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Contralateral Effects of Eccentric Resistance Training on Immobilized Arm Article in Scandinavian Journal of Medicine and Science in Sports · August 2020 DOI: 10.1111/sms.13821

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Received: 7 May 2020 DOI: 10.1111/sms.13821

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Revised: 27 August 2020

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Accepted: 31 August 2020

ORIGINAL ARTICLE

Contralateral effects of eccentric resistance training on immobilized arm Omar Valdes1,2 | Carlos Ramirez1 | Felipe Perez1 Kazunori Nosaka4 | Luis Penailillo1 1

Exercise Science Laboratory, School of Kinesiology, Faculty of Medicine, Universidad Finis Terrae, Santiago, Chile 2

Faculty of Health Sciences, Universidad de las Américas, Santiago, Chile 3

Physiology of Exercise and Activities in Extreme Conditions Unit, Operational Environments Department, French Armed Forces Biomedical Research Institute (IRBA), Brétigny sur Orge, France 4

Centre for Exercise and Sports Science Research, School of Medical and Health Sciences, Edith Cowan University, Joondalup, WA, Australia Correspondence Luis Peñailillo, School of Kinesiology, Universidad Finis Terrae, 1509 Pedro de Valdivia Av., Providencia, Santiago, Chile.

Email: lpenailillo@uft.cl

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Sebastian Garcia-Vicencio3

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Abstract This study compared the effects of contralateral eccentric-only (ECC) and concentric-/eccentric-coupled resistance training (CON-ECC) of the elbow flexors on immobilized arm. Thirty healthy participants (18-34 y) were randomly allocated to immobilization only (CTRL; n = 10), immobilization and ECC (n = 10), or immobilization and CON-ECC group (n = 10). The non-dominant arms of all participants were immobilized (8 h·day−1) for 4 weeks, during which ECC and CON-ECC were performed by the dominant (non-immobilized) arm 3 times a week (3-6 sets of 10 repetitions per session) with an 80%-120% and 60%-90% of one concentric repetition maximum (1-RM) load, respectively, matching the total training volume. Arm circumference, 1-RM and maximal voluntary isometric contraction (MVIC) strength, biceps brachii surface electromyogram amplitude (sEMGRMS), rate of force development (RFD), and joint position sense (JPS) were measured for both arms before and after immobilization. CTRL showed decreases (P < .05) in MVIC (−21.7%), sEMGRMS (−35.2%), RFD (−26.0%), 1-RM (−14.4%), JPS (−87.4%), and arm circumference (−5.1%) of the immobilized arm. These deficits were attenuated or eliminated by ECC and CON-ECC, with greater effect sizes for ECC than CON-ECC in MVIC (0.29: +12.1%, vs −0.18: −0.1%) and sEMGRMS (0.31:17.5% vs −0.15: −5.9%). For the trained arm, ECC showed greater effect size for MVIC than CONECC (0.47 vs 0.29), and increased arm circumference (+2.9%), sEMGRMS (+77.9%), and RDF (+31.8%) greater (P < .05) than CON-ECC (+0.6%, +15.1%, and + 15.8%, respectively). The eccentric-only resistance training of the contralateral arm was more effective to counteract the negative immobilization effects than the concentriceccentric training.

KEYWORDS

arm circumference, cross-education effect, elbow flexors, electromyography, interlimb transfer, joint position sense, muscle strength, rate of force development

© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Scand. J. Med. Sci. Sports. 2020;00:1–15. 

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wileyonlinelibrary.com/journal/sms 1

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1

| IN TRO D U C T ION

Immobilization is used to restrict joint movements to prevent further tissue damage after injuries,1 but decreases muscle strength and muscle mass of the immobilized limb, which takes a long time to recover.2-4 For instance, 1.2% decreases in maximal voluntary contraction (MVC) muscle strength and 0.2% decreases in muscle size per day have been reported for the elbow flexors during immobilization.3 Thus, clinical strategies to minimize the negative effects of immobilization on neuromuscular function and muscle atrophy are necessary.

It has been shown that resistance training of the non-immobilized contralateral limb minimizes the negative effects of immobilization due to “cross-education” or “interlimb-transfer” effect.5-7 In resistance training, the type of muscle contractions (eg, isometric versus dynamic) used in the training seems to be an important factor determining the magnitude of the cross-education effect. Previous meta-analysis studies have shown that greater cross-education effects are obtained by dynamic than isometric resistance training protocols.8,9 However, the meta-analysis did not include the studies that investigated contralateral training during immobilization.

To the best of our knowledge, only two studies have investigated the contralateral effect of dynamic resistance training on immobilization. Pearce et al6 reported that resistance training consisting of concentric-/eccentric-coupled contractions at 50%-70% of one repetition maximum (1-RM) increased maximal voluntary isometric contraction (MVIC) strength (5.8%) as well as dynamic (concentric 1-RM) strength (13.9%) of the elbow flexors in the trained arm, and maintained the MVIC and 1-RM strength of the contralateral non-trained arm after 3 weeks of sling immobilization.

Andrushko et al10 showed that contralateral maximal isokinetic eccentric training of the wrist flexors during 4 weeks of immobilization induced 33% increase in MVIC strength in the trained arm and preserved MVIC strength in the immobilized homologous muscles. Thus, it appears that dynamic resistance training of the contralateral limb is a good strategy to minimize the deleterious effects of immobilization. The heterogeneity of the contralateral effects could be attributable to the mode, intensity, volume, and velocity of the resistance exercise training.9 However, it is not clear whether concentric or eccentric contractions in dynamic resistance exercise training could affect the contralateral effect during immobilization differently.

Hortobágyi et al11 showed that maximal isokinetic eccentric resistance training of the knee extensor muscles induced 2 times greater increase in MVIC strength of the contralateral homologous muscles when compared to maximal isokinetic concentric resistance training. Kidgell et al12 compared volume-matched contralateral eccentric-only and concentric-only isokinetic strength training of the wrist flexors on muscle strength in the non-trained contralateral muscles.

VALDES et al.

They showed that the magnitude of strength transfer to the non-trained contralateral homologous muscles was 19% greater in the eccentric than concentric training, and stated that the greater eccentric-only contralateral training effect could be due to the greater increase in corticospinal excitability and decrease in intracortical inhibition in the non-trained limb.12 It seems possible that eccentric-only resistance training in which a heavier load can be applied induces a greater contralateral effect on muscle strength than dynamic resistance training consisting of concentric and eccentric contractions in which a load is lighter because of the less capability of maximal force generation for concentric than eccentric contraction. Comparisons between eccentric-only and concentric-only contractions are widely reported in favor of eccentric-only contractions.11-14 Thus, it is interesting to investigate whether eccentric-only contractions induce greater contralateral effects on immobilized muscles than concentric-/eccentric-coupled contractions. No previous study has compared eccentric-only and concentric-/eccentric-coupled resistance training with a matched training load for their effects on changes in muscle functions of trained and nontrained (immobilized) muscles after immobilization. The contralateral effects on rate of force development (RFD) and joint position sense (JPS) have not been examined in the previous studies, although they are important for functional tasks. It may be that RFD is more affected by immobilization than MVIC strength. 15,16 Moreover, it is possible that immobilization could also reduce feedback from muscle proprioceptors (ie, muscle spindles and Golgi tendons organs) and/ or articular mechanoreceptors, impairing JPS.17 Therefore, the aim of this study was to compare the contralateral effect of eccentric-only and concentric-/eccentric-coupled resistance training with a matched volume on changes in arm circumference, concentric 1-RM and MVIC strength, surface electromyography (sEMG), RFD, and elbow flexion JPS for both immobilized and non-immobilized (trained) elbow flexors before and after four weeks of immobilization using healthy young individuals. We hypothesized that the eccentric-only resistance training would increase muscle function of the trained arm and attenuate negative effects of immobilization on the immobilized muscles better when compared to concentric-/eccentric-coupled resistance training.

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| M ETHODS

2.1 | Participants and study design Thirty healthy men (n = 18) and women (n = 12) participated in this study. Their mean (± SD) age, height, body mass, and body mass index (BMI) were 24.3 ± 3.5 y, 169.4 ± 10.0 cm, 72.4 ± 17.9 kg, and 24.9 ± 4.4 kg/m2, respectively. The

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VALDES et al.

T A B L E 1 Resistance training protocols for concentric-/eccentric-coupled (CON-ECC) and eccentric-only (ECC) training groups CON-ECC Week

Set × Rep

1

4 × 10

ECC Intensity % CON 1-RM 60%

WV (kg) 763 ± 424

TWV (kg)

Set × Rep

5342 ± 2969

3 × 10

Intensity % CON 1-RM 80%

WV (kg) 864 ± 339

2

6 × 10

70%

1335 ± 742

4 × 10

100%

1440 ± 565

3

6 × 10

80%

1526 ± 848

4 × 10

110%

1584 ± 622

4

6 × 10

90%

1717 ± 954

4 × 10

120%

1728 ± 678

TWV (kg) 5616 ± 2220

Note: Sets and repetitions (set/rep), intensity based on concentric one repetition maximum (CON 1-RM), weight volume (WV, mean ± SD values of 10 participants) of each week (week 1 to week 4), and the total weight volume (TWV, mean ± SD) are shown. No significant differences (P = .73-.97) between ECC and CON-ECC were evident for WV and TWV.

present study excluded the participants who had been performing resistance training of upper limb muscles and/or who had an injury of upper limb in the previous one year. The participants were either right (n = 23)- or left (n = 7)-hand dominant based on the hand that participants use for writing. They were placed to one of the three groups (n = 10 per group): control (immobilization only) group (CTRL; 6 males and 4 females, 7 right handed and 3 left handed), immobilization and contralateral eccentric-only resistance training group (ECC; 6 males and 4 females, 8 right handed and 2 left handed), or immobilization and contralateral concentric-/ eccentric-coupled resistance training group (CON-ECC; 6 males and 4 females, 8 right handed and 2 left handed). The placement was random but considered that the gender and hand dominance balance were similar among the groups.

According to a meta-analysis study that reported an effect size of 0.6 for the contralateral muscle strength gains after resistance training,9 the present study used this effect size to estimate the sample size, with an alpha level of 0.05, and statistic power of 0.8 (G × Power 3.1, Germany). This estimation revealed that 10 participants per group would be sufficient. All participants were instructed to refrain from upper body resistance training outside of the study, any kind of nutritional supplement, and anti-inflammatory medication, and to maintain their normal daily routines during the experimental period. A written informed consent was obtained from all participants, and the study was approved by the Institutional Ethics Committee (clinical trial registration number: DRKS00017169) and conducted according to the Helsinki Declaration.

A week prior to the baseline measurements, all participants participated in a familiarization session in which anthropometric measurements were taken and all testing procedures were explained and practiced. The measurements of all dependent variables were assessed on both immobilized and non-immobilized arms. The dependent variables included upper arm circumference (CIR), concentric 1-RM strength (CON 1-RM), MVIC strength, muscle activity by sEMG, RFD, and elbow flexion JPS. The measurements were taken 72 hours (MVIC, sEMG, and RFD) or 48 hours

(JPS and CON1-RM) before the commencement of the immobilization and at 48 and 72 hours after the last training session in the same order. The same time frame was applied for the CTRL group without the training.

2.2 | Immobilization Four weeks of arm immobilization by a sling was implemented for the non-dominant arm of all participants, and the protocol was adapted from previous studies.5,6,18 The sling suspended the elbow joint at 90° of flexion with mild shoulder internal rotation to unload the elbow flexor muscles.

Participants were instructed to wear an arm sling for 8 hours per day during waking hours, and the sling was removed for driving, showering/bathing, and sleeping. The protocol has been shown to induce approximately 20% decrease in dynamic strength,6 35% decrease in the MVIC strength, and 11% decrease in muscle cross-sectional area of the elbow flexors.18

2.3 | Resistance training The participants in the ECC and CON-ECC groups performed resistance training of the elbow flexors using adjustable dumbbells with a preacher curl bench for the dominant (non-immobilized) arm three times a week during the four weeks of immobilization. The ECC training consisted of 4 seconds of eccentric contraction from 135° flexion to full extension (0° of elbow flexion) of the elbow joint (total ROM: 135°); then, the investigator took the dumbbell and brought it back to the staring position; thus, the participant returned the arm to the flexed position without load. The CON-ECC training consisted of 2 seconds of concentric contraction from full elbow extension (0°) to 135° flexion (total ROM = 135º) and 2 seconds of eccentric contractions from 135° elbow flexion to full extension (0°). A 2-s resting time between repetitions and a 2-min resting time between sets were provided for both training

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groups. Execution time during training was monitored using a metronome (Cifra Club for iOS, Minas Gerais, Brazil). Training workload was dosed to achieve the same total weight volume between the groups (Table 1).

2.4 | Dependent variables 2.4.1 | Upper arm circumference Upper arm circumference was measured at 3, 6, and 9 cm away from the interarticular line of the elbow when each participant was sitting while maintaining the arm relaxed at full elbow extension position (0° of elbow flexion). The arm circumference was also measured during maximal isometric contraction of elbow flexors with the shoulder and elbow joints at 90° of flexion using an inextensible metrical tape (Lufkin Executive Thinline, Maryland, USA). The circumference was used as a surrogate measure to estimate changes in muscle volume.19 Measurements were repeated three times for each site, and a median value was used to represent each measure, and the average of the four measurements (ie, 3, 6, 9 cm and maximal) was used for further analysis.

2.4.2 | Concentric one repetition maximum (CON 1-RM) Concentric single arm 1-RM strength was measured in sitting on the preacher curl bench in which each participant attempted to lift the heaviest dumbbell possible one time, based on a previous study.20 The dumbbell was adjusted in 0.5 kg, and CON 1-RM was obtained between 3 and 5 attempts.

2.4.3 | Maximal voluntary isometric contraction (MVIC) strength The MVIC strength of the elbow flexors was assessed simultaneously with surface electromyography (sEMG) of biceps brachii, from which the RFD analyses were also performed.

MVIC strength of the elbow flexors was assessed at 90º of elbow flexion and 30º of shoulder flexion on a bench customized with a load cell (Revere transducers 200 lb, Netherland).

Each participant performed a 3-s warm-up contraction for both arms at 50%, 70%, and 80% of the self-perceived MVIC with a 45-s rest between contractions after which each participant performed three MVICs of 3-s with a 60-s rest between attempts for each arm. A strong verbal encouragement and visual feedback were provided for all participants, which were instructed to “pull as hard and fast as possible.” The force signal was amplified and recorded using a Trigno EMG system (Delsys EMGworks®, National Instruments, Boston,

VALDES et al.

Massachusetts, USA). The greatest force value out of three measurements was used for further analysis.

2.4.4 | Muscle activity by surface electromyography The surface electromyography (sEMG) of biceps brachii muscle was recorded during the MVIC strength measures using active double-differential electrodes with a wireless system (Trigno Wireless EMG System, Delsys, Boston, Massachusetts, USA). The skin was prepared by shaving, abrasing, and cleaning the area with 70% isopropyl alcohol prior to placing the electrodes. The electrodes were positioned by marking the skin at two-thirds of the distance between the acromion and the lateral epicondyle, while the participant stood relaxed in anatomical position based on SENIAM guidelines.21 The electromyogram was analyzed using the company software (Delsys EMGworks® 4.5.4, Massachusetts, USA). The signals were amplified and filtered using a butterworth and band-pass filter with 10-450 Hz frequency range, gain of 1000, and recorded at high frequency (2000 Hz). The central 2-s filtered signal corresponding to the best trial of MVIC strength was used in the analyses, and the root mean square (RMS) of the signal amplitude was performed with a window length of 0.1 ms

2.4.5 | Rate of force development (RFD) RFD was measured as the slope of MVIC force trace of the greatest MVIC strength trial in the time windows of 0-50 ms (RDF50), 0-100 ms (RDF100), and 0-200 ms (RDF200) based on previous studies.15,16,22,23 The onset of muscle contraction was defined as the time point at force curve exceeded the baseline by > 8 N. Analyses were performed using MATLAB software version 7.12 (MathWorks, R2011a, Natick, Massachusetts, USA).

2.4.6 | Elbow flexion joint position sense The elbow flexion joint position sense was assessed using a smartphone application (Goniometer Pro Viewer 2.9, version for iOS, USA) with a method previously described.24 Each participant lied on a bed in supine position, and full active range of movement (AROM) was determined with the device located in the lateral forearm aligned to lateral epicondyle of the humerus and styloid apophysis of the radius for both arms. The participant with the eyes closed was asked to reproduce the elbow joint at a previously demonstrated position (30% and 50% of full AROM), from which the degrees of error from the targeted position were recorded. The error

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VALDES et al.

in degrees was recorded, and this was repeated three times for each target. The average of the errors for both positions (30% and 50% AROM) was used for analyses.

2.4.7 | Test-retest reliability of the dependent variable measures To assess the test-retest reliability of each dependent variable measure, another group of 10 participants was recruited. Their mean (± SD) age, height, body mass, and BMI were 26.2 ± 3.4 y, 167.8 ± 9.2 cm, 68.4 ± 12.4 kg, and 24.2 ± 3.2 kg/ m2, respectively, which were not different from those of the CTRL, ECC, and CON-ECC groups. The measurements were taken at two sessions with an interval of four weeks. The reliability between sessions was assessed using intra-class correlation coefficient (ICC2.1) with 95% confidence intervals (CIs). The within-participant coefficient of variation (CV) was calculated by using the formula CV = SDpooled/ mean and expressed as a percentage (CV %), where the mean is the difference between the two trials, and SDpooled is the standard deviation of differences of the trials.

2.5 | Statistical analyses Normal distribution was verified using a Shapiro-Wilk test, from which all variables were confirmed to be normally distributed. A two-way repeated-measures analysis of variance (ANOVA) was used to compare the three groups (CTRL, CON-ECC, and ECC) for changes in each variable over time (pre- and post-training) for all dependent variables. If a significant interaction effect was found, a Bonferroni post hoc test for pairwise comparisons was performed. To compare the normalized changes in each variable from the pre- to post-training between groups, a one-way ANOVA with Bonferroni post hoc test was used. These analyses were performed for both immobilized and non-immobilized arms. Additionally, the effect sizes (ES) were calculated for the changes over time for each dependent variable. ES were interpreted as 0.00 < trivial <0.20, 0.20 ≤ small <0.60, 0.60 ≤ moderate <1.20, 1.20 ≤ large <2.00, 2.00 ≤ very large < 4.00.25 All statistical analyses were done using a GraphPad (PRISM 7.0, California). The statistical significance was set at P ≤ .05. Descriptive data are presented as mean and standard deviation (mean ± SD).

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| R E S U LTS

3.1 | Baseline values No significant differences among the groups were found for age (CTRL = 23.5 ± 5.0 y, ECC = 25.0 ± 1.9

y, CON-ECC = 25.1 ± 3.8 y; P = .29), height (CTRL = 169.1 ± 12.1 cm, ECC = 168.1 ± 10.1 cm, CON-ECC = 172.1 ± 8.3 cm; P = .88), body mass (CTRL = 71.6 ± 17.4 kg, ECC = 73.0 ± 20.6 kg, CON-ECC = 74.3 ± 17.1 kg; P = .86), and BMI (CTRL = 24.7 ± 3.8 kg/m2, ECC = 25.5 ± 5.8 kg/ m2, CONECC = 24.8 ± 3.8 kg/m2; P = .57). As shown in Table 2, the baseline values were similar among the groups for immobilized and non-immobilized arm, respectively, for arm circumference (immobilized arm: P = .90, non-immobilized arm: P = .80), CON 1-RM (P = .76, P = .84), MVC (P = .70, P = .76), sEMG (P = .35, P = .55), RFD50 (P = .37, P = .41), RFD100 (P = .61, P = .47), RFD200 (P = .65, P = .44), and JPS (P = .90, P = .88).

3.2 | Exercise training As shown in Table 1, the training intensity and volume were progressively increased from week 1 to week 4 for the ECC and CON-ECC groups, respectively. No significant (P = .80) difference in the total weight volume lifted was evident between the groups.

3.3 | Test-retest reliability of the dependent variable measures The relative reliability (ICC2,1) for the dependent variables ranged from “moderate” (0.50-0.75) to “excellent” (≥0.90), and the absolute reliability (CV%) was less than 10% for all measures. The ICC2,1 and CV values for each dependent variable were arm circumference (ICC2,1:0.95, CV: 0.9%), CON 1-RM (0.98, 2.1%), MVIC (0.97, 2.2%), sEMGRMS (0.99, 5.6%), RFD50 (0.76, 8.9%), RFD100 (0.74, 7.7%), RFD200 (0.73, 8.3%), and elbow flexion JPS (0.85, 8.3%).

3.4 | Arm circumference (CIR) A significant interaction (group × time) effect was found for changes in upper arm CIR in the immobilized (P = .003) and non-immobilized arms (P < .001). The magnitude of the changes in the arm CIR from the baseline to post-immobilization for the immobilized and non-immobilized arms is shown in Table 2 and Figure 1. For the immobilized arm, the CTRL (P < .001), CON-ECC (P = .006), and ECC groups (P = .013) showed a decrease in arm CIR after 4 weeks. However, the decrease was smaller for the ECC (−2.1 ± 2.5%; P = .008) and CON-ECC (−2.1 ± 1.1%; P = .009) when compared to the CTRL group (−5.1 ± 2.1%). For the non-immobilized arm, a significant increase was evident only for the ECC (2.9 ± 1.4%; P < .001), while CON-ECC (0.6 ± 0.6%;

266.6 ± 79.5

594 ± 385

4349 ± 970

2299 ± 638

1135 ± 314

6.2 ± 2.4

MVIC Strength (N)

sEMGRMS (μV)

RFD50 (N/s)

RFD100 (N/s)

RFD200 (N/s)

JPS (º)

−0.87 (CI 95%: −1.79-0.05) −0.90 (CI 95%: −1.82-0.02)

3236 ± 1370†

−0.35 (CI 95%: −1.23-0.53)

2054 ± 692 1060 ± 332† 0.37 (CI 95%: −0.51-1.26)

−0.49 (CI 95%: −1.37-0.40)

†

7.0 ± 3.1

−0.66 (CI 95%: −1.56-0.24)

−0.16 (CI 95%: −1.03-0.72)

−0.17 (CI 95%: −1.05-0.71)

−0.04 (CI 95%: −0.91-0.84)

−0.01 (CI 95%: −0.89-0.87)

3680 ± 1165

420 ± 239

245.4 ± 75.7

10.9 ± 5.1

28.4 ± 4.3

10.2 ± 2.4

1.59 (CI 95%: 0.58-2.59)

−0.62 (CI 95%: −1.52-0.28)

918 ± 355† †

−0.88 (CI 95%: −1.79-0.04)

1738 ± 588

†

−0.74 (CI 95%: −1.65-0.16)

335 ± 118†

−0.27 (CI 95%: −1.15-0.61)

−0.35 (CI 95%: −1.23-0.54)

209.1 ± 67.8

9.2 ± 4.6

†

26.5 ± 3.9†

5.3 ± 1.6

1280 ± 503

2415 ± 858

3940 ± 1505

521 ± 303

283.9±105.5

10.6 ± 5.9

28.6 ± 3.5

6.1 ± 2.5

1295 ± 499

2545 ± 782

4916 ± 1465

511 ± 230

288.7 ± 115.0

10.2 ± 5.4

28.2 ± 3.5

0.31 (CI 95%: −0.59-1.17)

4.3 ± 1.3

1387 ± 441

2729 ± 799

†

4657 ± 1577

592 ± 337

−0.68 (CI 95%: −1.58-0.22)

0.22 (CI 95%: −0.66-1.10)

0.36 (CI 95%: −0.52-1.25)

0.45 (CI 95%: −0.44-1.33)

0.21 (CI 95%: −0.67-1.09)

314.5 ± 97.5† 0.29 (CI 95%: −0.59-1.17)

12.4 ± 6.2

0.04 (CI 95%: −0.83-0.92) †

0.18 (CI 95%: −0.69-1.06)

−0.30 (CI 95%: −1.19-0.58)

−0.20 (CI 95%: −1.08-0.67)

−0.33 (CI 95%: −1.21-0.56)

−0.15 (CI 95%: −1.03-0.72)

−0.18 (CI 95%: −1.05-0.70)

−0.02 (CI 95%: −0.89-0.86)

−0.18 (CI 95%: −1.06-0.70)

Effect size

28.8 ± 3.5

6.7 ± 2.9

1163 ± 310

2404 ± 513

4488 ± 1014

475 ± 212

271.0 ± 73.6

10.2 ± 5.5

27.6 ± 3.3†

Post

Significant difference from baseline to post-immobilization.

†

Note: No significant differences at baseline (P > .05) in all dependent variables between the groups were found for the immobilized and non-immobilized arms.

5.8 ± 2.6

JPS (º)

4513 ± 1246

RFD50 (N/s)

1198 ± 415

460 ± 249

sEMGRMS (μV)

2424 ± 763

260.3 ± 90.4

MVIC Strength (N)

RFD100 (N/s)

11.1 ± 5.4

CON 1-RM (kg)

RFD200 (N/s)

28.5 ± 4.2

Arm CIR (Cm)

Non-immobilized arm

10.5 ± 4.7

CON 1-RM (kg)

†

27.9 ± 4.1

Effect size

Pre

Post

Pre

Arm CIR (Cm)

Immobilized arm

CON-ECC

CTRL

5.9 ± 3.7

1031 ± 384

2038 ± 727

3653 ± 1634

393 ± 218

251.0 ± 99.2

12.0 ± 4.7

27.5 ± 4.2

6.7 ± 4.4

1075 ± 457

2174 ± 863

4067 ± 1559

410 ± 185

239.9 ± 90.2

119 ± 5.0

27.4 ± 4.3

Pre

ECC

†

0.35 (CI 95%: −0.55-1.22)

0.18 (CI 95%: −0.70-1.06)

−0.16 (CI 95%: −1.04-0.72)

0.03 (CI 95%: −0.85-0.90)

0.06 (CI 95%: −0.81-0.94)

0.08 (CI 95%: −0.80-0.96)

0.31 (CI 95%: −0.57-1.20)

0.29 (CI 95%: −0.59-1.17)

0.07 (CI 95%: −0.81-0.94)

−0.13 (CI 95%: −1.00-0.75)

Effect size

0.57 (CI 95%: −0.32-1.47) −0.64 (CI 95%: −1.54-0.26)

3.7 ± 2.7†

0.71 (CI 95%: −0.20-1.61) 1307 ± 526†

2652 ± 928

0.61 (CI 95%: −0.29-1.50)

4763 ± 1854† †

0.90 (CI 95%: −0.02-1.82)

624 ± 268†

303.5 ± 114.8† 0.47 (CI 95%: −0.42-1.36)

13.7 ± 5.0†

28.3 ± 4.4†

6.0 ± 4.3

1086 ± 398

2230 ± 823

4196 ± 1592

474 ± 206

267.9 ± 97.0

12.2 ± 5.0

26.8 ± 4.4†

Post

repetition maximum strength (CON 1-RM), maximal voluntary isometric contraction strength (MVIC), rate of force development at 0-50 ms (RFD50), 0-100 ms (RFD100), and 0-200 ms (RFD200), surface electromyographic root mean squared amplitude (sEMGRMS), and elbow flexion joint position sense (JPS) for the immobilized and non-immobilized arms of the control (CTRL), concentric-/ eccentric-coupled (CON-ECC), and eccentric-only (ECC) groups

T A B L E 2 Pre- and post-values (mean ± SD) with effect size (ES) 95% of confidence interval (CI) for the change from pre to post-condition of upper arm circumference (CIR), concentric one

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F I G U R E 1 Normalized changes in upper arm circumference (A, B) and concentric one repetition maximum (CON 1-RM; C, D) from baseline to post-immobilization for the immobilized arm (A, C) and non-immobilized arm (B, D) of individual participants and their average ± SD values for the control group (CTRL), concentric-/eccentric-coupled resistance training group (CON-ECC), and eccentric resistance training group (ECC). †Significant difference from baseline to post-immobilization. *Significant difference in comparison with the CTRL group. #Significant difference in comparison with the CON-ECC group

P = .38) and CTRL (−0.2 ± 0.9%; P = .34) groups did not show any significant changes, with ECC showing a greater increase in arm CIR than CON-ECC (P < .001) and CTRL (P < .001) groups.

3.5 | Concentric 1-RM strength A significant (P < .001) interaction (group × time) effect was observed for changes in concentric 1-RM strength from baseline to post-immobilization for both immobilized and non-immobilized arms. The magnitude of the changes in concentric 1-RM strength from the baseline to post-immobilization for the immobilized and non-immobilized arms is shown in Table 2 and Figure 1. For the immobilized arm (Figure 1C), concentric 1-RM strength decreased for the CTRL group (−14.4 ± 7.5%; P < .001), but the CON-ECC group did not show a significant change (−0.1 ± 19%; P = .99), and ECC

showed a tendency to increase (3.4 ± 4.8%; P = .06) with four out of 10 participants showed an increase (>5%). The magnitude of change in concentric 1-RM strength for ECC (P < .001) and CON-ECC (P < .001) was greater than the CTRL group. For the non-immobilized arm, concentric 1-RM strength increased for the ECC (15.2 ± 7.9%; P < .001) and CON-ECC groups (21.2 ± 9.7%; P < .001), but no significant change was found for the CTRL group (−1.2 ± 2.0%; P = .83). No difference between ECC and CON-ECC groups (P = .17) was found for the magnitude of change in concentric 1-RM.

3.6 | MVIC strength A significant interaction (group × time) effect was found for changes in MVIC strength of the immobilized and nonimmobilized arm (P < .001). The magnitude of the change

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in the MVIC strength from the baseline to post-immobilization for the immobilized arm and non-immobilized arm is shown in Table 2 and Figure 2. MVIC strength of the immobilized arm decreased by 21.7 ± 13.6% from the baseline for the CTRL group (P = .001), but did not change for the CON-ECC group (−0.1 ± 19.7%; P = .68) and increased for the ECC group (+12.7 ± 9.6%; P = .003).

Post-immobilization MVIC strength was greater for the ECC (P = .009) and CON-ECC (P < .001) than the CTRL group. For the non-immobilized (trained) arm (Figure 2B), MVIC strength increased more after training for ECC (20.9 ± 11.6%; P < .001; ES = 0.47) than the CON-ECC group (13.7 ± 9.3%; P = .009; ES = 0.29), while no significant change was evident for the CTRL group (−3.9 ± 12.3%; P = .08). The change in MVIC strength in non-immobilized arm was greater for the ECC (P < .001) and CON-ECC (P = .004) than the CTRL group.

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3.7 | sEMGRMS A significant interaction (group × time) effect was also evident for changes in sEMGRMS of the immobilized (P = .004) and non-immobilized arms (P = .005). The magnitude of the changes in sEMGRMS from the baseline to post-immobilization for the immobilized arm and non-immobilized arms is shown in Table 2 and Figure 2. The sEMGRMS of the immobilized arm was maintained for the ECC (17.5 ± 16.5%; P = .96) and CON-ECC groups (−5.9 ± 16.6%; P = .99), but decreased for the CTRL group (−35.2 ± 27.1%; P = .001) after immobilization. For the immobilized arm, the change in sEMGRMS was greater for ECC (P < .001) and CON-ECC (P = .014) than the CTRL group, and also for ECC than the CON-ECC group (P = .045). In the nonimmobilized (trained) arm, only the ECC group showed an increase in sEMGRMS (77.9 ± 71.2%; P = .001), while the

F I G U R E 2 Normalized changes in maximal voluntary isometric contraction (MVIC) strength for the immobilized arm (A) and nonimmobilized arm (B), and surface electromyographic root mean square amplitude (sEMGRMS) in the immobilized arm (C) and the non-immobilize arm (D) from baseline to post-immobilization for individual participants and their average ± SD values of the control group (CTRL), concentric-/ eccentric-coupled resistance training group (CON-ECC), and eccentric resistance training group (ECC). †Significant difference from baseline to post-immobilization. *Significant difference in comparison with the CTRL group. #Significant difference in comparison with the CON-ECC group

CON-ECC group (15.1 ± 27.5%; P = .58) and CTRL group (−0.2 ± 33.8%; P = .99) did not show significant changes.

For the non-immobilized arm, the change in sEMGRMS observed in ECC was greater than CON-ECC (P = .003) and CTRL (P = .024).

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3.8 | RFD

A significant interaction (group × time) effect was found for changes in all RFD measures (RFD50, RFD100, RFD200) of the immobilized (P < .05) and non-immobilized arms (P < .001).

F I G U R E 3 Normalized changes (mean ± SD) in rate force development at 0-50 ms (RFD50), 0-100 ms (RFD100), and 0-200 ms (RFD200) from baseline to the post-immobilization for the immobilized arm (A, C, D) and non-immobilize arm (B, D, F) of individual participants and their average ± SD values of the control group (CTRL), concentric-/eccentric-coupled resistance training group (CON-ECC), and eccentric resistance training group (ECC). †Significant difference from baseline to post-immobilization. *Significant difference in comparison with the CTRL group. # Significant difference in comparison with the CON-ECC group

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Table 2 and Figure 3 show the magnitude of change in RFD from the baseline to post-immobilization for the immobilized arm and non-immobilized arm. For the immobilized arm, RFD decreased for the CTRL group (RFD50: −25.7 ± 28.1%, P = .004; RFD100: −24.1 ± 21.3%, P = .001; RFD200: −21.0 ± 18.5%, P = .006), but did not change significantly for the ECC (1.6 ± 14.1%, P = .99; 3.8 ± 14.8%, P = .99; 3.8 ± 15.6%, P = .99) and CON-ECC groups (−5.6 ± 16.6%, P = .55; −2.2 ± 16.6%, P = .99; −5.4 ± 18.6%, P = .14), with a significant (P < .05) difference between CTRL and the two training groups. For the non-immobilized arm, RFD increased in all time slots after training for the ECC (RFD50: 53.3 ± 89.4%, P = .050; RFD100: 31.8 ± 18.6%, P < .001; RFD200: 26.9 ± 15.0%; P < .001), while the CON-ECC group increased the RFD100 only (15.8 ± 11.2%, P = .005).

However, RFD decreased for the CTRL group (RFD100: −14.9 ± 10.8%, P = .001; RFD200: −10.4 ± 6.1%, P = .003).

The changes in RFD were greater for both training groups in comparison with the CTRL group (P < .05), but the ECC group showed greater increases in RFD100 (P = .050) and RFD200 (P = .032) than the CON-ECC group.

3.9 | Elbow flexion JPS A significant (P < .001) interaction (group × time) effect was also evident for changes in elbow flexion JPS over time for both immobilized and non-immobilized arms.

The magnitude of change in the JPS from the baseline to post-immobilization for the immobilized and non-immobilized arms is shown in Table 2, Figure 4A,B, respectively.

For the immobilized arm, the position error increased after immobilization for the CTRL group (87.4 ± 78.9%;

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P < .001), but did not change for the ECC (−10.6 ± 56.2%; P = .99) and CON-ECC groups (10.3 ± 45.0%; P = .99).

The position error for the immobilized arm was greater for CTRL in comparison with the CON-ECC (P = .04) and ECC (P = .004) groups. The position error in the non-immobilized (trained) arm decreased for the ECC (−34.8 ± 33.8%; P = .014), but did not change for CONECC (−16.9 ± 17.8%; P = .47) and CTRL (33.3 ± 59.9%; P = .36) groups. For the non-immobilized arm, the error position was minor for ECC (P = .003) and CON-ECC (P = .032) than the CTRL group.

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| DISCUSSION

The present study compared the effects of eccentric-only and concentric-/eccentric-coupled resistance training performed by the non-immobilized arm during a 4-week immobilization for changes in several variables associated with muscle function and muscle atrophy after the immobilization in healthy young individuals. The main findings of the present study were 1) eccentric-only resistance training produced greater increases in upper arm circumference, MVIC strength, muscle activity, and RFD than concentric-/eccentric-coupled resistance training for the non-immobilized (trained) arm; and 2) eccentric-only resistance training improved MVIC strength and muscle activity of the contralateral immobilized elbow flexors in a greater extent than concentric-/eccentriccoupled resistance training. These results were in line with the hypothesis and suggest that the resistance training with high-intensity eccentric contractions is an effective strategy to minimize negative effects of immobilization in clinical setups.

F I G U R E 4 Normalized changes (mean ± SD) in elbow flexion joint position sense error for the immobilized arm (A) and non-immobilize arm (B) from baseline to the post-immobilization for individual participants and their average ± SD values of the control group (CTRL), concentric-/eccentric-coupled resistance training group (CON-ECC), and eccentric resistance training group (ECC). † Significant difference from baseline to post-immobilization. *Significant difference in comparison with the CTRL group

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4.1 | Immobilization effects In the present study, the 4 weeks of immobilization induced large decreases in muscle strength (MVIC: −21.7%, concentric 1-RM: −14.4%), RFD (RFD50: −25.7%; RFD100: −24.1%; RFD200: −21.0%), and upper arm circumference (−5.1%), and an increase in the error for elbow flexion JPS (87.4%) when compared to the baseline (Table 2). These were accompanied by a decrease in voluntary muscle activity of the biceps brachii during the MVIC strength measure (sEMGRMS: −35.2%). It should be noted that the upper arm circumference measure is a limitation as a surrogate of muscle size change; however, the test-retest reliability of this measure was high (eg, CV = 0.9%); thus, the decrease in the circumference in the immobilized arm was considered to indicate muscle atrophy. The changes in the variables after immobilization in the CTRL were comparable to those found after immobilization in the previous studies.6,10,18 For example, Yue et al18 showed that 4 weeks of arm sling immobilization of healthy young adults induced large decreases in MVIC strength (−35%), muscle activity (−43%), and muscle cross-sectional area (−11%) of the elbow flexors. Pearce et al6 reported that 3 weeks of sling immobilization induced 20% decrease in elbow flexor dynamic strength, 5% decrease in muscle thickness, and 19% decrease in corticospinal excitability. Interestingly, the non-immobilized arm of the CTRL group also showed a decrease in RFD (Figure 3). It is possible that a decrease in RFD precedes a decrease in MVIC or 1-RM strength, thus could be used an early marker of a decrease in muscle function.16

4.2 | Effects of resistance training on the non-immobilized (trained) arm For the non-immobilized “trained” arm, ECC elicited greater increases in MVIC strength (20.9%; ES = 0.47), muscle activity (77.9%, ES = 0.90), RFD50 (53.3%, ES = 0.61), RFD100 (31.8%, ES = 0.71), RFD200 (26.9%, ES = 0.57), and arm circumference (2.9%, ES = 0.18) in comparison with CON-ECC (13.7%, ES = 0.29; 15.1%, ES = 0.21, 20.5%, ES = 0.45; 15.8%; ES = 0.21; 12.0%, ES = 0.22; 0.6%, ES = 0.04, respectively) (Table 2). No previous study has compared between eccentric-only and concentric-/eccentric-coupled resistance training using a matched training load design. However, Cirer-Sastre et al8 suggested possibly greater contralateral effects of eccentric-only in comparison with concentric-only or concentric-/eccentric-coupled resistance training due to the unique neuromuscular responses to eccentric contractions. Tseng et al14 showed that 5 sessions of progressive (10%, 30%, 50%, 80%, and 100% of MVC) eccentric-only resistance training of elbow flexors over 5 weeks induced

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8.4% greater increase in MVIC strength when compared to progressive concentric-only resistance training with the same intensities as those of the eccentric-only training.

Hortobágyi et al13 also reported that 12 weeks of knee extensor eccentric-only maximal isokinetic training induced 9% greater increase in MVIC strength when compared to concentric-only training. Thus, despite a lack of comparison between eccentric-only and concentric-only resistance training in the present study, it seems possible that eccentric-only may be more effective than concentric-only resistance training to induce strength gains in the trained muscles.

It should be noted that the eccentric-only training increased CON 1-RM and MVIC strength, which were not specific to the training mode. Hortobágyi et al13 reported that eccentric-only resistance training increased concentric strength, and concentric training increased eccentric strength in a similar extent.13 Although we did not measure eccentric strength specifically in the present study, it is assumed that eccentric strength was increased more after ECC than CON-ECC. The increase in sEMGRMS observed after eccentric-only training was in line with the results of the study by Hortobágyi et al13 who showed a greater increase in muscle activity (ie, amplitude of sEMG) of vastus lateralis after 12 weeks of eccentric-only (86%) than concentric-only resistance training (12%). Thus, the greater increase in MVIC after ECC than CON-ECC was possibly associated with the larger increase in sEMGRMS. It is important to note that the intensity was greater in the ECC than CON-ECC in the present study such that the load was 80%-120% of concentric 1-RM for ECC, but 60%-90% of concentric 1-RM for CONECC. It has been speculated that sEMG is increased more by eccentric than concentric training due to an increased descending drive during eccentric contractions.11,13 The improvements related to RFD could be attributed to a greater recruitment of fast twitch motor units by eccentric contractions.26 Thus, it may be that eccentric resistance training can increase type II fiber recruitment more than concentric-/eccentric-coupled resistance training to enhance the RFD capacity.27,28 Furthermore, it has been reported that eccentric resistance training induces ipsilateral increases in corticospinal excitability and reductions on intracortical inhibition accompanied by increases in antagonist muscle inhibition.28 Although the present study did not include neurophysiological measures (eg, corticospinal excitability and inhibition), the increases in MVIC strength and RFD could be at least partially explained by the greater increases in sEMGRMS in the trained arm after ECC than CON-ECC (Figures 2 and 3, respectively). The upper arm circumference also showed greater increases for the ECC than CON-ECC group, despite the short training period (Figure 1). However, it should be considered that the greater increases in the circumference for the ECC than the CON-ECC groups may be related to muscle

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inflammation evoked in a greater extent by the higher intensity eccentric contractions of the last training session.14,29 Interestingly, elbow flexion JPS was improved after both ECC (ES = −0.64) and CON-ECC (ES = −0.68) (Figure 4).

It has been shown that exercise can enhance proprioception by modulating the sensitivity of muscles proprioceptors.30 Although the mechanisms underpinning the effect of resistance exercise on proprioception have not been identified, voluntary contractions have been shown to enhance the proprioceptive ability due to the stimulation of muscle spindles and Golgi tendon organs.17 In the training protocols, the elbow joint was extended to a full ROM with heavy loads for both groups; thus, it is possible that both training protocols were effective for stimulating muscle proprioceptors and joint mechanoreceptors similarly, which enhanced the JPS ability in response to both training modes.24 Overall, the magnitude of changes in the dependent variables was greater for the ECC than CON-ECC groups for the trained arm, suggesting that ECC could provide greater mechanical stimulus to the trained muscles when compared to CON-ECC.

4.3 | Effects of resistance training on the immobilized arm Regarding the contralateral training effects on the immobilized arm, ECC induced greater increases in MVIC (12.1%, ES = 0.29) and muscle activity (17.5%, ES = 0.31) in comparison with CON-ECC (−0.1%, ES = −0.18; −5.9%, ES = −0.15) that showed no changes over time in these variables (Table 2). It was a surprise that ECC increased the strength of the immobilized, non-trained arm. This could be attributed to the greater cross-education effect on the immobilized arm by ECC than CON-ECC as discussed below.

It is important that both ECC and CON-ECC prevented the deleterious effects of immobilization. No previous study has compared ECC and CON-ECC for the cross-education effect in relation to immobilization; however, some studies have shown effectiveness of both muscle contraction modes on immobilized arm. For example, Pearce et al6 reported that 3 weeks of traditional contralateral concentric-/eccentriccoupled resistance training of elbow flexors (50%-70% of 1-RM) maintained muscle strength (MVIC and concentric 1-RM) of the immobilized homologous muscles. This was in line with the findings of the present study. It seems likely that the greater cross-education effect was associated with the greater load used in the ECC than CON-ECC. Andrushko et al10 showed that 4 weeks of contralateral maximal isokinetic eccentric training of the wrist flexors maintained the muscle strength (average of isometric, concentric, and eccentric strength) of the immobilized homologous muscles. In the present study, the intensity was not maximal,

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although it was 80%-120% of concentric 1-RM for ECC, and the intensity was lower for CON-ECC (60%-90% of concentric 1-RM) than ECC. It may be that the use of dumbbell made the exercise more complex in motor task than isokinetic resistance training performed on a dynamometer, because load and velocity in the dumbbell exercise were needed to be controlled by the participant not by the dynamometer, which may have induced greater cortical activity.31,32 Furthermore, in two different studies, Farthing et al33,34 showed that complex tasks induced greater contralateral strength transfer when a hand grip and a ulnar deviation training were compared. It was speculated that complex task (ie, ulnar deviation) induced greater cortex activation with greater bilateral connections, which might have induced greater contralateral transfers.33,35 Magnus et al5 showed that 4 weeks of isometric contralateral resistance training of the elbow flexor and extensor muscles during sling immobilization resulted in 8% and 32% increases in MVIC strength for the contralateral immobilized elbow flexor and extensor muscles, respectively.

They speculated that the increases in the muscle strength in the immobilized arm were due to the activation of other muscles (eg, posterior deltoid and latissimus dorsi) during training. It is possible that high-intensity eccentric contractions co-activated other muscles greater, which might contribute to the increases in the muscle strength of the immobilized arm after ECC. The present study found that both ECC and CON-ECC induced a sparing effect for RFD and elbow flexion JPS in the immobilized arm. To the best of our knowledge, no previous studies have reported changes in these variables using contralateral training with immobilization. It is known that RFD is influenced by neural (eg, increases in central descending motor drive, motor neuron excitability, and motor unit firing rates) and muscular factors (eg, increases in muscle fiber area and type).36 The present study also found that JPS of the immobilized arm was maintained similarly after ECC and CON-ECC. It is possible that contralateral training improves motor engrams, which may explain the maintenance of JPS on immobilized arm in both training groups. It seems possible that associated contralateral contractions (ie, neural mirror activity) during training also produced sufficient stimulation to muscle proprioceptors and cortical representation in the ipsilateral hemisphere to maintain the elbow flexion JPS ability in the immobilized arm.37 These speculations should be investigated in future research.

The mechanisms underpinning the contralateral effect are likely to be associated with neural and muscular adaptations.38 The neural adaptations include cortical cross-activation and bilateral access.35,38 The cortical cross-activation means that an unilateral muscle contractions drives a bilateral cortical activation that induces neuroplasticity changes in both trained and non-trained cortical hemispheres.35 The bilateral access

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is that motor learning process occurs in response to unilateral training and could generate an enhanced motor unit recruitment, including inhibition of antagonists and coordination of synergist muscles, which could later be used by the trained and non-trained limbs. Supporting the neural adaptations, Kidgell et al12 showed that 4-week eccentric-only training induced 51% greater contralateral corticospinal excitability (ie, motor evoked potentials amplitude) than concentric-only (13%) training of the wrist flexor muscles and found 32% greater reductions in the short-interval intracortical inhibition (SICI) and 15%-27% reduction in corticospinal inhibition (ie, silent period duration) in the non-trained hemisphere when compared to concentric training (2% and 4%-8%, respectively). However, Manca et al39 reported that corticospinal excitability (ie, motor evoked potentials) and sEMG played a limited role in the interlimb transfer effect, but showed that SICI and silent period in the non-trained hemisphere were more strongly involved in the cross-education effect in the contralateral limb. Taken together, it seems possible that contralateral eccentric-only training modulated the corticospinal and intracortical inhibition to a greater extent than the coupled CON-ECC training. Contralateral muscular adaptations may be explained by endocrine factors that modulate protein synthesis and degradation in the contralateral muscles inducing muscle growth after contralateral resistance training.38 However, this may not be the main factor in the present study, since no increase in arm circumference was observed for the immobilized arm, but still induced large increases in muscle strength. It is also important to consider that arm circumference is only a gross marker of arm volume and is not able to distinguish between different soft tissues. Further studies are warranted to investigate the mechanisms underpinning the greater effects of ECC than CON-ECC on the immobilized muscle. It is interesting to investigate whether any difference exists between eccentric-only and concentric-eccentric contractions when the intensity for eccentric contractions is the same.

4.4 | Limitations One of the limitations of the present study was that we did not monitor muscle activities in training sessions. It is possible that the elbow flexor muscle activity of the immobilized arm during training was greater for ECC than CON-ECC due to the heavier loads used in ECC, which might have evoked greater contralateral-associated contractions. We only used surface EMG during MVIC measures, which is a gross marker of muscle activity and does not determine the provenance (eg, supraspinal or spinal) of the neural adaptations, and we did not normalize the sEMG to a maximal evoked response. In the present study, the immobilization was limited to 8 hours a

day, and we did not monitor the activities of the immobilized and non-immobilized arms during the immobilization period.

However, the CTRL group demonstrated that the immobilization affected all of the outcome measures negatively to a large extent. It is interesting to repeat the present study by using a full immobilization with monitoring muscle activities of the immobilized and non-immobilized arms during the immobilization. Other muscles than the elbow flexors such as wrist muscles or leg muscles such as plantar flexors and knee extensors and flexors should be investigated in future studies. Moreover, we did not include a concentric-only group, in which the total volume is matched to the other groups and/or using heavier loads than those in CON-ECC. It is interesting to compare eccentric-only, concentric-only, and concentriceccentric contractions with the same load for their effects on muscle function and size of the immobilized limb.

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| CONCLUSION

A 4-week sling immobilization induced 5% atrophy and 22% decrease in MVIC strength together with decreased muscle activity, concentric 1-RM strength, RFD, and joint position sense ability for the immobilized arm. However, these changes were attenuated by ECC-only and CON-ECC-coupled resistance training of the non-immobilized arm, and the effects were greater for ECC-only than CON-ECC-coupled resistance training. It is concluded that performing resistance training consisting of eccentric contractions in the contralateral non-immobilized arm is effective for minimizing the negative effects of immobilization.

Contralateral heavy eccentric resistance training appears to be a better option than concentric-/eccentric-coupled resistance training to maximize the contralateral effects related to strength and muscle activation during immobilization. However, it should be noted that coupled concentric-eccentric contractions (with shortening and lengthening contractions cycles) may be easier to be implemented in a clinical setting, since practitioners (eg, physiotherapists, personal trainers) are more familiar with coupled concentric-eccentric resistance exercises, when compared to eccentric-only resistance exercises. Thus, more studies are warranted to investigate whether eccentric-only resistance training is feasible in a clinical setting and effective for clinical conditions such as stroke or musculo-skeletal injuries. It is also necessary to investigate the mechanisms underpinning the greater contralateral effects by eccentric than concentric or concentric-/eccentric-coupled resistance training.

5.1 | Perspectives It is clear from the results of the present and previous studies that negative effects of immobilization on muscle function

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and atrophy can be minimized by resistance exercise training of non-immobilized homologous contralateral muscles.

The present study showed that resistance exercise training consisting of high-intensity eccentric contractions was more effective for minimizing and eliminating the negative effects of immobilization than traditional resistance exercise training. Thus, it can be recommended from the present study results that it is better to use high-intensity eccentric contractions to increase cross-education effects on immobilized elbow flexors at least. Future studies should focus on developing training modalities that minimize the negative effects of immobilization on muscle function and muscle atrophy in a clinical setting. In addition to the type of muscle contractions, training device (eg, free-weight vs isokinetic), load (intensity, volume), and complexity of task (cognitive demand) should be considered when contralateral effect is to be maximized. It is interesting to apply eccentric resistance exercise training for clinical immobilization cases to start examining its effects on muscle function and size of the immobilized limb.

CONFLICT OF INTEREST All authors declare that they have no conflict of interest.

ORCID Kazunori Nosaka https://orcid. org/0000-0001-7373-4994 Luis Penailillo https://orcid.org/0000-0001-7697-9700 R E F E R E NC E S

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How to cite this article: Valdes O, Ramirez C, Perez F, Garcia-Vicencio S, Nosaka K, Penailillo L. Contralateral effects of eccentric resistance training on immobilized arm. Scand. J. Med. Sci. Sports.

2020;00:1–15. https://doi.org/10.1111/sms.13821