzano G, Fernandez-deLas-Penas C. Cost-effectiveness Evaluation of the Inclusion of Dry Needling into an Exercise Program for Subacromial Pain Syndrome: Evidence from a Randomized Clinical Trial. Pain Med. 2018.

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IJSPT

CLINICAL COMMENTARY

REHABILITATION CONSIDERATIONS FOR SPONDYLOLYSIS IN THE YOUTH ATHLETE Mitchell Selhorst, DPT, OCS1 Michael Allen, PT, OCS2 Robyn McHugh, DPT, OCS2 James MacDonald, MD, MPH3

ABSTRACT Low back pain in adolescent athletes is quite common, and an isthmic spondylolysis is the most common identifiable cause. Spondylolysis, a bone stress injury of the pars interarticularis, typically presents as focal low back pain which worsens with activity, particularly with back extension movements. Research on spondylolysis has focused on diagnosis, radiographic healing, the effects of bracing, and rest from activity. Although physical therapy is frequently recommended for adolescent athletes with spondylolysis, there have been no randomized controlled trials investigating rehabilitation. Additionally, there are no detailed descriptions of physical therapy care for adolescent athletes with spondylolysis. The purpose of this clinical commentary is to provide a brief background regarding the pathology of isthmic spondylolysis and provide a detailed description of a proposed plan for physical therapy management of spondylolysis in adolescent athletes. Level of Evidence: 5 Keywords: Adolescent, Low Back Pain, Stress Fracture, Movement System

Sports and Orthopedic Physical Therapy, Nationwide Children’s Hospital, Columbus, Ohio, United States. 2 Division of Occupational Therapy and Physical Therapy, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States. 3 Division of Sports Medicine, Nationwide Children’s Hospital, Columbus, Ohio, United States. Source of Funding: The authors have no funding to declare. Ethics Approval: Not applicable

CORRESPONDING AUTHOR Mitchell Selhorst, DPT, OCS 6499 East Broad St. Suite 140 Columbus, Ohio, 43214 E-mail: Mitchell.Selhorst@ Nationwidechildrens.org Telephone: 614-306-8852 Fax: 614-355-9765

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 287 DOI: 10.26603/ijspt20200287

INTRODUCTION Half of all adolescents report experiencing low back pain (LBP) and those who are active in sports report an even higher rate.1,2 The growing spine of the adolescent introduces variables into the assessment and management of lumbar injuries which do not exist in the developed spine of the adult.3 The most common identifiable cause of LBP in the adolescent athlete is an isthmic spondylolysis, a stress injury in the pars interarticularis.4-6 Research on spondylolysis has focused on diagnosis, radiographic healing, the effects of bracing, and rest from activity. Although spondylolysis is a common injury among adolescent athletes, no detailed description of physical therapy care for this population exists. The purpose of this clinical commentary is to provide a brief background regarding the pathology of isthmic spondylolysis and provide a detailed description of a proposed plan for physical therapy management of spondylolysis in adolescent athletes. PREVALENCE The prevalence of spondylolysis in adolescent athletes is reported to be 7-21%.7-9 The prevalence of spondylolysis in symptomatic adolescent athletes is reported to be two to five times higher than nonathletes, with a prevalence of 14-30% among adolescent athletes reporting LBP.6,10,11 Spondylolysis is 1.6-4.5 times more prevalent in adolescent males than females reporting LBP.6,11 Spondylolysis occurs in other populations but at a much lower rate; the prevalence reported in children is 2.5-4.5%, increasing to 6% in the general adolescent and adult populations.4,5,12,13 Spondylolysis may be present in asymptomatic individuals as well,12 and an incidental identification of a spondylolysis in an asymptomatic individual should not warrant treatment. ANATOMY AND MECHANISM OF INJURY Isthmic spondylolysis is the most common type of spondylolysis and is the focus of this clinical commentary.14,15 Isthmic spondylolysis refers to an overuse stress injury in the pars interarticularis (Figure 1 and Figure 2). A spondylolysis may be unilateral or bilateral and most commonly occurs at the L5 vertebra with L4 being the next most commonly affected level.14 An association has been noted with spondylolysis and spina bifida occulta.4,16-18 Additionally,

Figure 1. Depiction of an Isthmic Spondylolysis.

Figure 2. Radiographic image of bilateral spondylolysis at L4 vertebra.

some evidence shows that individuals with a spondylolysis have a pars with a smaller cross-sectional area than other adolescents.19 Among adolescent spondylolytic injuries, there are different subgroups: acute or active, progressive, and terminal. These

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subgroups are determined by the appearance of the lesion on imaging, rather than the chronicity of the injury.20,21 The mechanism of injury for spondylolysis is thought to be excessive and repetitive extension movements, particularly when combined with rotation.11 Risk of spondylolytic injury exists for all athletes, but athletes who perform repetitive extension and rotation motions, have an even higher risk.3,5,6,8,20,22,23 Sports such as baseball, throwing events in track and field, cricket, diving, gymnastics, soccer, wrestling, and weightlifting have a higher risk of spondylolysis.6,8,11,24 CLINICAL PRESENTATION The adolescent athlete will typically present with complaints of atraumatic, insidious-onset, focal LBP which worsens with activity, especially lumbar extension movements. Adolescent athletes with symptomatic spondylolysis typically present with axial LBP without radiation into the legs.22 Adolescents with a spondylolysis demonstrated increased lumbar lordosis and tightness of the hamstring muscles when compared to adolescents without a spondylolysis.19,25 Currently, patient history and clinical special tests have little diagnostic value.26,27 The most well-known clinical test to screen for spondylolysis is the single-leg hyperextension test, however this test has been found to be neither sensitive nor specific for detecting spondylolysis.28,29 Therefore, imaging is necessary when a clinician wishes to confidently determine if a spondylolytic lesion is present in an adolescent athlete with LBP.26 IMAGING The most appropriate imaging to diagnose a spondylolysis has not been clearly established. Two-view radiographs include anterior-posterior (AP) and lateral views while four-view radiographs additionally include oblique views of the spine. Four-view radiographs have fallen out of favor due to exposing the patient to higher levels of radiation with little, if any, increased sensitivity.30 Radiographs have low sensitivity making it difficult to rule out a spondylolysis without advanced imaging.31 Computed tomography (CT) or single photon emission computed tomography (SPECT) have historically been considered the gold standard for diagnosing spondylolysis. SPECT/ CT is quite sensitive for detecting lesions, but exposes

the patient to significant amounts of radiation.32,33 Magnetic resonance imaging (MRI) has become more popular in the diagnosis of spondylolysis.34,35 The diagnostic accuracy of MRI for detecting spondylolysis has improved in recent years approaching that of SPECT/CT,31 and has the advantage of no ionizing radiation.33 There remain, however, challenges to MRI’s use, with issues of cost, insurance coverage, access, and variable quality of imaging in different centers. Tofte et al.36 recommends using two-view radiographs as the best initial study, subsequently followed by MRI in early diagnosis or CT with more persistent LBP. OUTCOME MEASURES Traditional adult patient reported outcome measures for LBP, such as the Oswestry Disability Index and the Roland-Morris Disability Questionnaire, have significant limitations for adolescent athletes with spondylolysis. The Oswestry Disability Index becomes notably less reliable for high functioning individuals, such as adolescent athletes, because of a significant floor effect.37 The Roland-Morris Disability Questionnaire is similarly not designed for higher functioning populations.38,39 Adolescents with a spondylolysis typically struggle with higher level activities such as running, jumping and sport specific motions, but are relatively quickly able to perform ADL’s without much difficulty. The Micheli Functional Scale (MFS) is a relatively new patientreported outcome measure specifically designed for adolescent athletes with LBP.40 The MFS demonstrates high internal consistency (α = 0.90), and the concurrent validity has been established using the Oswestry Disability Index.40,41 The minimal clinically important difference has yet to be established for the MFS. Although more research is needed on the psychometric properties of the MFS, the authors believe this outcome measure is the most appropriate to use in this population. NON-SURGICAL AND SURGICAL CARE Non-surgical care should be the initial treatment for adolescent athletes with spondylolysis.14,42 The vast majority of patients with spondylolysis can successfully be managed with non-surgical care;14 and surgery, involving direct repair or indirect reduction and compression,43,44 may only be indicated after

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failure to improve with at least six months of comprehensive treatment.45 REST FROM ACTIVITY Cessation of sport activity is recommended for at least three months in this population.46 Resting from sport for three months has been closely associated with a favorable clinical outcome.47,48 Varying recommendations on the optimal time to begin physical therapy have been made with some recommending starting early, when symptoms have resolved,3,49,50 and others recommending no rehabilitation until after three months of rest.42,51 In a retrospective review,52 patients whose physical therapy was initiated earlier were able to return to sport sooner than the patients who physical therapy was not initiated until after three months. Recommendations for activity modification including sport and initiating physical therapy are based on low-level evidence.46,52 The authors believe that supervised therapeutic exercise can be completed safely and should be initiated early within the first few weeks after diagnosis to help reduce muscle atrophy, deconditioning, and potentially reduce time out of sport. BRACING Although lumbar bracing may be prescribed in an attempt to stabilize the spine and promote healing, controversy exists about the efficacy of bracing for spondylolysis. Several investigators have advocated for the routine use of lumbar bracing using several different types of lumbosacral orthoses to limit extension and rotation of the spine.53-59 However, in a meta-analysis of patients with spondylolysis, bracing was not found to influence clinical outcomes.14 Additionally, bracing prescription was not found to be predictive of the long-term ability to participate in sport, symptom recurrence, or the patientâ&#x20AC;&#x2122;s perceived outcome.60 A randomized controlled trial is necessary to determine the true effectiveness of bracing, but based on the current evidence, the authors recommend forgoing routine use of bracing and instead reserve its use for patients whose symptoms fail to improve. PROGNOSIS Excellent short-term clinical outcomes should be expected for adolescents with spondylolysis,14

however these positive short-term clinical outcomes are not maintained by all.60,61 A recent systematic review suggests that with non-surgical treatment, consisting of activity restriction, rest, and physical therapy with or without adjunctive bracing, 92% of individuals are able to return to sport with little to no pain within six months.62 The short-term clinical outcomes for athletes with a spondylolysis appear to be more promising than adolescents with nonspecific LBP, as only 33-35% of the adolescents with non-specific LBP were without pain and dysfunction following individualized physical therapy exercise and manual therapy.63,64 Long-term efficacy (1.5-8 years) of non-surgical treatment for spondylolysis suggests that LBP interfering with activity returns in 45%-51% of individuals, and 18-40% decreased or stopped their sport participation due to pain.60,61 Non-surgical treatment of spondylolytic injuries has attempted to promote bony healing of the lesion.56,59,65 In a meta-analysis of 10 radiographic studies,14 only 28% of spondylolytic lesions healed. Unilateral injuries were significantly more likely to heal (71%) compared to bilateral injuries (18%).14 Additionally, acute lesions had a 68% chance of healing, while terminal or chronic lesions did not heal with non-surgical treatment.14 Despite a goal to promote bony healing, radiographic healing is not associated with quality of life or ability to return to sport.14,49,66 Repeat imaging to assess for radiographic healing is no longer recommended in a patient who is responding well to treatment, due to unnecessary exposure to radiation as well as the associated cost.33 In the authors opinion, clinicians should base treatment progression on functional ability and not bony healing, since it is not associated with clinical outcomes. PSYCHOSOCIAL IMPACT OF SPONDYLOLYSIS INJURY Spondylolysis is typically viewed through the biomedical model due to the existence of a discrete identifiable injury to the vertebra. In contrast, the authors recommend clinicians address this condition using the biopsychosocial approach. Spondylolytic injuries not only affect athletes physically but also psychologically and socially with athletes experiencing feelings of loss, decreased self-esteem,

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anxiety, frustration, isolation, and depression.67-69 These psychosocial factors are important for clinicians to consider and address throughout rehabilitation, as these adolescent athletes are often unable to participate in their desired sport for months.67,69,70 Effective patient-clinician communication and positive relationships can provide social support and are also associated with improved health outcomes.68,71 Moreover, athletes may perceive their low back as “broken” resulting from the explanation they have received regarding the spondylolytic injury. This exaggerated perception can easily increase fear of activity and fear of re-injury. Clinicians should reassure adolescent athletes that, although they have a bone stress injury, their back is not “broken”. Furthermore, the positive outcomes seen in this patient population and the high likelihood of a making full return to sport should be emphasized.14,60 RATIONALE OF PHYSICAL THERAPY CARE Though physical therapy treatment for adolescent athletes with spondylolysis has not been specifically described in the literature, there is value in leveraging evidence from other relevant populations. The presence of a spondylolysis has been found to result in lumbar instability, with increased translation and rotation motion occurring segmentally.72-75 Establishing good performance of specific muscles, including the transversus abdominis and multifidus, has been theorized to promote segmental lumbar stability for this population.76,77 In a randomized controlled trial of adults with spondylolysis, targeting the deep abdominals and lumbar multifidus muscles was found to be superior to general exercise.76 The clinical practice guidelines on low back pain recommend motor control exercises, transversus abdominis training, lumbar multifidus training, and dynamic lumbar stabilization exercises for individuals with spinal instability including spondylolysis.78 Additional recommendations applicable to athletes with spondylolysis as they progress back to sport include trunk coordination and motor control training, functional strengthening, and endurance exercises.78 FRAMEWORK FOR TREATMENT The authors propose a framework for the physical therapy treatment of adolescent athletes with acute spondylolysis. In many ways physical therapy for

the adolescent athlete with spondylolysis is similar to those with non-specific LBP, but there are certain factors that are important for this population. First and foremost is that the athlete has a healing bone stress injury. Phase I of the program is performed in a relatively static and neutral lumbar position allowing for muscle activation and strengthening while avoiding undue stress on the injured pars interarticularis. During this phase, the authors recommend addressing the deep abdominals and lumbar multifidus, as targeting these muscles was found to be superior to general exercise among adults with spondylolysis or spondylolisthesis.76 Second, as the patient’s symptoms improve, extension and rotation motions should be promoted, not avoided. Recommendations have been made to avoid exercises that cause extension or rotation motions in adolescent athletes with spondylolysis.79 Although repetitive forceful extension and rotation is thought to be the mechanism of injury and endrange extension stresses the pars interarticularis,80 these motions are functional and necessary in most sports.81,82 It is important for athletes to progressively work into these motions to be successful when they return to sport. Finally, clinicians should remember that although there is a bone stress injury in the lumbar spine, athletes use their entire body when participating in sport. Impairments in other regions can increase stress throughout the lumbar spine and should be addressed.83,84 REHABILITATION This rehabilitation program (Table 1) is designed with three phases to progress patients through their rehabilitation. The first, “isolated” phase uses exercises that target specific muscle groups. The “integrated” phase emphasizes coordinated performance of the muscles throughout the body during functional exercises. The final “return to sport” phase highlights advanced exercises and sport reintegration. Progression is based on achieving specific criteria, as opposed to following a rigid, time-based protocol. This approach allows athletes to progress at their own pace, yet still ensures safe and comprehensive care.

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Table 1. Physical Therapy for Youth Athletes with Spondylolysis.

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To guide treatment initially, it is essential to understand the following conceptualization of the trunk muscles. This conceptualization draws a distinction between two muscular systems based on their functional role: a local muscle system and a global muscle system. The local system provides precise, tonic segmental stabilization, while the global system is responsible for movement generation.85 This two-category grouping of trunk muscles is listed in Table 2. PHASE I – ISOLATED TRAINING Objectives of Phase I At the outset of Phase I, clinicians have a critically important role in promoting positive beliefs about LBP. Even with the presence of a spondylolytic injury, patients should be encouraged to stay active and view movement as beneficial to their recovery. Initially, patients will benefit from avoiding paineliciting activities. However, this guidance should be offered within the overarching theme of remaining active. Exercise interventions in this phase target isolated muscle groups and any movement restrictions. It should be noted that scapular stabilizers, hip muscles and other muscles of the local system likely need attention as well. Adolescent athletes with acute spondylolysis may need interventions for pain

control, such as therapeutic modalities or manual therapy. Like other populations with LBP, these interventions should be used sparingly. Thrust (manipulation) manual therapy is not recommended in the lumbar spine. When pain-control interventions are used, the goal should be to promote activity and exercise. Muscle Performance Considerations The patient is encouraged to begin targeted exercises to improve activation and performance of the local muscle system. Exercises should occur in a painminimized neutral position, and not in end-range. Exercises can be progressed by adding extremity movements while maintaining a neutral spinal position. Detailed descriptions of local stabilization have previously been described.85 Younger patients may have difficulty performing or engaging in the focused local exercises in Phase I. The authors find that use of external feedback such as attempting to keep a half foam roll or towel roll steady on their back or abdominal muscles may help with performance. For these athletes who find these “low level” exercises too easy or boring, adding an unstable surface, can increase difficulty and improve patient engagement. Mobility Considerations In this first phase, athletes should achieve lumbar motion required for activities of daily living. For

Table 2. Local and Global Muscle Systems of the Core. (Adapted from Hoogenboom and Kiesel31).

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most adolescent athletes, specific motion exercises will not be necessary as their motion will return once the pain subsides. Patients with spondylolysis may present with decreased flexibility of the hip flexor and hamstring muscles.19,25,86 Excessive tightness of the hip flexor muscles results in increased lumbar lordosis, which can increase the stress on the posterior elements of the lumbar spine.87 If the clinician determines that stretching of these muscles is appropriate, care should be taken to maintain a neutral spine position while stretching. Clinicians should identify and address impairments in other areas of the body integral to the athlete’s sport. A good understanding of each patient’s sport and sport-specific movements can help identify a relationship between the individual’s LBP and a seemingly unrelated impairment. For example, a baseball pitcher who has limited trunk rotation and shoulder external rotation may perform excessive lumbar extension and rotation to be able to pitch effectively.88 This excessive lumbar motion results in increased lumbar stress which is compounded by the repetitive nature of pitching and may be a potential cause of spondylolysis.81 Phase I Tests and Criteria to Progress to Phase II Tests of the local muscles guide exercise selection and verify progress in the first phase. Qualitative assessment via palpation is an acceptable method, but the pressure biofeedback unit test of the transversus abdominis and the multifidus lift test attempt to bring more objectivity and standardization.89,90 The transversus abdominis should be judged as “good,” defined by a 4 mmHG drop for at least 10 seconds using a pressure biofeedback device in prone (Figure 3), and an obvious (palpable) contraction of the multifidus should be noted (Figure 4).72 Although the multifidus is difficult to assess clinically, the multifidus lift test has shown acceptable reliability (Kappa 0.75-0.81) and a moderate correlation with real-time ultrasound imaging.90 At the end of Phase I, the clinician should assess the quality and quantity of lumbar motion. Lumbar motion can be assessed using an inclinometer,91 and the athlete should be able to demonstrate lumbar motion within normal limits. Clinicians

Figure 3. Pressure Biofeedback Unit Test of the Transverse Abdominis. The patient is prone over a pressure biofeedback device, which is inﬂated to 70 mmHg. The therapist provides the cue “Draw in abdominal wall for 10 seconds without moving your back and while breathing normally.” The therapist records the length of time the patient can hold a ≥4mmHg drop, while monitoring for improper compensations. Performance is considered “good” with a duration of 10 seconds or greater.

Figure 4. Multifidus Lift Test. Patient lies prone, with shoulders at approximately 120˚ of abduction and elbows at 90˚ of flexion. The therapist palpates immediately lateral and adjacent to the interspinous space of L4/L5 and L5/S1. The patient is instructed to lift their contralateral arm towards the ceiling approximately 5 cm. The therapist qualitatively assesses multifidus as contralateral arm is lifted. A normal contraction is described as a robust and obvious muscle contraction, while little or no palpable contraction is considered abnormal.

must recognize that functional motion for athletes will likely exceed normal ranges in some sports. Repeated forward and backward bending of the lumbar spine should be pain-free and without aberrant movement.92

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PHASE II – INTEGRATED TRAINING Objectives The goal of Phase II is to integrate the local muscle system with the global muscle system during dynamic functional exercises. In this phase, exercises should incorporate greater resistance and be performed throughout increasing ranges of spinal motion. Additionally, the endurance of the local muscle system should be progressed to prepare for the demands of the athlete’s sport. During this phase, the athlete should achieve sufficient strength and flexibility in other to ensure controlled spinal movement during functional activities including extension. Muscle Performance Considerations In contrast to the initial phase when the spine remains in static, supported positions, patients now perform unsupported, dynamic exercises. Exercises advance to functional upright positions and progress from single plane to multiple planes including end-range spinal movements while assuring proper movement patterns. Clinicians should include exercises that build eccentric strength and force development. Additionally, clinicians must not forget about the strength of other muscles in the sport specific kinetic chain, including the hips, scapulothoracic, and shoulder musculature.

athlete’s extensor muscles (Figure 5).93 The supine double leg lowering test can assess global trunk flexion performance (Figure 6). Lateral core strength and endurance can be assessed using a timed lateral plank. The patient should demonstrate full, painfree lumbar movement all directions. The MFS can provide insight into the patient’s beliefs about their functional level and scores should approach 0% on

Figure 5. Prone Double Leg Raise Test. The patient is positioned in prone with hands underneath their forehead. The therapist instructs the patient to raise both legs until their knees are off the table and hold the position. The test is timed until the patient can no longer maintain knee clearance or reports pain.

Mobility Considerations Exercise progressions should promote controlled, normalized lumbopelvic rhythm and be monitored to avoid uncontrolled lumbar motion.82 The functional motion an athlete needs for sport, not only in the lumbar spine but also in other areas such as the hips and shoulders, often exceeds normal motion. Therefore, clinicians should focus on achieving sufficient motion for the demands of sport. Phase II Tests and Criteria to Progress to Phase III The athlete’s ability to integrate the local and global muscle systems during dynamic functional movement will be assessed using clinical tests recommended in the LBP clinical practice guidelines to assess trunk muscle power and endurance.78 The prone double leg raise can be useful to judge the pain-free performance and endurance of the

Figure 6. Supine Double Leg Lowering Test. The patient is positioned in supine; the therapist elevates both of the patient’s fully extended legs to the point at which the sacrum begins to rise off the table. The patient is instructed to maintain contact of the low back with the table while slowly lowering extended legs to the table without assistance. The examiner observes and measures when the lower back loses contact with the tabletop due to anterior pelvic tilt.

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the ADL (part B) and pain (part C) subsections. It is important to consider the requirements of the athlete’s sport as certain sports require greater strength, power, endurance and mobility to be successful and the patient should demonstrate sufficient motion and strength in their sport/position specific kinetic chain. PHASE III – RETURN TO SPORT Objectives of Phase III The primary objective of this phase is to reintegrate the athlete back into sport. The second objective is to ensure that the athlete is able to translate dynamic core exercises to sport specific activity. The third objective is to maximize aerobic capacity, endurance, and sport specific strength. As the athlete has been at a reduced level of activity, their aerobic capacity, endurance, and sport specific muscle strength may have suffered. Clinicians must not forget that athletes can practice for hours most days of the week and one to two hours of physical therapy a week is not adequate preparation. Finally, the clinician should work with the athlete and family to establish a proper training regimen and ongoing independent management program following discharge. Phase III Considerations Successful reintegration of the athlete into sport cannot be completed solely within the confines of the clinic. The athlete should perform a monitored, graded return to practice and competition. The clinician should communicate with the family, coach and the athletic trainer to determine an appropriate initial tolerable level of sport participation. Input from all of these sources will help the clinician know when to progress the athlete until they are participating fully in all aspects of sport. Injured athletes should progressively perform higher levels of sport activity until they can fully resume sport safely as an effective athlete. The return-to-sport progression may be relatively short or take many weeks depending on how long the athlete was out of sport as well as the intensity and level of the sport to which they are returning. An overview of how to progress each athlete back to their desired sport is outside of the scope of this commentary, but many return-to-sport progressions exist which can guide clinicians who may be unfamiliar with this process.94-98

Sport specific exercises should mimic the wide array of activities the athlete will need to perform. Balls and unstable surfaces can be incorporated to stress the athlete’s ability to respond in the unpredictable environment of their sport. Patient assessment and criteria for discharge Phase III At this stage of rehabilitation, athletes are returning to sport and preparing for discharge. The athlete’s sport-specific mechanics should be assessed for impaired movement or compensations throughout the kinetic chain. Attaining perfect form is unlikely and not expected in these adolescent athletes, however even minor improvements may help reduce the stress on the pars interarticularis as the athlete resumes sport.81,82 The clinician should also monitor the athlete’s symptoms as they reintegrate back into sport. Athletes should be able to resume similar competitive levels with little to no pain even during high level sport activity.60 There are no significant change scores reported for the MFS, but in our experience most athletes score at or near zero at discharge. CONCLUSIONS Evidence in non-surgical care of isthmic spondylolysis in adolescents is growing and physical therapy is frequently recommended, thus, this commentary provides much needed guidance regarding the phased implementation of physical therapy care. Although the physical therapy recommendations in this commentary are largely based on expert opinion and research generalized from similar populations, they are helpful in establishing a safe and effective approach for treating adolescent athletes with a spondylolysis. Additionally, the rehabilitation program in this commentary may serve as a framework for developing additional studies designed to assess physical therapy care for this population. REFERENCES 1. Burton AK, Clarke RD, McClune TD, et al. The natural history of low back pain in adolescents. Spine (Phila Pa 1976). 1996;21(20):2323-2328. 2. Calvo-Munoz I, Gomez-Conesa A, Sanchez-Meca J. Prevalence of low back pain in children and adolescents: a meta-analysis. BMC Pediatr. 2013;13:14.

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31. Kobayashi A, Kobayashi T, Kato K, et al. Diagnosis of radiographically occult lumbar spondylolysis in young athletes by magnetic resonance imaging. Am J Sports Med. 2013;41(1):169-176.

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33. Miller R, Beck NA, Sampson NR, et al. Imaging modalities for low back pain in children: a review of spondyloysis and undiagnosed mechanical back pain. J Pediatr Orthop. 2013;33(3):282-288.

48. El Rassi G, Takemitsu M, Glutting J, et al. Effect of sports modiﬁcation on clinical outcome in children and adolescent athletes with symptomatic lumbar spondylolysis. Am J Phys Med Rehabil. 2013;92(12):1070-1074.

34. Rush JK, Astur N, Scott S, et al. Use of magnetic resonance imaging in the evaluation of spondylolysis. J Pediatr Orthop. 2015;35(3):271-275. 35. Ledonio CG, Burton DC, Crawford CH, 3rd, et al. Current evidence regarding diagnostic imaging methods for pediatric lumbar spondylolysis: a report from the scoliosis research society evidence-based medicine committee. Spine Deform. 2017;5(2):97-101. 36. Tofte JN, CarlLee TL, Holte AJ, et al. Imaging pediatric spondylolysis: a systematic review. Spine. 2017;42(10):777-782. 37. Brodke DS, Goz V, Lawrence BD, et al. Oswestry disability index: a psychometric analysis with 1,610 patients. Spine J. 2017;17(3):321-327. 38. Kent P, Grotle M, Dunn KM, et al. Rasch analysis of the 23-item version of the Roland Morris Disability Questionnaire. J Rehabil Med. 2015;47(4):356-364. 39. Hall AM, Maher CG, Latimer J, et al. The patientspeciﬁc functional scale is more responsive than the Roland Morris disability questionnaire when activity limitation is low. Eur Spine J. 2011;20(1):79-86. 40. d’Hemecourt PA, Zurakowski D, d’Hemecourt CA, et al. Validation of a new instrument for evaluating low back pain in the young athlete. Clin J Sport Med. 2012;22(3):244-248.

49. Sys J, Michielsen J, Bracke P, et al. Nonoperative treatment of active spondylolysis in elite athletes with normal X-ray ﬁndings: literature review and results of conservative treatment. Eur Spine J. 2001;10(6):498-504. 50. Iwamoto J, Takeda T, Wakano K. Returning athletes with severe low back pain and spondylolysis to original sporting activities with conservative treatment. Scand J Med Sci Sports. 2004;14(6):346-351. 51. Standaert CJ. Spondylolysis in the adolescent athlete. Clin J Sport Med. 2002;12(2):119-122. 52. Selhorst M, Fischer A, Graft K, et al. Timing of physical therapy referral in adolescent athletes with acute spondylolysis: a retrospective chart review. Clin J Sport Med. 2017;27(3):296-301. 53. d’Hemecourt PA, Zurakowski D, Kriemler S, et al. Spondylolysis: returning the athlete to sports participation with brace treatment. Orthopedics. 2002;25(6):653-657. 54. Kraft DE. Low back pain in the adolescent athlete. Pediatr Clin North Am. 2002;49(3):643-653. 55. McTimoney CA, Micheli LJ. Current evaluation and management of spondylolysis and spondylolisthesis. Curr Sports Med Rep. 2003;2(1):41-46.

41. MacDonald JP, d’Hemecourt PA, Micheli LJ. The reliability and validity of a pediatric back outcome measure. Clin J Sport Med. 2016;26(6):490-496.

56. Steiner ME, Micheli LJ. Treatment of symptomatic spondylolysis and spondylolisthesis with the modiﬁed Boston brace. Spine. 1985;10(10):937-943.

42. Kurd MF, Patel D, Norton R, et al. Nonoperative treatment of symptomatic spondylolysis. J Spinal Disord Tech. 2007;20(8):560-564.

57. King HA. Back Pain in Children. Orthop Clin North Am. 1999;30(3):467-474.

43. Buck JE. Direct repair of the defect in spondylolisthesis. Preliminary report. J Bone Joint Surg Br. 1970;52(3):432-437. 44. Nicol RO, Scott JH. Lytic spondylolysis. Repair by wiring. Spine. 1986;11(10):1027-1030. 45. Radcliff KE, Kalantar SB, Reitman CA. Surgical management of spondylolysis and spondylolisthesis in athletes: indications and return to play. Curr Sports Med Rep. 2009;8(1):35-40.

58. Kessous E, Borsinger T, Rahman A, et al. Contralateral spondylolysis and fracture of the lumbar pedicle in a young athlete. Spine. 2017;42(18):E1087-e1091. 59. Hu SS, Tribus CB, Diab M, et al. Spondylolisthesis and spondylolysis. J Bone Joint Surg Am. 2008;90(3):656-671. 60. Selhorst M, Fischer A, Graft K, et al. Long-rerm clinical outcomes and factors that predict poor prognosis in athletes after a diagnosis of acute

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spondylolysis: a retrospective review with telephone follow-up. J Orthop Sports Phys Ther. 2016;46(12):1029-1036. 61. Sousa T, Skaggs DL, Chan P, et al. Benign natural history of spondylolysis in adolescence with midterm follow-up. Spine Deform. 2017;5(2):134-138. 62. Overley SC, McAnany SJ, Andelman S, et al. Return to play in adolescent athletes with symptomatic spondylolysis without listhesis: a meta-analysis. Global Spine J. 2018;8(2):190-197. 63. Ahlqwist A, Hagman M, Kjellby-Wendt G, et al. Physical therapy treatment of back complaints on children and adolescents. Spine. 2008;33(20):E721-727. 64. Selhorst M, Selhorst B. Lumbar manipulation and exercise for the treatment of acute low back pain in adolescents: a randomized controlled trial. J Man Manip Ther. 2015; 23:226-33. 65. Bono CM. Low-back pain in athletes. J Bone Joint Surg Am. 2004;86-a(2):382-396. 66. Miller SF, Congeni J, Swanson K. Long-term functional and anatomical follow-up of early detected spondylolysis in young athletes. Am J Sports Med. 2004;32(4):928-933.

75. Wang JP, Zhong ZC, Cheng CK, et al. Finite element analysis of the spondylolysis in lumbar spine. Biomed Mater Eng. 2006;16(5):301-308. 76. O’Sullivan PB, Phyty GD, Twomey LT, et al. Evaluation of speciﬁc stabilizing exercise in the treatment of chronic low back pain with radiologic diagnosis of spondylolysis or spondylolisthesis. Spine. 1997;22(24):2959-2967. 77. Ward SR, Kim CW, Eng CM, et al. Architectural analysis and intraoperative measurements demonstrate the unique design of the multiﬁdus muscle for lumbar spine stability. J Bone Joint Surg Am. 2009;91(1):176-185. 78. Delitto A, George SZ, Van Dillen LR, et al. Low back pain. J Orthop Sports Phys Ther. 2012;42(4):A1-57. 79. Lawrence KJ, Elser T, Stromberg R. Lumbar spondylolysis in the adolescent athlete. Phys Ther Sport. 2016;20:56-60. 80. Berger RG, Doyle SM. Spondylolysis 2019 update. Curr Opin Pediatr. 2019;31(1):61-68. 81. Singh H, Lee M, Solomito MJ, et al. Lumbar hyperextension in baseball pitching: A potential cause of spondylolysis. J Appl Biomech. 2018:1-6.

67. Covassin T, Beidler E, Ostrowski J, et al. Psychosocial aspects of rehabilitation in sports. Clin Sports Med. 2015;34(2):199-212.

82. Smith J. Moving beyond the neutral spine: stabilizing the dancer with lumbar extension dysfunction. J Dance Med Sci. 2009;13(3):73-82.

68. Tracey J. The emotional response to the injury and rehabilitation process. Journal of Applied Sport Psychology. 2003;15(4):279-293.

83. Sueki DG, Cleland JA, Wainner RS. A regional interdependence model of musculoskeletal dysfunction: research, mechanisms, and clinical implications. J Man Manip Ther. 2013;21(2):90-102.

69. Mainwaring LM. Restoration of self: A model for the psychological response of athletes to severe knee injuries. Canadian Journal of Rehabilitation. 1999;12:143-154. 70. O’Sullivan P, Smith A, Beales D, et al. Understanding adolescent low back pain from a multidimensional perspective: Implications for management. J Orthop Sports Phys Ther. 2017;47(10):741-751. 71. Stewart MA. Effective physician-patient communication and health outcomes: a review. CMAJ. 1995;152(9):1423-1433. 72. Sakamaki T, Katoh S, Sairyo K. Normal and spondylolytic pediatric spine movements with reference to instantaneous axis of rotation. Spine. 2002;27(2):141-145. 73. Mimura M. [Rotational instability of the lumbar spine--a three-dimensional motion study using bi-plane X-ray analysis system]. Nihon Seikeigeka Gakkai Zasshi. 1990;64(7):546-559. 74. Niggemann P, Kuchta J, Beyer HK, et al. Spondylolysis and spondylolisthesis: prevalence of different forms of instability and clinical implications. Spine. 2011;36(22):E1463-1468.

84. Shimamura KK, Cheatham S, Chung W, et al. Regional interdependence of the hip and lumbopelvic region in divison ii collegiate level baseball pitchers: a preliminary study. Int J Sports Phys Ther. 2015;10(1):1-12. 85. Hoogenboom BJ, Kiesel K. 74 - Core stabilization training. In: Giangarra CE, Manske RC, editors. Clinical Orthopaedic Rehabilitation: a Team Approach (Fourth Edition). Philadelphia: 2018. p. 498-513.e491. 86. Purcell L, Micheli L. Low back pain in young athletes. Sports Health. 2009;1(3):212-222. 87. Bugg WG, Lewis M, Juette A, et al. Lumbar lordosis and pars interarticularis fractures: a case-control study. Skeletal Radiol. 2012;41(7): 817-822. 88. Wasser JG, Zaremski JL, Herman DC, et al. Prevalence and proposed mechanisms of chronic low back pain in baseball: part i. Res Sports Med. 2017;25(2):219-230. 89. Storheim K, Bo K, Pederstad O, et al. Intra-tester reproducibility of pressure biofeedback in

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90.

91.

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93.

measurement of transversus abdominis function. Physiother Res Int. 2002;7(4):239-249. Hebert JJ, Koppenhaver SL, Teyhen DS, et al. The evaluation of lumbar multifidus muscle function via palpation: reliability and validity of a new clinical test. Spine J. 2015;15(6):1196-1202. Saur PM, Ensink FB, Frese K, et al. Lumbar range of motion: reliability and validity of the inclinometer technique in the clinical measurement of trunk flexibility. Spine. 1996;21(11):1332-1338. Hicks GE, Fritz JM, Delitto A, et al. Interrater reliability of clinical examination measures for identification of lumbar segmental instability. Arch Phys Med Rehabil. 2003;84(12):1858-1864. Arab AM, Salavati M, Ebrahimi I, et al. Sensitivity, specificity and predictive value of the clinical trunk muscle endurance tests in low back pain. Clin Rehabil. 2007;21(7):640-647.

94. Hurd W, Hunter-Giordano A, Axe M, et al. Databased interval hitting program for female college volleyball players. Sports Health. 2009;1(6):522-530. 95. Spigelman T, Sciascia A, Uhl T. Return to swimming protocol for competitive swimmers: a post-operative case study and fundamentals. Int J Sports Phys Ther. 2014;9(5):712-725. 96. Jayanthi N, Esser S. Racket sports. Curr Sports Med Rep. 2013;12(5):329-336. 97. Chang ES, Bishop ME, Baker D, et al. Interval throwing and hitting programs in baseball: Biomechanics and rehabilitation. Am J Orthop. 2016;45(3):157-162. 98. Sweeney EA, Howell DR, James DA, et al. Returning to sport after gymnastics injuries. Curr Sports Med Rep. 2018;17(11):376-390.

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IJSPT

ORIGINAL RESEARCH

PAST, CURRENT AND FUTURE INTERVENTIONAL ORTHOBIOLOGICS TECHNIQUES AND HOW THEY RELATE TO REGENERATIVE REHABILITATION: A CLINICAL COMMENTARY Christopher J. Centeno, MD1,2 Sarah M. Pastoriza, DO1

ABSTRACT Interventional orthobiologics is changing the landscape of orthopedic medicine. Various methods exist for treatment of many different musculoskeletal pathologies. Candidacy for such injections remains a debated topic, and current research is underway for stratifying the patients that would be most successful for certain techniques. Described in this commentary are the various methods of interventional orthobiologic techniques available such as: prolotherapy, platelet rich plasma (PRP), mesenchymal stromal cells (MSCs), culture-expanded MSCs and amniotic-based products. Here we review the healing cascade and how this relates to the application of the various injectates and rehabilitation protocols. In conclusion, there exists orthobiologic techniques for the healing of a multitude of musculoskeletal ailments, from ligamentous instabilities/tears, tendon derangements and osteoarthritis, however candidacy grades continue to be an area for discussion as to which type of treatment is the most beneficial, and which rehabilitation protocols are required. More randomized controlled trials and comparative analyses are needed for direct correlative conclusions for which interventional orthobiologic treatment and rehabilitation protocol is best after each respective treatment. Level of Evidence: 5 Key words: mesenchymal stromal cells (MSCs), orthobiologics, orthopedic medicine, Platelet Rich Plasma (PRP), regenerative medicine, regenerative rehabilitation, Stem Cells

1 2

Centeno-Schultz Clinic, Broomﬁeld, CO, USA Regenexx, LLC, Des Moines, IA, USA

Conﬂicts of interest: CC is a shareholder and CMO of Regenexx, LLC and president and owner of the CentenoSchultz Clinic. SP has declared no competing interests.

CORRESPONDING AUTHOR Sarah M. Pastoriza, DO 403 Summit Blvd Suite 201, Broomﬁeld, Colorado 80021, USA Tel: 303-429-6448 Fax: 303-957-5797 E-mail: spastoriza@centenoschultz.com

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 301 DOI: 10.26603/ijspt20200301

INTRODUCTION TO REGENERATIVE REHABILITATION Regenerative rehabilitation is defined by the American Physical Therapy Association as the integration of interventional orthobiologic techniques coupled with appropriate rehabilitation protocols that harness the bodies innate healing mechanisms through movement to augment the orthobiologic injections.1 From regenerative rehabilitation stems a separate but interconnected field known as mechanotherapy. Mechanotherapy refers to the therapeutic modalities used to propagate the physiologic mechanism by which body movements provide mechanical stimuli to remodel cells. This field examines mechanobiology, transduction and adaptation to effectively direct tissue modeling and remodeling.2 In 2016, mechanotherapy was defined as exercise-based activity that promoted the adequate force through a specific bodily structure that contributed to the restructuring, stabilization and eventual contribution to healing.3 Physical therapy is a pivotal part of the regenerative/orthobiologic landscape. The aim of all regenerative therapy is to facilitate healing through targeted specific mechano-adaptations (through appropriate exercise and mobilization of joints) in order to foster healthy balance of forces to prevent future injuries and maximize well-being.4 Understanding interventional orthobiologics procedures and how cellular responses respond to mechano-transduction will help guide the development of appropriate rehabilitation programs for each type of regenerative therapy.5 The purpose of this commentary is to provide a history of orthobiologics and describe the role of rehabilitation after these interventional procedures. This will allow the reader to better understand the physiology of disease states requiring orthobiologic interventions and to describe how interventional orthobiologics should be coupled with rehabilitation for optimal healing and return to function. THE HEALING CASCADE, AS IT RELATES TO THE MUSCULOSKELETAL SYSTEM The healing cascade encompasses three major phases: 1) inflammation, 2) proliferation, and 3) maturation.6 Inflammation is the start of the healing cascade from injury to approximately days 4 to 6,

and the beginning is characterized by initial bleeding from injury which causes the body to need to stop the bleeding with vasoconstriction which activates the coagulation cascade which leads to formation of a clot from platelets composed of collagen, thrombin and fibronectin.5 This clot works as the scaffold for other healing cells such as cytokines and growth factors to invade and start the inflammatory cascade. Growth factors modulate healing and the inflammatory phase which then results in vasodilatation with increased vascular permeability and migration of cells.6 The inflammatory phase also summons neutrophils through various cell signaling, which help with managing cellular debris while uninjured tissues are protected by protease inhibitors.7 Subsequently, the body switches to other cells known as monocytes that signal macrophages to move in to clear out the neutrophils to then release fibroblasts and begin the proliferative phase of healing.5 Proliferation is characterized by angiogenesis and fibroplasia, modulated by the fibroblasts and epithelial cells during approximately days four to 14. Angiogenesis occurs as a mechanism of the body to enhance blood flow to the injured area. Next, fibroplasia commences when fibroblasts come in and begin to lay down collagen. Maturation and remodeling is the phase between approximately day 8 and one year composed of strengthening of the extracellular matrix (ECM) and production of collagen in an organized network.5 The organization continues to form along lines of stress, however it never returns back to its original state.6 The estimation regarding the amount of time each phase takes is dependent on patient age, comorbidities, and level of injury. There is not a distinct stepwise approach but more of a progression with overlap of the various phases of healing. This is more of an estimate to help in coordinating appropriate rehab protocols after injury. The largest difference between regenerative rehabilitation and post-orthopedic surgery rehabilitation is not only to get the patient back to activity that was being done prior to the intervention, but also to change the biomechanical factors that contributed to the injury in the first place.

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MUSCULOSKELETAL TISSUES: STRUCTURE AND FUNCTION RELATED TO HEALING The musculoskeletal system is composed of different types of connective tissue, including muscles, tendons, ligaments, cartilage and bone.7 Each of these tissues is unique with regard to function and composition, and has healing potential, to some degree, Muscles The main function of muscle is to generate contractions that transmit load across a joint to facilitate motion and provide stability.7 In skeletal muscle injury the healing cascade is activated when the muscle tissue is injured, due to myofiber rupture along with damage to local capillaries. This triggers an influx of calcium and clot formation begins.9 Inflammatory cells migrate to the injured site, activates fibroblasts and satellite cells (SC’s) which are myogenic stem cells.7-10 During the proliferative phase of muscle healing, SC’s differentiate into myoblasts, and in the remodeling phase the new myofibers differentiate into muscle fibers.7,10 The ability of skeletal muscle to respond to trauma such as associated with exercise, immobilization, trauma, or chemical insult relies on the regenerative capacity that exists due to the presence of myogenic SC’s.11 Teixeira et al. proposed that skeletal muscle loading may increase the number of SC’s, their proliferation, and their differentiation capacities which collectively enhances skeletal muscle regeneration. Skeletal muscle loading increases both vascularization and collagen turnover.11 The data collected by Teixeira et al suggests that active skeletal muscles (muscle that has been in movement such as after exercise) might be better prepared to respond effectively to a muscle injury. Therefore, the authors implied that even electric stimulation should be considered in limbs that have impaired movement to preserve the SC pool in order to improve skeletal muscle rehabilitation.11 Tendons Tendons primarily function to interlink the muscle and bone and have been demonstrated to have specific structural characteristics. The location of a tendon in vivo affects the mechanics and the amount of shear, compression, tension or torque placed on a

tendon, which makes in vitro modeling of tendons difficult to extrapolate.12 Tendinopathies encompass over 30% of all musculoskeletal consultations.13 The process of tendon remodeling involves both synthesis and degradation of collagen with a net degradation that begins immediately after exercise then shifts to a net synthesis.14 Matrix metalloproteinases (MMP) have been shown to play a part in tendinopathy, however, it is unclear whether overloading inhibits the MMP activity leading to the transformation from adaptation to degeneration.15 Mechano-biologically, tendons have been shown to improve with loading which activate protein kinases and increase turnover of Type 1 collagen to promote anabolism.16,17 The underlying mechanisms associated with pathogenesis of tendinopathies is largely unknown.18 However, many orthobiologic treatments have been targeted to manage various upper and lower extremity tendinopathies. Ligaments Ligaments function to link bones with other bones, in order to stabilize a joint. Ligaments function in a similar model to tendon, however with decreased tensile loads. They function to provide passive joint stability throughout normal range of motion of a joint and to provide joint proprioception.7,19 Traumatic ligamentous injury can result in either a partial or complete tear and can proceed through the typical three phases of healing that includes inflammation, proliferation and remodeling.7 During the first phase, retraction of the disrupted segments of ligament forms a gap and within that gap a clot forms reigning in cytokines and the inflammatory phase.7,20,21 In the fibroblast/ proliferation phase the disorganized fragments are mostly composed of less organized collagen, and in the remodeling phase the fragments start to organize and improve to withstand tensile loads and for force transmission.7 Ligamentous tissue that has been damaged and then heals, is not as elastic as the original healthy ligament.7,22 Cartilage The articular cartilage present in joints can withstand an impressive amount of forces (compression, shear, etc.) and allows for smooth gliding motion without

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friction.7 The absence of blood supply is what limits the healing capabilities of articular cartilage. A defect that penetrates cartilage into the subchondral plate has a greater capacity to heal because it may facilitate clot formation and cell migration7,23. Once cartilage heals it is histologically more like fibrocartilage than hyaline cartilage and will be stiffer than original cartilage.7,24,25 Bone Bone also proceeds through the same healing cascade of inflammation, proliferation and remodeling. With a fracture, the inflammation phase begins with bleeding and then the clot forms. The release of cytokines and growth factors which are responsible for proliferation of chrondroblasts and osteoblasts fills the fracture site with granulation tissue.7,26,27 Chrondrocytes initially form a soft callus then osteoblasts gradually replace soft callus with immature woven bone and eventually to hard callus.7,28 If bony fragments from a fracture are well approximated the healing is more reliable than a torn ligament or tendon due to the inherent blood supply of the bone that is absent in other tissues. REVIEW OF INTERVENTIONAL ORTHOBIOLOGIC TECHNIQUES Because each tissue type in the body has differences and similarities in healing, orthobiologic techniques have been developed that are specific to each connective tissue type. Vora et al. described regenerative therapy (a.k.a interventional orthobiologics) as â&#x20AC;&#x153;the injection of a small volume of solution into multiple sites of painful ligament and tendon insertions and adjacent joint spaces, with the goal of reducing pain and ostensibly promoting tissue repair and growthâ&#x20AC;?.29 p. S104 The first type of regenerative therapy to be discussed is the use of a hypertonic solution known as prolotherapy that has aided in paving the field for other types of orthobiologic therapeutics. Prolotherapy Prolotherapy is the use of a composition of hypertonic dextrose solution for promoting local healing of chronically injured extra-articular and intra-articular tissue through stimulating both inflammatory and noninflammatory pathways. In the 1950s, Dr. George Hackett, a general surgeon in the United

States, formalized the injection protocols for prolotherapy as an orthobiologic injection technique.30 Liu et al injected the medial collateral ligaments of rabbits with sodium morrhuate (irritant), and found that after repeated injections there was a significant increase in collagen fibrils and this increased stabilization.31 Hypertonic dextrose is the most commonly used prolotherapy solution with favorable outcomes shown in multiple clinical trials dating back to the 2000s for treatment of OA.32 Dextrose prolotherapy is proposed to function by creating a hyperosmolar environment to induce the healing cascade via releasing growth factors and scarring down/forming collagen that eventually strengthens with improved tensile strength.32 This in-turn promotes the tightening or strengthening of a tissue from a big picture standpoint. The magnitude of benefit of prolotherapy is varied by treatment protocols, evaluation intervals, and therapeutic measurement tools.33 Clinical Research Two studies of dextrose prolotherapy in the treatment of hand osteoarthritis exist, one study compared it to steroid injection and the other compared prolotherapy to lidocaine. In the steroid comparison study hand movement and function improved more in the prolotherapy group at six months than the group receiving steroid injection.34 In the study comparing with lidocaine, the prolotherapy improved more in pain during movement and range of motion at six months as compared to those treated with lidocaine.35 Centeno et al. published a case series in 2005 in which the cervical posterior elements were injected under fluoroscopic-guidance, and demonstrated a statistically significant improvement in pain scores and improved stability in flexion translation.36 The use of dextrose prolotherapy for knee osteoarthritis is supported by Level 1 evidence in the form of a systematic review and meta-analysis published in 2016.37 Sit et al. compared four randomized controlled studies noted that intraarticular and periarticular hypertonic dextrose knee injections over three to five sessions had a statistically significant and clinically relevant effect in the improvement of function and pain when compared to formal home therapy exercise alone and the benefits were sustained for one year.35,38-40

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Low back pain and Sacroilitis A Cochrane review was performed in 2009 to determine if injection therapy with prolotherapy is more effective than placebo or other treatments for patients with subacute or chronic low back pain in which 18 trials were selected for review.41 The injection sites varied from epidural sites and facet joints (intra-articular, peri-articular and nerve blocks) to local sites (tender and trigger points) along with a variety of drugs that were compared including corticosteroids, local anesthetics, and a variety of other drugs which prevents head to head comparison.41 Only 10 of the 18 randomized controlled trials pooled were rated as a high-quality methodology; however, insufficient evidence was noted to support for or against the use of any injection therapy in the subacute and chronic low back pain.41 Kim et al published a randomized controlled trial noting that sacroiliac joint prolotherapy injections were found to be superior to steroid injections.42 And again, a retrospective cohort study by Hoffman et al noted that prolotherapy may be a satisfactory option for SI joint instability.43 A recent prospective study by Solmaz et al concluded that prolotherapy injections performed posterior and laterally may be a viable option prior to considering reoperation in failed back surgery syndrome (FBSS).44 All injections were done using ultrasound and posterior injections performed were directed to the posterior sacroiliac ligament insertions bilaterally, iliolumbar ligament insertions bilaterally, while lateral injections targeted the transverse ligament insertions and lumbar facet joints bilaterally. Laterally, the ultrasound was also used to direct injections into the pubofemoral ligamentous insertion, piriformis muscle origin and insertion, iliofemoral ligament insertion and ischiofemoral ligament insertion.44 Tendinopathy Rabago et al and Scarpone et al published two randomized-controlled trials that have demonstrated effectiveness of prolotherapy in lateral epicondylosis where prolotherapy participants showed improved isometric strength and grip strength compared to baseline status and to controls.45,46 Osgood Schlatter disease is a tendinopathy of the patellar

tendon at the tibial tubercle of children age 9-17 who are engaged in kicking sports.45 Prolotherapy was compared to lidocaine only, and at one year 84% of the prolotherapy treated knees were pain free with comparison to the 46% of lidocaine-treated knees.45 Treatment of rotator cuff tendinopathy was tested in a three-arm masked randomized controlled trial with comparison between prolotherapy and a control solution placed at the enthesis of the rotator cuff tendons and another a third group with a superficial saline injection.45,47 Pain was the primary outcome in the rotator cuff study, and 59% of the prolotherapy participants reported a 2.8-point change on the VAS (visual analog scale) pain score with comparison to 37% who received saline at the enthesis and 27% who received the superficial saline injections.45,47 The next orthobiologic is known as platelet rich plasma which is the use of concentrated autologous blood that has been separated into its most enriching growth factor components as further described below. Platelet Rich Plasma Platelet rich plasma (PRP) is a substance that is composed from whole blood which consists of higher concentration of platelets from whole blood that is spun down into separate components and concentrated to be more potent than is physiologically possible. The goal of the use of PRP is to have supra-therapeutic platelet concentration in a small volume of plasma in order to induce healing potential in tissue that has otherwise poor inherent healing capacity including joints, cartilage, tendons, and ligaments.48 PRP therapy initially gained popularity in dentistry and cardiac surgery in the 80â&#x20AC;&#x2122;s and 90â&#x20AC;&#x2122;s.48 The mechanism behind PRP is to enhance the healing cascade in a controlled fashion due to a higher concentration of platelets and growth factors being injected than are normally physiologically present. The platelets play a central role in the anabolic mechanism of healing by releasing growth factors stored in the alpha granules.48 The key growth factors stored in alpha granules are: Platelet-derived growth factor, transforming growth factor-beta, vascular endothelial growth factor, epidermal growth factor, basic fibroblast growth factor, and Insulin-like growth factor 1. A common misconception is that PRP is a stem cell treatment. PRP is not a stem cell procedure as the

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blood contains little if any circulating mesenchymal stromal cells (MSCs, aka stem cells) in comparison with bone marrow. The presence or absence of leukocytes in PRP is important. Leukocytes are essential mediators of the inflammatory response, that assist the host defense in protection against infectious agents, and contribute to wound healing.49 Although leukocytes aid in the protection against infectious agents, they can also oppose the intended healing effects of the platelets. Boswell et al. proposed that reducing leukocyte concentrations in PRP is more important than maximizing the PRP.49 It is important to note that red blood cells are eliminated from the PRP preparation as the iron contained in heme can release cytotoxic oxygen free radicals which can be a toxic/destructive process in human synoviocytes.48 Of note, application of PRP in individuals on NSAIDs is not recommended as NSAIDs inhibit platelet degranulation and therefore inhibit platelet function and may have a diminished therapeutic effect.48,50 Types of PRP and why does it matter? There are two types of PRP that are used for injections: 1) Leukocyte rich (LR-PRP) which is red in color and is rich in red (RBC) and white blood cells (WBC); 2) Leukocyte poor (LP-PRP) which is white blood cell (leukocyte) and red blood cell poor51 as shown in Figure 1. The composition of the preparations continues to be a widely debated topic for standardization proceedings and what types are better for which structures of the musculoskeletal system. Based on the literature for knee OA, the red LR-PRP can be toxic to synoviocytes,52 and on the other hand the amber has been shown to stimulate cartilage better than the red53 and was found to have more functionality and pain relieving benefits as compared to the red.52 The concern with removing the RBCs and WBCs is that healing cells are being eliminated, however it has been shown that taking out the RBCs and WBCs did not impact the PRPs ability to heal.54 The debate with maintaining leukocytes is that that type of PRP also maintains neutrophils which can be harmful to healing tissues and increase the inflammatory response. However, that leukocytes generally maintained are monocytes and lymphocytes which have been shown

Figure 1. Vials on the left of picture are red LR-PRP which has high concentration of platelets and also contains RBCs and WBCs. The amber colored vials on the right of the picture are LP-PRP without the RBCs or WBCs which contains the concentrated platelets as well. Used with permission from Centeno-Schultz Clinic.

to be present with stem cells and thus a higher percentage theoretically increases stem cells.55 Leukocyte rich PRP (amber with white blood cells) was shown to decrease cytokine production and promote tissue regeneration56 in tenocytes. More studies need to be conducted on the specific types of PRP in order to better stratify a standardized treatment protocol. Does concentration matter? Berger et al. demonstrated that concentration matters with reference to healing potential.57 Age plays a role in how much blood is needed to concentrate in order to obtain the desired effect; therefore, older cells tend to require higher PRP concentrations to kick start the healing cascade. Berger et al. concluded that higher concentrations of platelet lysate can induce tenocytes to heal tendinopathies in older populations.57 Clinical Evidence Tendinopathy Based on the previously described heterogeneity in processing, PRP has had variable reports of efficacy in the literature. PRP for common extensor

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tendinopathy has demonstrated efficacy in treating chronic common extensor tendinopathy when compared to steroids at one- and two-year followups.48,58,59 Examination of the results of treatment of Achilles and patellar tendinopathy in case series60-69 and retrospective studies70-72 has demonstrated that PRP injections improved function and pain with good functional outcomes for about four years post-injection. Many studies of rotator cuff tendinopathy have been performed with platelet rich fibrin injections done intraoperatively, however, platelet rich fibrin differs in concentration as compared to that which is used in PRP for tendinosis, not in an operating room setting. Gumina et al published on intraoperative PRP fibrin which improved repair integrity for large tears without an associated greater improvement in function73 and had lower re-tear rates for small to large tears at one year.48,73-76 Mautner et al. studied the optimization of ingredients for tendinopathy concluded that higher platelet counts with leukocytes and a slightly acidic pH injected under ultrasound guidance may be ideal to facilitate the healing of tendinopathies that have failed other conservative management.55 PRP in Osteoarthritis Osteoarthritis (OA) is related to intraarticular cartilage loss from a joint space, due to injury or joint instability, and is related to the inadequate healing cascade of articular cartilage, leading to subsequent additional degeneration. Laver et al. performed a systematic review which encompassed the treatment of hip and knee OA.77 Twenty-six of the included studies examined knee OA and three studies examined hip OA, and the results demonstrated variability in PRP processing, all injections were directed intraarticularly without other periarticular structures however the authors concluded that PRP can be beneficial for both knee and hip OA in terms of pain and functionality.77 Another systematic review conducted by Shen et al. demonstrated that intraarticular PRP injections are more efficacious in treatment of knee OA in terms of pain relief and functional improvement at 3, 6, and 12 months follow-up compared with other injectates (saline placebo, hyaluronic acid [HA], ozone, and corticosteroids).78 Most studies that have been performed are only performed via an intraarticular approach not taking

into consideration the entire joint and treating the instabilities (such as laxity of ligaments) that may have led to the osteoarthritis to begin with. However, a pilot study on knee osteoarthritis published by Sit et al, described a PRP injection protocol that involved a single intraarticular injection and extraarticular injections in the medial coronary and medial collateral ligaments.79 This is the start of exploring whether concomitant intra-articular and extraarticular PRP injections are feasible in producing a favorable outcome.79 In order to have decreased pain in osteoarthritis, off-loading the region of cartilage that is subjected to the highest force is important to prevent further degeneration, and part of rehabilitation protocols post knee procedures would be to recommend an unloader brace. It is important to note that treatments offered to date cannot regrow cartilage, however injecting the structures surrounding a lax or unstable joint can help to stabilize and improve the healing environment to improve pain and function. Lumbar Radiculopathy Low back pain with radiculopathy is treated most commonly with an epidural steroid injection which is the most commonly performed pain management procedure in the United States.80-82 The side effects of steroids have led to the trial of orthobiologics in the spine. Clinical evidence for PRP in the literature are mostly limited to treatment of facet and intradiscal pathology.80,83-85 Bhatia performed a small pilot study of PRP for the treatment of radiculopathy and reported gradual improvement in Visual Analog Scale, straight leg raise test and Oswestry Disability Index sustained over three months.86 Platelet lysate (PL) may be preferable to PRP for the treatment of radicular pain as PRP carries a potential for platelet adhesion and aggregation which increases the risk of vascular occlusion.87 PL is created by lysing platelets and removing cell debris, resulting in GF-rich (Growth Factor-rich) injectate, devoid of other platelet material.88 PL also has been shown to promote the proliferation of various cell types including mesenchymal stromal cells (MSCs) aka stem cells.89 PL has also been shown to be beneficial in peripheral nerve regeneration in patients with peripheral neuropathy and peripheral nerve

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regeneration after injury.90-95 Centeno et al. published a retrospective review of 470 patients treated with platelet lysate for lumbar radicular pain, and tracked them for 24 months.80 Over 72% of these patients reported significantly less pain after treatment which was sustained for 24 months.80 Patients also reported increased function over time which may suggest continued effect of PL over time.80 PRP and PL therapies tend to have a prolonged recovery time, which are directly correlated with the healing cascade and the phases of healing as portrayed in Figure 2: The general timeline depicted in Figure 4 can be extrapolated to represent the phases of healing

Figure 2. Depicts the healing cascade as it relates to healing after a PRP injection.

involved and how long it takes with PRP injections. However, there is a range among patients as this depends on the structure being treated. For example, in mild knee osteoarthritis the initial inflammatory flare can last from a few days to a week and then the patient will start to feel better over the course of a few weeks, and in this scenario the LR-PRP vs LP-PRP does not seem to make a difference in flare response. The flare response and timing after an injection varies. Figure 5 demonstrates the level of pain and how it can be gradual with “ups” and “downs” prior to completely healing. Joints tend to be “faster responders” than tendons and ligaments. Typically, tendons and ligaments can take up to two to three months to feel improvement. One study on patients with lateral epicondylosis noted that significantly more patients noted improvement at six months than the three month mark post procedure.89 Also, in reference to pain, the patient may experience waxing and waning pain symptoms, and may take a “one-step forward, two-steps backward” approach with a trend being towards the positive as portrayed in Figure 3. Is PRP treatment permanent? If the disease process is in degenerative nature, the relief from PRP can last from one to two years in mild arthritis, however in more severe arthritis pain relief may only last a few to six months. In cases of arthritis, PRP works to attempt to improve the environment to help with pain but does not alter (regrow or regenerate cartilage) a degenerated joint. There are current trials being conducted on how the knee microenvironment and content within the synovial fluid can play a role in pain control. It is important to note that when using orthobiologics to treat tendons or ligaments the theory is that this intervention is more of a semi-permanent solution as it is assisting in repairing the tendon. With that said, many tendons can be stubborn and ligaments may require multiple treatments prior to deeming them as “healed”.

Figure 3. Describes the ebb and ﬂow of recovery after a PRP or Stem cell injection. There will be “Good” days and “Bad” days but the natural course will slowly progress to a decrease in pain, and tightening of the ligament and tendon. PRP has a shorter time course than stem cell treatments, however every patient varies on recovery rate.

The next orthobiologic is stem cells which can be harvested from bone marrow and fat, which contains nucleated cells and growth factors that serve to start the healing cascade.

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Figure 4. Pre and post MRI 9 months apart from Bone marrow stem cell injection into ACL and surrounding knee structures. Copyright release of photograph obtained during patient evaluation.

Stem Cells Stem cells have become a much-debated topic in the media, with the biggest difference being between embryonic and adult stem cells. From a treatment standpoint there is also a debate on how the adult cells are harvested and what the yield of cells is and how they are being processed which is what impacts treatment efficacy. Orthopedic surgeons have been using bone marrow aspirate in the use of non-union fractures and avascular necrosis for many years. A recommended treatment was first described in 1939 for non-union fracture that improved implantation of cancellous bone chips from the proximal tibia to stabilize the fixation.96 Hernigou et al. have been performing bone marrow stem cell injections into avascular necrosis lesions of the hip and knees which has been demonstrated to be a successful alternative to replacement in some patients.96-98 What cells sources for Stem Cells are used in orthopedics? The most common cell types include: bone marrow nucleated cells, adipose stromal vascular fraction (SVF), adipose fat grafts, and amniotic fluid stem cells, listed in order in which they will be discussed. There are two types of groups in the stem cell world and that is allogeneic (comes from another person) or autologous (comes from the person themself). Allogeneic stem cells are most commonly from the amniotic cord blood, followed by amniotic and embryonic tissues. Autologous stem cells are most

commonly from bone marrow aspiration or adipose-derived. The process of autologous-derived stem cells that is extracted from bone marrow or fat results in a heterogenous mixture of cells that can be centrifuged and lysed to create a more concentrated stem cell product. The process of taking cells out and concentrating them for use in orthopedic procedures under US FDA regulations is classified as “minimal manipulation”94,99 and legally acceptable. After the process of centrifugation, the resultant solution must be reinserted back into the patient within 24 hours in order to also meet the regulation standard of “minimal manipulation”. Any cell that is removed and cultured in vitro to increase the cell concentration over a number of weeks is not considered “minimal manipulation”99,100and is currently illegal in the United States. Mesenchymal Stem Cells Mesenchymal stem cells (MSCs) was a term coined in the 90’s to represent a class of cells that has in vitro capacity to form bone, cartilage, fat and other tissues via the mesogenic process.101,102 Because of their multipotent capabilities, MSC lineages have been used successfully in animal models to regenerate articular cartilage.103-117 In 2006, The International Society for Cellular Therapy recommended that cells should fulfill the following criteria to be considered as MSCs: 1) the cells must adhere to plastic in culture conditions; 2) must express CD markers, which are cluster for differentiation (CD) cell surface glycoprotein antigens such as 73, 90 and 105, and cannot express CD 34, 45, 14, 11b and 19, and cannot express HLA-DR; and 3)

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they should be able to differentiate into osteoblasts, chrondroblasts, and adipocytes in vitro.118 The perceived risk of these types of orthobiologic cell therapies has been the risk of cancer or tumor formation, however, Hernigou et al. published a 12.5 year follow-up of 1873 patients receiving autologous bone marrow-derived stromal progenitors and found no increased cancer/tumor risk at site of placement or in any other distant site.119 Centeno et al in 2016, reported on a total of 3012 procedures along with 2373 patients followed for up to 2.2 years demonstrated seven cases of reported neoplasms (lower than general population) and concluded that there is no increased risk of neoplasm with MSC treatment.120 What are the sources of MSCs? Bone marrow aspiration is a technique used to harvest bone marrow concentrate (BMC) which is derived from bone marrow stroma. The safest way to harvest this is with ultrasound or fluoroscopic guidance at the posterior iliac crest, as this has been shown to have the highest concentration of bone marrow MSCs.121 Multi-site draws of small volumes have been shown to yield the highest number of total nucleated cells.122 Hernigou et al. published positive outcomes on patients being treated with higher concentration of colony forming units (CFU) of BMC123,124 than lower concentrations that are found in raw bone marrow aspiration without concentrating it. Regarding dose, a higher concentration of total nucleated cells (TNCs) within bone marrow concentrate demonstrated more improvement and pain and function than lower concentrations,125,126 and Centeno et al. found TNC concentrations of >4x 108 to be the most effective.125 Adipose tissue is another source for harvesting MSCs via lipoaspiration of subcutaneous fat from areas such as the abdomen, flank, perigluteal region and thighs. However, studies have shown that bone marrow MSCs have greater intrinsic osteogenic and chondrogenic differentiation potential when compared with adipose MSCâ&#x20AC;&#x2122;s.127,128 Synovial MSCs came into favor with the hypothesis that MSCs closest to the target tissue would better differentiate into that target tissue. Koga et al. noted

that synovial MSCs have the greatest chrondrogenic potential and lowest osteogenic potential, while bone marrow has the greater osteogenic potential than does adipose.129 The utility of synovial MSC harvest is limited as it is low volume and the concentration cannot be improved without culture expansion, therefore this may be a consideration to be used in culture expansion techniques in the future. Bone Marrow Concentrate (BMC) Clinical Research Knee osteoarthritis is a common joint pain that afflicts approximately 50 million adults with a large healthcare expenditure.129-132 And the common regimen for people with severe osteoarthritis is non-steroidal anti-inflammatory drugs (NSAIDs), physical therapy, steroid injections or knee arthroplasty (TKA). Steroid injections have been shown to hasten the progression of cartilage loss.132,133 Complications of the above treatment options to date have many side effects and can be riddled with complications such as deep vein thrombosis and neuropathy with persistent pain after a TKA occurring in approximately 34% of patients.132,134,135 Cell based therapies have been researched previously and have some encouraging results although few controlled trials exist.132,136,137 Centeno et al. published a randomized controlled trial of a specific protocol of image-guided percutaneous injection of a combination of bone marrow concentrate (BMC) and platelet products versus an exercise therapy regimen. Comparing the exercise therapy group to the BMC group it was noted that there was significant improvement in activity levels, pain, ROM and stability at three months in the BMC group over those who followed a home exercise program alone.132 All of the exercise therapy group crossed over to the BMC group, and it was noted that at a two year follow-up there was still noted to be significant improvement in pain and function that was sustained after the BMC procedure.132 Centeno et al also conducted a prospective case series injecting autologous bone marrow concentrate as an investigational approach to treatment of anterior cruciate ligament (ACL) tears.138 Patients included in the study had sustained Grades 1-3 ligament injury, with 1cm or less of retraction.138 Grade 1 was defined as partial tear with less than half of the

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ligament disrupted, Grade 2 was defined as partial tear with greater than half of the ligament disrupted and Grade 3 was defined as a completely torn ligament.139 Seven of ten patients completed all pre- and post-procedural outcome measures including preand post- intervention imaging and demonstrated improvement in at least four of the five measures which were the Numeric Pain Scale (NPS), the Lower Extremity Functional Scale (LEFS), the International Knee Documentation Committee (IKDC) form, a modified version of the Single Assessment Numeric Evaluation (SANE), and grey scale measurements of the MRI to determine healing. Four of the five measures were statistically significantly different including the LEFS, SANE, IKDC and MRI grey scale measurements. ImageJ software was used to measure MRI pixel intensity and a trend towards darker ACLs (indicates more normal appearing) was demonstrated in five subjects, three of those subjects the change in pixel quality was statistically significantly different, however not completely normal appearing. Figure 4 demonstrates an MRI of a torn ACL at left and post procedure on the right, and this is an example of an MRI that was examined using ImageJ software, however the improvement is apparent to the naked eye. Post procedural rehabilitation was given with the goal of advancing activity as tolerated and allow the patient to load the ligament dependent on pain since past studies had demonstrated loading as being essential to ligament healing.138,140 Bracing was not part of the protocol and therapy regimens were not standardized. The authors concluded that although it was a small case series, the precise injection of autologous bone marrow-derived nucleated cells into the ACL maybe a viable treatment method for Grades 1,2 and non-retracted Grade 3 tears.138 Centeno et al studied a total of 115 shoulders in 102 patients who were treated with autologous BMC injections for symptomatic osteoarthritis at the glenohumeral joints and/or rotator cuff tears.141 Shoulders treated with BMC noted a statistically significant different in NPS of 44% reduction in pain when the minimum important difference is defined as 30%, with functional improvement and pain reduction that started at one month post treatment and was noted to be sustained for up to two years.141

No serious adverse events were reported after the procedures.141 PRP vs Stem cells for treatment The public often struggles with which type of intervention to consider. The options are vast and poorly understood by most, thus, the best way to describe the difference is with a construction site analogy. Stem cells are known as the general contractor coordinating the repair job, and if needed can turn into “brick and mortar” cells as well. PRP provides the supplies needed to do the job. The general consensus is that PRP is better for mild arthritis and partial ligament tears and stem cells is better for treating more severe arthritis and bigger tendon tears.132,142 Controversy remains regarding exact recommendations and research providing direct comparison between prolotherapy, PRP and stem cells, however preliminary studies are leaning towards the consensus above, and further randomized controlled, multisite studies are needed to better stratify pathology to specific treatment required. The following orthobiologic procedure to be discussed is culture-expanded stem cells which are currently not legal in the United states, however it is an important technique to discuss as it is the next step of treatment for potential enhancement of more significant healing than existing treatments. As it has been shown that higher concentration of MSCs can lead to greater reduction in pain and promote proliferation of cartilage for tissue healing.143,144 Culture Expanded MSCs Clinical Research Culture-expanded MSCs are MSCs that are plated on plastic and grown for weeks at a time to multiply the number of stem cells yielded and increase the TNC for better healing potential and pain relief, as stated above. This design is currently illegal in the United States due to the regulation of section 351 of the Public Service Act (42 U.S.C. 262) as it is considered “more-than-manipulated” cellular therapy.142 Centeno et al. studied six patients who received injections of adult autologous culture expanded MSCs in their thumb CMC joints. Preoperative radiographic reading demonstrated two patients with Grade 2 OA (obvious arthrosis), and four patients with Grade 3 OA

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(destroyed joint) of the first CMC.145,146 The authors concluded that the injection of culture-expanded MSCs with platelet-derived growth factors into first CMC joint of the hand was associated with positive outcomes similar-to those reported with arthroscopic hemitrapeziectomy with tendon interposition.147 However, this was only a case series and further studies with larger sample sizes and randomization is necessary for direct inference on whether cultureexpanded stem cells can replace surgical options.

alive similar-to a sick patient on life support, versus a cell that is alive similar to an individual who is active and running or working out. In short, viability testing does not measure whether the cell functions. Accordingly, percentage of viability can be a misleading number, and due to the manufacturing process of amniotic products as demonstrated in Figure 5, it is speculated that the cells are essentially nonfunctional and not living by the time an injection occurs into the patient.

Centeno et al published on the treatment of lumbar degenerative disc disease of culture-expanded mesenchymal stem cells into the discs of the lumbar spine as a prospective pilot study of 33 patients for up to six years. The study demonstrated that patients had improvement in pain from three months to six years, along with SANE improvement of 60% and 20 of 33 patients underwent post-treatment MRI and 85% had a reduction of disc bulge of 23%, without any significant adverse events.148 Prior to this study in 2010, Centeno et al tested the safety and feasibility of culture-expanded MSCs in the spine and demonstrated no tumorgenicity and no significant adverse events.149

The process of making an amniotic product is not as pure as taking it straight from the umbilical cord then transporting it to the lab for processing and then injecting it into the patient. The process that actually occurs is demonstrated in Figure 5, and when the baby is born the cord blood is taken into freezer storage and later gets transported into the lab for processing and packaging which is then cryopreserved, until it is sold to the clinic. When ready to be used, the product is flash warmed to room temperature very quickly and gets injected into the patient. The cells that were viable at the lab processing phase have gone through such a drastic change during the distinct process of flash warming additional cells may lose viability (especially those that were barely hanging on to begin with). Therefore, by the time the patient receives the injectate the cord blood that was taken originally is likely no longer viable living tissue.

Allogeneic (Amniotic) Products The drive behind the production of allogeneic products is to create a substance that can be “shelf-stable” and can provide benefit without subjecting the patient to the harvesting process of autologous stem cells. However, these allogenic products do contain growth factors, interleukins, and hyaluronic acid,150,151 which is an important point as there could be some utility in these products to help stimulate healing via other growth factors that are present in amniotic products and not in PRP. Therefore, using allogenic products as an adjunct therapy to autologous therapy is a much more promising option than amniotic products in isolation. What do amniotic or cord blood product viability numbers really mean? Viability testing is performed on products as a snapshot to discern how many cells are “alive” but does not factor in the health or vitality of the live or viable cells. Therefore, no matter if the cells are barely

Unpublished data courtesy of Centeno-Schultz Clinic demonstrate the lack of living stem cells via direct comparison of amniotic products versus older adult bone marrow stem cells in Figure 6 below. Also, a veterinary research scientist from Cornell University conducted independent research and

Figure 5. The process that amniotic products go through prior to injection.

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Figure 6. Assessment of colony forming units (CFU-F, aka, MSC colonies) which are the purple dots on the right, and absent on the left. The left side demonstrates the absence of nucleated cells. TNCC = total nucleated cell count. Used with permission from Centeno-Schultz Clinic.

concluded that out of 11 amnion products currently on the market that were tested, no living cells and low growth factor levels were noted in all products. She concluded in her talk at the AMSSM Sports Medcast and BMJ talk medicine Episode #360 with, “The amnion field is the wild west right now”.152 Other studies have demonstrated similar results. Secco et al. examined 10 matched umbilical cord and amniotic cord samples, and the authors were only able to culture out MSCs from one (10% recovery) noted from umbilical cord blood.153 Sibov et al. plated 118 umbilical cord blood units with only 11 containing MSCs (~10% recovery)154 and finally, Divya et al. plated 45 umbilical cord blood samples, nine of which generated MSCs (20% recovery), however the timing for growth in culture was approximately 2-3 weeks.155 Are these products approved by the FDA? Comparisons between donor tissue products and PRP There are two pathways for FDA approval of donor tissues that are designated sections through the Public Health Service Act (PHSA) are: 1) 361 registration that is largely unregulated and 2) 351 cellular drug approval142 and uses these two sections for interventional orthobiologic products for regulating biologics. Current amniotic products on the market have

only a 361 registration which requires no clinical trials or data. The 361-registration process involves only a check box form that is performed online. However, when companies claim to have living cells this makes the products a drug and many of these companies are riding the line between an online registration which is 361 versus a 351 which includes obtaining grants and funding for research and Stage 1, 2, and 3 clinical trials that can take up to 5-10 years for approval. Many of the companies are likely selling dead umbilical cord stem cells but discuss the research on their websites from a completely different perspective, claiming live culture-expanded umbilical cord stem cells, which is what is known as the classic “bait and switch”. Based on an internal research assessment from the Centeno-Schultz clinic, what the amniotic products do have is a variety of growth factors, however when the growth factors in LiveyonPure and StemVive were analyzed in comparison to a weak PRP of approximately two times more concentrated than platelet content in whole blood, and the results are displayed in Figures 7-11. Transforming Growth Factor (TGF-beta) is a good growth factor that should be present for positive results with biologic therapy. As shown in Figure 7, 2x PRP demonstrated superior density over both amniotic products.

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Figure 7. Transforming Growth Factor (TGF-beta) demonstrated higher amounts in a weak PRP formulation than in two amniotic products: StemVive and Liveyon Pure. Used with permission from the Centeno-Schultz Clinic.

Figure 9. Tissue Inhibitor of MetalloProteinases (TIMP) 1 in blue and 2 in orange are noted to be highest in StemVive> PRP2x >Liveyon Pure. Used with permission from the Centeno-Schultz Clinic.

or LiveyonPURE. However, as noted above in a traditional 7x-14x PRP the levels could be higher than in the weak PRP solution as displayed from internal data from the Centeno-Schultz clinic in Figure 9.

Figure 8. Vascular Endothelial Growth Factor (VEGF) higher contents in Liveyon Pure > PRP 2x > StemVive. Used with permission from the Centeno-Schultz Clinic.

Vascular endothelial growth factory (VEGF) is important for helping develop new blood vessels. As shown in Figure 8, internal data from the Centeno-Schultz clinic demonstrated that weak PRP (2x concentration) has a lower concentration of VEGF as compared to LiveyonPURE, however this low of a concentration would not be used therapeutically. However, using a traditional 7x-14x concentration (moderate strength PRP) could demonstrate greater concentration of VEGF. Tissue Inhibitor of MetalloProteinases (TIMP) is an anti-breakdown cytokine that may help protect joints against OA. The internal data demonstrated that StemVive had higher concentrations than weak PRP

Interleukin-8 (IL-8) on the other hand is a cytokine that is potentially negative to healing, as it can attract white blood cells and increase inflammation in an area. To give a clinical example, the serum blood levels of IL-8 in a knee arthritis patient are generally lower than 10pg/mL, however in this study the composition of IL8 in the internal data demonstrated that LiveyonPure was almost 300 and in Stemvive was more than 900 as displayed in Figure 10 (internal data from the Centeno-Schultz clinic). This concentration could indicate increased inflammation without promoting the healing cascade. There is an epigenetic study by Takahashi et al. that correlated increased IL-8 to the progression of OA due to inflammation and reports IL-8 as a possible target for decreasing inflammation by modulating expression.156 Basic Fibroblast Growth Factor (bFGF) is a good growth factor that promotes the growth of tendon cells, the internal data from the Centeno-Schultz clinic demonstrated that the higher concentrations in some solutions could explain why some providers are noting positive results with tendon type injuries such as rotator cuff tears. As noted in Figure 11, bFGF was highest in StemVive and much lower in the weak PRP and LiveyonPure samples.

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Figure 10. Interleukin-8 (IL-8), an inďŹ&#x201A;ammatory cytokine, ideally would need to be low to nonexistent, and StemVive had the most followed by LiveyonPure, then Weak PRP. Used with permission from the Centeno-Schultz Clinic.

Figure 11. bFGF, a positive growth factor for tendon healing, StemVive had the greatest content with Weak PRP and Liveyon Pure demonstrating minimal content. Used with permission from the Centeno-Schultz Clinic.

Other internal Centeno-Schultz clinic data has tested two additional birth tissue products and found that StemVive produced more bFGF than the other two products, which is impressive however clinical translation of these findings is unknown to date, and only speculative benefit may be seen in tendinopathies. Allogeneic products in summary Growth factors are present in widely variant levels in various preparations used in orthobiologic interventions, as demonstrated in the figures above. Which of those could prove beneficial in treatment

of stubborn tendons due to bFGF levels being higher is yet unknown due to the lack of research comparing amniotic products to weak PRP in the treatment of tendons. The mislabeling of amniotic stem cells is what brings about much debate, however the proposition of calling them amniotic growth factors may be a new discussion. To date, the indications for amniotic products are not clear, and the risk for possible donor/recipient mismatch and cell dose are amplified with multiple transfusion exposures (aka, multiple injections) that might sensitize the recipient to donor alloantigens and cause the recipient to have an immune response against the product.157 This graft versus host reaction could prove much more harmful than the benefit of improving tendinopathy, however more studies are needed. CURRENT REHABILITATION CONSIDERATIONS IN REGENERATIVE ORTHOPEDIC MEDICINE Research on rehabilitation protocols for regenerative procedures is lacking. To date, there are no standard protocols for rehabilitation after interventional orthobiologic procedures in humans. However, animal studies exist that corroborate the mechanotransduction model for promotion of healing. In the equine population undergoing PRP injections, it has been shown that controlled gradual return to activity is the best course of action, with restricted exercise in the acute and subacute phases of tendon and ligament healing being paramount.158 McKay et al. recently published proposed regenerative rehabilitation guidelines and proposed protocols for the treatment of knee osteoarthritis.159 They suggest that moderate physical exercise decreases the progression to severe knee osteoarthritis by inducing a protective effect against cartilage degradation.15,159 A common issue in patients with knee osteoarthritis is weakness of the quadriceps which has also been correlated with ligamentous instability and therefore inactivity as a result.159,160 There are patients that have weak muscles and have ligamentous laxity and those with strong muscles but continue to have ligamentous laxity.159 In those patients that have weak muscles, muscle strengthening is beneficial, and in those with strong muscles, knee stabilizing exercises are necessary.160 A combination

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of interventions targeting restoration of mobility, strength, stability, proprioception and neuromuscular control is recommended in post orthbiologic rehabilitation due to the role rehabilitation plays in chondrocyte stimulation and role in improving function of patients with knee OA159 after orthobiologics. General rehabilitation guidelines exist for PRP and stem cell therapy which involve four phases of therapy. The following example applies the four phase approach to the rehabilitation of a patient with various joint pathologies after PRP48 which can be extrapolated to stem cell therapies however typically with a longer time course of action to allow for healing. See descriptions in Table 1 and a graphic display in Figure 12.48

A suggested rehabilitation protocol following platelet-rich plasma for treatment of tendons is slightly different to the OA model above, this protocol encompasses three phases versus four phases as noted above in the protocol for treatment of joints.55

Figure 12. General phases of healing summarizing the regenerative rehabilitation process.

Table 1. Descriptions of the four phases of rehabilitation, in general after a orthobiologic procedure.

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Table 2. Descriptions of the three phases of rehabilitation, in tendinopathy after an orthobiologic procedure.

See descriptions of the phases in Table 2, along with a summary of the phases in Figure 13.55 Currently, there is no consensus on rehabilitation after PRP injections but as described above, the notion of gradually increasing the load and activity as tolerated may augment the tissue healing cascade,55 along with gauging the intensity of workouts based on pain level to keep it at a minimum of 2/10 to avoid further soft tissue injury. Therapeutic modalities that can help augment recovery after regenerative injections: Blood Flow Restriction

Figure 13. Three proposed phases of rehabilitation after PRP injection for tendinopathy healing.

Blood flow restriction (BFR) is a rapidly growing therapeutic modality for helping apply load through the muscles in areas that are unable to tolerate the addition of enough load to achieve a strengthening stimulus either due to muscular inhibition or pain. It is currently being used in several post-operative conditions such as after ACL reconstructions. BFR utilizes an applied tourniquet to the extremity of the injured patient, which partially restricts the blood

flow to the limb, as the patient undergoes mobilization or exercise.159,161 Takarada et al. demonstrated that with BFR, only the muscles whose bloodflow was restricted (due to the BFR) demonstrated a significant increase in muscle cross sectional area and thigh strength.162 The exact mechanism of this phenomenon is not readily understood, however the proposed mechanisms include increased selective fiber

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type recruitment, alterations in metabolic accumulation, activation of muscle protein synthesis, and the induction of cell swelling.163 There is also a proposed metabolite theory in which the increase in metabolic byproducts from anaerobic metabolism such as lactate and hydrogen. In BFR, the “burn” (release of byproducts of hydrogen and lactate) in the muscle that is felt during treatment releases growth factors and helps in hypertrophy and healing of the muscle.163 Which was shown in discussion about the healing cascade, that stimulating muscles improves the satellite cell population contributing to healing. In the early stages of healing the goal is to mitigate atrophy and promote healing, therefore with BFR this can be achieved with isometric-type exercises without ranging an already inflamed and otherwise painful joint. More studies are still needed to provide any direct correlation with BFR in patients that have undergone orthobiologic procedures. At this time, the theoretical perspective of BFR is compelling however will need to have more studies with patients that have undergone orthobiologic type procedures. Whole Body Vibration Whole body vibration (WBV) is an intervention that involves the use of a vibrating platform that changes amplitudes while the patient is either positioned statically (supine, sitting, kneeling, or standing) or performing a dynamic movement.159,164 The purpose of the vibratory stimulus is to induce reflex motor contractions which may assist in improving muscle recruitment and proprioception. In the elderly with knee OA the induction of isometric, concentric, and eccentric contractions of the hip, knee extensor muscle groups and the plantar flexors assists in improving the control and execution of functional movements such as those required for static and dynamic balance and gait performance.159,164 This modality has been shown to possibly slow the progression of cartilage loss due to the modulation of skeletal tissue, increasing oscillation of chondrocytes, and potentially augmenting thickness of the chondrocyte layer,159,165 therefore it has been suggested to be used in combination with the regenerative rehabilitation program for patients with knee OA who have been treated with orthobiologics. The theory behind whole body vibration as above is interesting, however no distinct research has been done to prove this in vivo.

CONCLUSIONS Prolotherapy may work well in “tilling the soil” for other interventional orthobiologic techniques in order to kick start the inflammatory cascade to promote healing. Prolotherapy is used as either a first line treatment for mild instability of ligaments and/ or tendons, however it will produce more collagen that is not as strong as the original collagen. PRP is a treatment adjunct for mild to moderate tendinopathy and ligamentous laxity cases. PRP seems to work best for mild arthritis by providing growth factors that help conjugation of collagen back to Type I collagen, providing collagen that is stronger and more robust than the injured structure. Finally, MSCs are used in more severe or refractory cases of tendon and ligamentous injury as well as in treatment of moderate to severe osteoarthritis that can be coupled with bone augmentation treatments in disease states that are more advanced such as avascular necrosis, bone marrow edema, or cystic changes. Although more aggressive surgeries may be warranted in refractory or severe cases where orthobiologics did not help; having an orthobiologic option coupled with targeted rehabilitation protocols would be optimal prior to moving onto surgery. Interventional orthobiologics as a field, is in its infancy and has a long way to go to develop consensus regarding the types of procedures to utilize for various patients as well as the recommendations for physical therapy management after procedures. Such recommendations need to be formulated based on patient specifics and correlated with the mechanobiology of the body segment or tissue being treated. Being familiar with the stages of healing as they relate to orthobiologics is crucial to understanding the limitations of the patient at certain timepoints in healing and wisely choosing physical therapy interventions. The 30,000-foot view is that rehabilitation post-orthopedic surgical procedures directs more emphasis on returning a patient back to the level prior to the surgery, with the hope of gaining additional function. The goal of regenerative rehabilitation is not only to restore a patient back to the level of function prior to the injection (which is not as debilitating as surgery), but also to restore the biomechanical influences that contributed to the injury by focusing on the joint or injured area as a

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part of a whole. The goal of interventional orthobiologics is not only to heal damaged to tissue but to rectify the kinetics of the surrounding structure in order to optimize the body’s function as a whole. Adjunctive modalities for regenerative rehabilitation such as blood flow restriction and whole-body vibration with the goal of strengthening an injured peripheral segment rapidly in order to maintain or improve muscle mass and enhance proprioception are currently being explored. These two adjunctive interventions could facilitate the continued direction towards movement as the best rehabilitation alternative and the avoidance of immobilization and bedrest. To move orthopedics and sports medicine away from the current emphasis on pain management, the use of NSAIDs, steroid injections and rest, towards progressive movement, combined with strengthening is desired. A combined rehabilitative approach to improving biomechanics along with utilizing regenerative injections of prolotherapy, PRP and/or MSCs to induce healing and promote stability may assist in keeping joints, ligaments, tendons and muscles healthy and stronger as we age or prevent future injury in the younger population. REFERENCES 1. Regenerative Rehabilitation. Secondary Regenerative Rehabilitation 11/7/2017 2017. http://www.apta.org/ RegenerativeRehab/. 2. Ng JL, Kersh ME, Kilbreath S, Knothe Tate M. Establishing the basis for mechanobiology-based physical therapy protocols to potentiate cellular healing and tissue regeneration. Front Physiol. 2017;8:303 doi: 10.3389/fphys.2017.00303[published Online First: Epub Date]|. 3. Thompson WR, Scott A, Loghmani MT, Ward SR, Warden SJ. Understanding mechanobiology: Physical therapists as a force in mechanotherapy and musculoskeletal regenerative rehabilitation. Phys Ther. 2016;96(4):560-9. 4. Wang Y, McNamara LM, Schafﬂer MB, Weinbaum S. A model for the role of integrins in ﬂow induced mechanotransduction in osteocytes. Proc Natl Acad Sci.2007;104(40):15941-6. 5. Head PL. Rehabilitation considerations in regenerative medicine. Phys Med Rehabil Clin N Am. 2016;27(4):1043-54. 6. Liu SH, Yang RS, al-Shaikh R, Lane JM. Collagen in tendon, ligament, and bone healing. A current review. Clin Orthop Relat Res. 1995;318:265-78.

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118. Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for deﬁning multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315-7. 119. Hernigou P, Homma Y, Flouzat-Lachaniette CH, Poignard A, Chevallier N, Rouard H. Cancer risk is not increased in patients treated for orthopaedic diseases with autologous bone marrow cell concentrate. J Bone Joint Surg Am. 2013;95(24):2215-21. 120. Centeno CJ, Al-Sayegh H, Freeman MD, Smith J, Murrell WD, Bubnov R. A multi-center analysis of adverse events among two thousand, three hundred and seventy two adult patients undergoing adult autologous stem cell therapy for orthopaedic conditions. Int Orthop. 2016;40(8):1755-65. 121. McDaniel JS, Antebi B, Pilia M, et al. Quantitative assessment of optimal bone marrow site for the isolation of porcine mesenchymal stem cells. Stem Cells Int. 2017;2017:1836960 doi: 10.1155/2017/1836960[published Online First: Epub Date]|. 122. Hernigou P, Homma Y, Flouzat Lachaniette CH, et al. Beneﬁts of small volume and small syringe for bone marrow aspirations of mesenchymal stem cells. Int Orthop. 2013;37(11):2279-87. 123. Hernigou P, Poignard A, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for

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nonunions. Inﬂuence of the number and concentration of progenitor cells. J Bone Joint Surg Am. 2005;87(7):1430-7. 124. Hernigou P, Poignard A, Zilber S, Rouard H. Cell therapy of hip osteonecrosis with autologous bone marrow grafting. Indian J Orthop. 2009;43(1):40-5. 125. Centeno CJ, Al-Sayegh H, Bashir J, Goodyear S, Freeman MD. A dose response analysis of a speciﬁc bone marrow concentrate treatment protocol for knee osteoarthritis. BMC Musculoskelet Disord. 2015;16:258 doi: 10.1186/s12891-015-0714z[published Online First: Epub Date]|. 126. Jo CH, Chai JW, Jeong EC, et al. Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: A 2-year follow-up study. Am J Sports Med. 2017;45(12): 2774-83. 127. Li CY, Wu XY, Tong JB, et al. Comparative analysis of human mesenchymal stem cells from bone marrow and adipose tissue under xeno-free conditions for cell therapy. Stem Cell Res Ther. 2015;6:55 doi: 10.1186/s13287-015-0066-5[published Online First: Epub Date]|.

complications and mortality following total knee arthroplasty: incidence and risk factors among a national sample of 15,321 patients. J Bone Joint Surg Am. 2014;96(1):20-6. 135. Grosu I, Lavand’homme P, Thienpont E. Pain after knee arthroplasty: an unresolved issue. Knee Surg Sports Traumatol Arthrosc. 2014;22(8):1744-58. 136. Rodriguez-Fontan F, Piuzzi NS, Kraeutler MJ, Pascual-Garrido C. Early clinical outcomes of intra-articular injections of bone marrow aspirate concentrate for the treatment of early osteoarthritis of the hip and knee: A cohort study. Phys Med Rehabil. 2018;10(12):1353-59. 137. Shapiro SA, Kazmerchak SE, Heckman MG, Zubair AC, O’Connor MI. A prospective, single-blind, placebo-controlled trial of bone marrow aspirate concentrate for knee osteoarthritis. Am J Sports Med. 2017;45(1):82-90. 138. Centeno CJ, Pitts J, Al-Sayegh H, Freeman MD. Anterior cruciate ligament tears treated with percutaneous injection of autologous bone marrow nucleated cells: a case series. J Pain Res 2015;8: 437-47.

128. Mohamed-Ahmed S, Fristad I, Lie SA, et al. Adiposederived and bone marrow mesenchymal stem cells: a donor-matched comparison. Stem Cell Res Ther. 2018;9(1):168 doi: 10.1186/s13287-018-09141[published Online First: Epub Date]|.

139. Hong SH, Choi JY, Lee GK, Choi JA, Chung HW, Kang HS. Grading of anterior cruciate ligament injury. Diagnostic efﬁcacy of oblique coronal magnetic resonance imaging of the knee. J Comput Assist Tomogr. 2003;27(5):814-9.

129. Koga H, Muneta T, Nagase T, et al. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res. 2008;333(2):207-15.

140. Hsu WH, Peng KT, Lai LJ, Hung CH, Chang PJ. Cellular senescence occurring in the rabbit medial collateral ligament during healing. J Orthop Res. 2013;31(1):81-90.

130. CDC. National and state medical expenditures and lost earnings attributable to arthritis and other rheumatic conditions - United States. MMWR Morb Mortal Wkly Rep. 2003(56):4-7. 131. CDC. Prevalence of doctor-diagnosed arthritis and arthritis-attributable activity limitation - United States, 2010-2012. MMWR Morb Mortal Wkly Rep. 2013;44(62):869-73. 132. Centeno C, Sheinkop M, Dodson E, et al. A speciﬁc protocol of autologous bone marrow concentrate and platelet products versus exercise therapy for symptomatic knee osteoarthritis: a randomized controlled trial with 2 year follow-up. J Transl Med. 2018;16(1):355 doi: 10.1186/s12967-018-17368[published Online First: Epub Date]|. 133. Vaishya R, Pariyo GB, Agarwal AK, Vijay V. Nonoperative management of osteoarthritis of the knee joint. J Clin Orthop Trauma. 2016;7(3):170-6. 134. Belmont PJ, Jr., Goodman GP, Waterman BR, Bader JO, Schoenfeld AJ. Thirty-day postoperative

141. Centeno CJ, Al-Sayegh H, Bashir J, Goodyear S, Freeman MD. A prospective multi-site registry study of a speciﬁc protocol of autologous bone marrow concentrate for the treatment of shoulder rotator cuff tears and osteoarthritis. J Pain Res. 2015;8:269-76. 142. Administration UDoHaHSFaD. Regulatory considerations for human cells, tissues, and cellular and tissue-based products: Minimal manipulation and homologous use: Guidance of industry and food and drug administration staff, 2017. https:// www.fda.gov/media/109176/download. 143. Pettine KA, Suzuki RK, Sand TT, Murphy MB. Autologous bone marrow concentrate intradiscal injection for the treatment of degenerative disc disease with three-year follow-up. Int Orthop. 2017;41(10):2097-103. 144. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143-7.

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145. Centeno CJ, Freeman MD. Percutaneous injection of autologous, culture-expanded mesenchymal stem cells into carpometacarpal hand joints: a case series with an untreated comparison group. Wien Med Wochenschr. 2014;164(5-6):83-7. 146. Sodha S, Ring D, Zurakowski D, Jupiter JB. Prevalence of osteoarthrosis of the trapeziometacarpal joint. J Bone Joint Surg Am. 2005;87(12):2614-8. 147. Buterbaugh GA, Brown TR, Horn PC. Ulnar-sided wrist pain in athletes. Clin Sports Med 1998;17(3):567-83. 148. Centeno C, Markle J, Dodson E, et al. Treatment of lumbar degenerative disc disease-associated radicular pain with culture-expanded autologous mesenchymal stem cells: a pilot study on safety and efﬁcacy. J Transl Med. 2017;15(1):197 doi: 10.1186/s12967-017-1300-y[published Online First: Epub Date]|. 149. Centeno CJ, Schultz JR, Cheever M, Robinson B, Freeman M, Marasco W. Safety and complications reporting on the re-implantation of cultureexpanded mesenchymal stem cells using autologous platelet lysate technique. Curr Stem Cell Res Ther. 2010;5(1):81-93. 150. Ellis I, Banyard J, Schor SL. Differential response of fetal and adult ﬁbroblasts to cytokines: cell migration and hyaluronan synthesis. Development. 1997;124(8):1593-600. 151. Willett NJ, Thote T, Lin AS, et al. Intra-articular injection of micronized dehydrated human amnion/chorion membrane attenuates osteoarthritis development. Arthritis Res Ther. 2014;16(1):R47 doi: 10.1186/ar4476[published Online First: Epub Date]|. 152. Fortier L. AMSSM Sports Medcast and BMJ Talk Medicine. In: McFadden D, ed. Episode #360: Regenerative Medicine: Game Changing Innovation of Next Big Flop? 360 ed, 2019. 153. Secco M, Zucconi E, Vieira NM, et al. Multipotent stem cells from umbilical cord: cord is richer than blood! Stem Cells. 2008;26(1):146-50. 154. Sibov TT, Severino P, Marti LC, et al. Mesenchymal stem cells from umbilical cord blood: parameters for isolation, characterization and adipogenic differentiation. Cytotechnology. 2012;64(5):511-21. 155. Divya MS, Roshin GE, Divya TS, et al. Umbilical cord blood-derived mesenchymal stem cells consist of a unique population of progenitors co-expressing mesenchymal stem cell and neuronal markers capable of instantaneous neuronal differentiation. Stem Cell Res Ther. 2012;3(6):57 doi: 10.1186/ scrt148[published Online First: Epub Date]|.

156. Takahashi A, de Andres MC, Hashimoto K, Itoi E, Oreffo RO. Epigenetic regulation of interleukin-8, an inflammatory chemokine, in osteoarthritis. Osteoarthritis Cartilage. 2015;23(11):1946-54. 157. Stavropoulos-Giokas C, Dinou A, Papassavas A. The role of HLA in cord blood transplantation. Bone Marrow Res. 2012;2012:485160 doi: 10.1155/2012/485160[published Online First: Epub Date]|. 158. Ortved KF. Regenerative medicine and rehabilitation for tendinous and ligamentous injuries in sport horses. Vet Clin North Am Equine Pract. 2018;34(2):359-73. 159. McKay J, Frantzen K, Vercruyssen N, et al. Rehabilitation following regenerative medicine treatment for knee osteoarthritis-current concept review. J Clin Orthop Trauma. 2019;10(1):59-66. 160. Knoop J, Steultjens MP, Roorda LD, et al. Improvement in upper leg muscle strength underlies beneficial effects of exercise therapy in knee osteoarthritis: secondary analysis from a randomised controlled trial. Physiotherapy. 2015;101(2):171-7. 161. Loenneke JP, Wilson JM, Wilson GJ, Pujol TJ, Bemben MG. Potential safety issues with blood flow restriction training. Scand J Med Sci Sports. 2011;21(4):510-8. 162. Takarada Y, Tsuruta T, Ishii N. Cooperative effects of exercise and occlusive stimuli on muscular function in low-intensity resistance exercise with moderate vascular occlusion. Jpn J Physiol. 2004;54(6):585-92. 163. Hylden C, Burns T, Stinner D, Owens J. Blood flow restriction rehabilitation for extremity weakness: a case series. J Spec Oper Med. 2015;15(1):50-6. 164. Simao AP, Avelar NC, Tossige-Gomes R, et al. Functional performance and inflammatory cytokines after squat exercises and whole-body vibration in elderly individuals with knee osteoarthritis. Arch Phys Med Rehabil. 2012;93(10):1692-700. 165. Wang P, Yang L, Liu C, et al. Effects of Whole Body Vibration Exercise associated with Quadriceps Resistance Exercise on functioning and quality of life in patients with knee osteoarthritis: a randomized controlled trial. Clin Rehabil 2016;30(11):1074-87.

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IJSPT

CLINICAL SUGGESTION

CRITERIA-BASED RETURN TO SPRINTING PROGRESSION FOLLOWING LOWER EXTREMITY INJURY Daniel Lorenz, DPT, PT, ATC, LAT, CSCS1 Steve Domzalski, PT, SCS, ATC, CSCS2

ABSTRACT In the terminal phases of athletic rehabilitation, transitioning back to sport is a critical aspect to prepare an athlete for return to full participation. Numerous interval sport programs have been published in the literature and return to sports guidelines and criteria-based progressions for returning to sport have been published, but no such protocol exists for returning to the task of sprinting. Any field or court athlete must be able to sprint as part of his/her sport demands. Because of the absence of a specific progression, sports rehabilitation professionals lack knowledge about objective criteria to progress to sprinting as well as a progressive program to do so. Given that sports rehabilitation professionals have limited visits to complete rehabilitation or their athletes have limited financial resources to do so, it is imperative that a structured, criteria-based progression be available. The purpose of this clinical suggestion is to provide a criteria-based return to sprinting progression. Level of Evidence: 5 Keywords: Criteria-based progression, Interval sports program, return to sport, sprinting

Lawrence Memorial Hospital/OrthoKansas, Lawrence, KS, USA 2 Wayne StateÂ University, Detroit, MI, USA The authors have no conďŹ&#x201A;icts of interest to disclose.

CORRESPONDING AUTHOR Daniel Lorenz, DPT, PT, ATC, LAT, CSCS, Director of Sports Medicine, Lawrence Memorial Hospital/OrthoKansas 1112 W. 6th St. Suite 124 Lawrence, KS 66044 E-mail: danielslorenz@gmail.com 815-370-5337

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 326 DOI: 10.26603/ijspt20200326

THE PROBLEM Return to running and eventually sprinting is an objective in the terminal phases of rehabilitation after every lower extremity injury, especially for field and court sport athletes. Athletes in anaerobic field and court sports that require interval sprinting should reach top speed in a controlled, predictable environment prior to engaging in competition. Given that prior research has shown that up to 19% of athletes do not return to sport for fear of re-injury after ACL reconstruction,1 fostering limb confidence by successfully reaching maximum sprint speed may help facilitate improvements in the ability to return to sport. Criteria-based progressions have been published previously to progress athletes through a rehabilitation program,2-9 but there remains little agreement and consistency in the literature about when the appropriate time is to begin jogging,7 and when an athlete does begin, what specific distances or work:rest ratios should be completed. There are several papers that have highlighted work: rest ratios in a number of sports,10-15 and technological advances have allowed the rehabilitation professional to use Global Positioning Systems (GPS) to determine distances athletes run during completion.9,15 Furthermore, numerous interval sport programs have been published in the literature,16-19 but no such protocol exists for returning to actual sprinting. There is little guidance for the rehabilitation professional to utilize when returning an athlete back to high speed running (sprinting). Given that many sports rehabilitation professionals have athletes with reduced or minimal visits in the terminal phases of rehabilitation and that, to the author’s knowledge, no return to sprinting progression has been published to date, a structured program for both the rehabilitation professional and the athlete is necessary. The purpose of this clinical suggestion is to provide a criteria-based return to sprinting progression. In circumstances where an athlete will be performing more self-guided workouts due to lack of financial resources, insurance limitations, or any inability to continue supervised rehabilitation, the program will help minimize the guesswork that often transpires in the terminal phases of rehabilitation. THE SOLUTION The first step in considering readiness to begin the return to sprinting progression is to ensure a

screening of other potential lower extremity impairments has been performed and any limitations or deficits have been addressed. Secondly, physician clearance should be obtained. Prior to initiation of the return to sprint progression, the author suggests athletes complete a four-week return to jogging program. For many patients, it might be reasonable to expect readiness to return to running around the 8th–16th postoperative weeks,7 provided they have physician clearance, meet testing criteria, and have no effusion or pain. While a number of these return to running progressions are available online, there have been some published in the literature.20,21 Essentially, all of these programs involve walk: jog intervals that progressively reduce time walking and increase time jogging, most of them up to about thirty minutes of jogging. The authors are not aware of any research comparing these programs to determine the ideal time frame with associated walk:jog ratios. The purpose completing a walk:jog interval program is to build an aerobic base to prepare for more intense runs in the return to sprinting program. A previous review has proposed guidelines to begin return to running and it is suggested the clinician consider strength and performance-based criteria including hamstring and quadriceps limb symmetry index (LSI) and quadriceps LSI>70% evaluated by isometric assessments and hop test LSI>70%. The addition of a single-leg squat or step-up assessment performed without increase in knee valgus may also be considered. Return to running decision-making should be individualized for each athlete/patient.7 It is advised to perform a general warm-up to increase blood flow, which can consist of a light jog, cycling, elliptical, or calisthenics for 5-10 minutes or until the athlete breaks a sweat. Following the general warm-up, a more specific/dynamic warm-up should take place consisting of activities including but not limited to walking lunges, “toy soldiers”, skipping, bounding, high knees, “butt kickers”, ankling, and other similar activities to potentiate more explosive activities. The return to sprinting program should be performed on alternating days. Progression/regression should be based on soreness and effusion,8 as well as the athlete’s ability to complete all runs in the specified work:ratio. If the athlete is unable to complete the specified runs due to fatigue, the step

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should be repeated without progression until they are able to do so. If an athlete completes the prescribed runs in the specified work:rest ratio but they have yet to achieve criteria to advance stages, the authors suggest repeating the runs at the same intensity, but shorter work:rest ratio. For example, if the athlete has completed all Stage 2 runs but has yet to achieve strength and hop testing criteria to advance to Stage 3, start back over at Step 1 and do the same runs in a 1:4 or 1:3 work:rest ratio. The rationale for this is that the athlete will have a greater overall fitness as the same volume was achieved but in less time. There are a few potential limitations of this program that are worth noting. Tolerance of running volume will likely be athlete-specific. The program outlined may have too much volume and can be adjusted accordingly. For example, the volume may be adjusted down for an offensive tackle in American football, but may be increased for a soccer athlete. Similarly, distance of runs can be decreased based on sport and position. An American football wide receiver or defensive back may have run distances that cover >30 yards, while a defensive lineman may have more runs that cover <30 yards. The sports rehabilitation professional should ensure that the volumes are systematic and progressive and allow the athlete to match work:rest ratios prescribed. The objective is to build tolerance to sprinting and to achieve top speeds with specific rest times to replicate sport demands. Secondly, the program does not involve any change of direction, nor any perceptual or decision-making tasks. Most anaerobic sports require cutting/change of direction at top speeds and in unpredictable environments. Clearly, these activities will need to be incorporated into a comprehensive rehabilitation/return to sport program. The return to sprinting program be completed at full speed before an athlete attempts achieves full speed in change of direction tasks as sprinting is a single plane activity and change of direction involves multiple planes. That being said, change of direction tasks at lower speeds can be completed concurrently with the return to sprinting progression. To build in more change of direction movement, the rehabilitation professional might consider performing the drills over the provided distances in the program, but put in cones for cutting tasks. During these later stages,

athletes will likely be returning to participation with team activities or individual drills. This program can be done after sport-specific drills are complete with team activities. Any explosive or power-based activities take priority over completion of this program, except for the final stage which is approaching or at maximum effort. Return to Sprint Progression: Stage 1 (Appendix A) Criteria to begin: Completion of a four week walk:jog program for 30 minutes, strength testing of quadriceps and hamstrings at least 70% of the uninvolved side, hop testing at least 70% of the uninvolved, no pain, no effusion. Objectives: Build work capacity for higher intensity runs, build overall fitness Athlete cue: “Run about 50% of your maximum effort” In Stage 1, the athlete begins building intensity during the runs. Rather than long-slow distance as in the return to jogging programs, the athlete is asked to keep a 1:3 work:rest ratio. The program says “untimed” in steps 1 and 2 to leave the athlete and rehabilitation professional the ability to adjust the program should the individual fitness levels not tolerate the demands of the work:rest ratio. Note that both volume of runs and overall distance increases as Stage 1 progresses to build anaerobic endurance due to specific work:rest ratios, rather than untimed runs. Distances are moderate to high. It is advised that the athlete achieve the runs with the work:rest ratio suggested to ensure appropriate fitness base for later phases. While the amount of runs may seem high, even at the peak distance, the athlete has not even run ¾ of a mile. Return to Sprinting Progression: Stage 2 Criteria to begin: Completion of Stage 1, all strength and functional testing 80-85% or better, full passive flexion restored. Objectives: Continue building sport-specific work:rest ratios, build repeated sprint ability. Athlete cues: “Don’t reach top gear, but go harder than you did in Stage 1,” or “Run about 75% of your maximum effort”

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Because intensity is increasing, rest periods will increase. The athlete should focus at this time on running technique. Full passive flexion of the knee is critical to allow the leg to complete the recovery cycle and to promote proper sprint mechanics. The rehabilitation professional can test this with the prone knee bending test.22 While the athlete is prone, the rehabilitation professional places one hand on the posterior pelvis and the other on the ankle. The knee is passively flexed to end range or when the athlete reports pain or discomfort. Symmetry in range of motion and soft tissue compliance should be symmetrical. While the rehabilitation professional can measure this with a goniometer, assessment of this involves more “feel” comparing side-to-side passive mobility. The effort for the rehabilitation professional to reach full passive flexion should feel the same as well as the resistance from the athlete’s knee and/or soft tissues. Volume and distance decreases significantly compared to Stage 1. Distances are more moderate and distances >60 yards will be emphasized less. Total yardage decreases as this stage progresses because intensity should be increasing and rest periods should be followed. Fatigue will likely become more a factor as intensity increases, so total distance is decreased. This phase also involves building repeated sprint ability (RSA). RSA describes the ability of an athlete to recover and maintain maximal effort during subsequent sprints, an attribute considered important to team sports. It is often trained and measured via high-intensity sprints, interspersed with brief recovery bouts (≤30 seconds). Most strength and conditioning coaches agree that for validity and correspondence to the actual sport, the RSA training session or testing protocol should resemble the work to rest ratio of the sport in question. Because of this, it is important that the athlete achieve prescribed repetitions with prescribed rest periods.23 Return to Sprinting Progression: Stage 3 Criteria to Begin: Completion of Stage 2, all strength and functional testing 90% or better. No effusion or pain. Objective: Achieve maximum effort, normal mechanics, improve limb confidence, prepare for sport-specific work: rest ratio

Athlete cue: “You should be very close to or at maximum effort” or “Run at 90-100% of your maximum effort” In this phase, maximum effort as well as maximum recovery should be practiced. While there are more runs than in Stage 2, the distance of each run is markedly less, most of which are <30 yards. These distances can of course be adjusted based on the athlete’s position or specific work:rest ratio in their sport. In Steps 1 and 2 of this stage, the rehabilitation professional might allow full subjective recovery between sprints if the athlete’s conditioning level cannot tolerate the work:rest ratios prescribed. If the athlete is not able to maintain the prescribed work:rest ratio in the final two steps, the program should stop for that workout as there clearly is a decline in maximum sprint performance and the quality of the session will be sacrificed. Instead, the rehabilitation professional can encourage a “finish” attitude by completing the remaining runs at a lower intensity, perform lower intensity runs from previous steps, or perform more sport-specific drills/activities. The athlete should be reminded that in this phase, they have to “train fast to be fast.” Once there is a decline, further attempts at running at maximum effort in this session will likely not be beneficial. Much like Stage 2 the volume of runs is relatively the same, but the total distance decreases as the stage progresses due to likely increase in sprinting intensity. DISCUSSION A specific progression for the rehabilitation professional in the terminal phases of rehabilitation to return an athlete to maximum effort sprinting has not been previously published, to the author’s knowledge. A progressive, structured program with specific distances as well as appropriate work:rest ratios helps take what is often guesswork out of the late stage rehabilitation programming. What is more, many rehabilitation professionals are forced to provide programming for self-guided sessions due to financial or insurance visit limitations. Therefore, a return to sprinting program is something the rehabilitation professional can provide to their athletes should more independent, unsupervised workouts be necessary.

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The rehabilitation continuum is a combination of science and art. There is so much variability and individualization of rehabilitation programs based on a number of factors including but not limited to injury history, sport, level of sport, residual impairments, and response to training. Providing a specific, criteria-based progression to return to sprinting is necessary to provide the rehabilitation professional and the athlete the ability to follow a structured program in order to help ensure safe return to sport. Given that recent literature has proposed lengthening the return to release to full sports participation after anterior cruciate ligament reconstruction specifically,9,24-33 the program suggested here will assist the sports rehabilitation professional in providing a structured, criteria-based progression. Furthermore, it should help the athlete progress back to activity while at the same time “buy time” to extend and enhance recovery. REFERENCES 1. Ardern CL, Webster KE, Taylor NF, Feller JA. Return to sport following anterior cruciate ligament reconstruction surgery: a systematic review and meta-analysis of the state of play. Br J Sports Med. 2011; 45: 596-606. 2. Bizzini M, Hancock D, Impellizzeri F. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: soccer. J Orthop Sports Phys Ther. 2012; 42(4): 304-12. 3. Waters E. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: basketball. J Orthop Sports Phys Ther. 2012; 42(4): 326-36. 4. Verstegen M, Falsone S, Orr R, Smith S. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: American football. J Orthop Sports Phys Ther. 2012; 42(4): 337-44. 5. Kokmeyer D, Wahoff M, Mymern M. Suggestions from the field for return to sports participation following anterior cruciate ligament reconstruction: alpine skiing. J Orthop Sports Phys Ther. 2012; 42(4): 313-25. 6. Wahoff M, Dischiavi S, Hodge J, Pharez JD. Rehabilitation after labral repair and femoroacetabular decompression: criteria-based rehabilitation progression through the return to sport phase. Int J Sports Phys Ther. 2014; 9(6): 813-26. 7. Rambaud AJM, Ardern CL, Thoreux P, et al. Criteria for return to running after anterior cruciate ligament

reconstruction: a scoping review. Br J Sports Med. 2018; 52(22): 1437-1444. 8. Adams D, Logerstedt DS, Hunter-Giordano A, Axe MJ, Snyder-Mackler L. Current concepts for anterior cruciate ligament reconstruction: a criterion-based rehabilitation progression. J Orthop Sports Phys Ther. 2012; 42(7): 601-614. 9. Grindem H, Snyder-Mackler L, Moksnes H, et al. Simple decision rules can reduce injury risk by 84% after ACL reconstruction: the Delaware-Oslo ACL cohort study. Br. J Sports Med. 2016; 50: 800-808. 10. Reilly, T., & Secher, N. Physiology of Sports: An Overview. In Reilly T, Secher N, Snell P, Williams Williams C, Eds. Physiology of Sports. London: E. & F.N. Spon; 1990: 465-485. 11. Bracko MR. On-ice performance characteristics of elite and non-elite women’s ice hockey players. J Strength Cond Res. 2001; 15(1): 42-7. 12. Noonan BC. Intragame blood-lactate values during ice hockey and their relationships to commonly used hockey testing protocol. J Strength Cond Res. 2010; 24(9): 2290-5. 13. Iosia MF, Bishop PA. Analysis of exercise-to-rest ratios during Division IA televised football competition. J Strength Cond Res. 2008; 22(2): 332-40. 14. Rhea MR, Hunter RL, Hunter TJ. Competition modeling of American football: observational data and implications for high school, collegiate, and professional player conditioning. J Strength Cond Res. 2006; 20(1): 58-61. 15. Bradley PS, Sheldon W, Wooster B, et al. Highintensity running in English FA Premier League soccer matches. J Sports Sci. 2009; 27(2): 159-68. 16. Myers NL, Sciascia AD, Kibler WB, Uhl TL. Volumebased interval training program for elite tennis players. Sports Health. 2016; 8(6): 536-540. 17. Reinold MM, Wilk KE, Reed J, et al. Interval sport programs: guidelines for baseball, tennis, golf. J Orthop Sports Phys Ther. 2002; 32(6): 293-298. 18. Hurd W, Hunter-Giordano A, Axe M, Snyder-Mackler L. Data-based interval hitting program for female college volleyball players. Sports Health. 2009; 1(6): 522-530. 19. Spiegelman T, Sciascia A, Uhl T. Return to swimming protocol for competitive swimmers: a post-operative case study and fundamentals. Int J Sports Phys Ther. 2014; 9(5): 712-725. 20. Liem BC, Truswell HJ, Harrast MA. Rehabilitation and return to running after lower limb stress fractures. Curr Sports Med Reports. 2013; 12(3): 200-207.

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21. Kraeutler MJ, Anderson J, Chahla J, et al. Return to running after arthroscopic hip surgery: literature review and proposal of physical therapy protocol. J Hip Preserv Surg. 2017; 4(2): 121-130. 22. Sanchis-Alfonso V. Anterior Knee Pain and Patellar Instability. Springer Science and Business Media; 2011: 109-111. 23. Turner AN, Stewart PF. Repeat sprint ability. Strength Cond J. 2013; 35(1): 37-41. 24. Nagelli CV, Hewett TE. Should return to sport be delayed until 2 years after anterior cruciate ligament reconstruction? Biological and functional considerations. Sports Med. 2017; 47(2): 221-232. 25. Welling W, Benjaminse A, Seil R, et al. Low rates of patients meeting return to sport criteria 9 months after anterior cruciate ligament reconstruction: a prospective, longitudinal study. Knee Surg Sports Traumatol Arthrosc. 2018(26(12): 3636-3644. 26. Angelozzi M, Madama M, Corsica C, et al. Rate of force development as an adjunctive outcome measure for return-to-sport decisions after anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2012; 42(9): 772-780. 27. Toole AR, Ithurburn MP, Rauh MJ et al. Young athletes cleared for sports participation after anterior cruciate ligament reconstruction: how many actually meet recommended return-to-sport criterion cutoffs? J Orthop Sports Phys Ther. 2017; 47(11): 825-833. 28. Curran MT, Lepley LK, Palmieri-Smith RM. Continued improvements in quadriceps strength and biomechanical symmetry of the knee after postoperative anterior cruciate ligament reconstruction rehabilitation: is it time to reconsider the 6-month return to activity criteria? J Ath Train. 2018; 53(6): 535-544.

29. Filbay SR, Grindem H. Evidence-based recommendations for the management of anterior cruciate ligament rupture. Best Pract Res Clin Rheumatol. https://doi.org/10/1016/j. berh.2019.01.018. 30. Kyritsis P, Bahr R, Landreau P, et al. Likelihood of ACL graft rupture: not meeting six clinical discharge criteria before return to sport is associated with a four times greater risk of rupture. Br J Sports Med. 2016; 50(15): 946-951. 31. Van Melick N, van Cingel REH, Brooijmans F, et al. Evidence-based clinical practice update: practice guidelines for anterior cruciate ligament rehabilitation based on a systematic review and multidisciplinary consensus. Br J Sports Med. 2016; 50: 1506-1515. 32. Nawasreh Z, Logerstedt D, Cummer K, et al. Do patients failing return to activity criteria at 6 months after anterior cruciate ligament reconstruction continue demonstrating deďŹ cits at 2 years? Am J Sports Med. 2016; 45(5): 1037-1048. 33. Ardern C, Taylor NF, Feller JA, Webster KE. Fifty-ďŹ ve percent return to competitive sport following anterior cruciate ligament reconstruction surgery: an updated systematic review and meta-analysis including aspects of physical functioning and contextual factors. Br J Sports Med. 2014; 48: 1543-1552.

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APPENDIX A PROGRESSION TO SPRINTING Stage 1. 50% INTENSITY ( 1:3 work to rest ratio).

Stage 2. 75% INTENSITY (1:5 work to rest ratio).

Stage 3. 90 - 100% INTENSITY (1:7 work to rest ratio).

The International Journal of Sports Physical Therapy | Volume 15, Number 2 | April 2020 | Page 332

PERFORMANCE & RECOVERY We believe in Powering Motion. Activity is the key to living a healthier lifestyle, better treatment outcomes, and improved healthcare economics for all. We do this by delivering a complete Orthopedic Continuum of Care from performance and mobility to surgical intervention and post-operative rehabilitation. Get and keep people movingâ&#x20AC;&#x201D;thatâ&#x20AC;&#x2122;s our philosophy.

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Individual results may vary. Neither DJO Global, Inc. nor any of its subsidiaries dispense medical advice. The contents of this ad do not constitute medical, legal, or any other type of professional advice. Rather, please consult your healthcare professional for information on the courses of treatment, if any, which may be appropriate for you. Copyright DJO, LLC MKT00-9279 Rev A

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