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Dr Mouwafak Majeed Mola Documents | 2012-2013

‫سلسلة الدكتور موفق مجيد المولى لتطوير الفكر البحثي العربي‬ ‫الرياضي‬

‫مصادر الباحث العلمي في رياضة‬ )1(‫الجمناستك‬ Special Project coordinator – Aspire Academy member of Development Committee – QFA Mouwafak Majeed Mola

2013-2012

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Dr Mouwafak Majeed Mola Documents | 2012-2013

Distal radius geometry and skeletal strength indices after peripubertal artistic gymnastics J. N. Dowthwaite and T. A. Scerpella Author information ► Copyright and License information ► The publisher's final edited version of this article is available at Osteoporos Int See other articles in PMC that cite the published article.

Go to: Abstract Summary Development of optimal skeletal strength should decrease adult bone fragility.

Nongymnasts (NON) were compared with girls exposed to gymnastics during growth (EX/GYM), using peripheral quantitative computed tomography (pQCT) to evaluate postmenarcheal bone geometry, density, and strength. Pre- and perimenarcheal gymnastic loading yields advantages in indices of postmenarcheal bone geometry and skeletal strength.

Introduction Two prior studies using pQCT have reported bone density and size advantages in Tanner I/II gymnasts, but none describe gymnasts‘ bone properties later in adolescence. The current study used pQCT to evaluate whether girls exposed to gymnastics during late childhood growth and perimenarcheal growth exhibited greater indices of distal radius geometry, density, and skeletal strength.

Methods Postmenarcheal subjects underwent 4% and 33% distal radius pQCT scans, yielding: 1) vBMD and cross-sectional areas (CSA) (total bone, compartments); 2) polar strength-strain index; 3) index of structural strength in axial compression.

Output was compared for EX/GYM vs. NON, adjusting for gynecological age and stature (maturity and body size), reporting means, standard errors, and significance.

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Results Sixteen postmenarcheal EX/GYM (age 16.7 years; gynecological age 3.4 years) and 13 NON (age 16.2 years; gynecological age 3.6 years) were evaluated. At both diaphysis and metaphysis, EX/GYM exhibited greater CSA and bone strength indices than NON; EX/GYM exhibited 79% larger intramedullary CSA than NON (p<0.05). EX/GYM had significantly higher 4% trabecular vBMD; differences were not detected for 4% total vBMD and 33% cortical vBMD.

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Conclusions Following pre-/perimenarcheal gymnastic exposure, relative to nongymnasts, postmenarcheal EX/GYM demonstrated greater indices of distal radius geometry and skeletal strength (metaphysis and diaphysis) with greater metaphyseal trabecular vBMD; larger intramedullary cavity size was particularly striking.

Keywords: Adolescence, Bone geometry, Bone strength, Female, Mechanical loading, pQCT Go to: Introduction Artistic gymnastics provides a prime model of mechanical loading, generating forces of up to ten times body weight [1] via extreme weight bearing and impact loading. Dual energy X-ray absorptiometry (DXA) studies have shown high areal bone mineral density (aBMD) and bone mineral content (BMC) in gymnasts [2–9].

However, DXA does not measure bone cross-sectional geometry, or volumetric bone mineral density (vBMD); thus, results cannot distinguish bone size differences from bone density differences. In addition, DXA yields mean aBMD and BMC; it does not assess cross-sectional bone architecture or compartmental vBMD. In contrast, peripheral quantitative computed tomography (pQCT) assesses cross-sectional bone geometry and compartmental density, characterizing bone size, tissue distribution, and vBMD. However, because pQCT samples a narrower region of interest, care must be taken in positioning scans, particularly across the variable metaphyseal region.

Recently, our group applied formulae to distal radius DXA data from premenarcheal females, deriving bone mineral apparent density (BMAD) as well as indices of bone geometry and skeletal strength [10–12]. Gymnast vs. nongymnast comparisons indicated significantly greater bone size and mass in gymnasts, yielding greater indices of metaphyseal and diaphyseal bone strength.

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Gymnast BMAD was greater only at the metaphysis. Results suggested that gymnastic loading increases bone size and vBMD in a site-specific manner, as previously shown in racquet sport models [13–15]. However, DXA-derived indices rely upon geometric simplifications to approximate cross-sectional geometry and vBMD [10].

Because gymnastics loads the forearm in a manner that is not duplicated by other activities, the radius provides an indication of skeletal adaptation to weight bearing and impact loading [10, 16]. In addition, the radius contains regions of cortical (diaphyseal) and corticocancellous (metaphyseal) composition, allowing assessment of bone tissue-specific adaptation using pQCT [10] (Fig. 1). Few publications have reported pQCT-measured bone properties in gymnasts and nongymnasts [16–20]. Most have evaluated the radius in prepubertal and/or early pubertal subjects. One study (recently published by our group) focused on the explanatory value of muscular indices [muscle cross-sectional area (CSA) and arm fat-free mass (FFM)] vs. gymnastic exposure for radius outcomes in postmenarcheal girls, without characterizing bone outcomes for gymnasts relative to nongymnasts [16]. Another publication has identified significant advantages for pQCT parameters in adult former gymnasts compared with age-matched nongymnasts [20]. In the present analysis, we tested the hypothesis that gymnastics exposure from late childhood through menarche is linked to greater indices of bone geometry, density, and theoretical strength after menarche. We expected that advantages in cortical CSA would predominate at the diaphysis and that advantages in trabecular vBMD would predominate at the metaphysis.

Fig. 1 For 33% diaphysis (a, c) and 4% metaphysis (b) sites, sample pQCT scans are presented, indicating bone compartments in gymnasts and nongymnasts. For both sites, the ―total‖ compartment includes both cortical and intramedullary/trabecular (more ...)

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Dr Mouwafak Majeed Mola Documents | 2012-2013

Methods Postmenarcheal subjects from an ongoing longitudinal study of gymnastics-related bone accrual were recruited to undergo pQCT scans of the distal radius.

Subjects/guardians provided written assent/consent using a document approved by the SUNY Upstate Medical University Institutional Review Board, in compliance with the US bioethical legislation and the Declaration of Helsinki. Gymnasts/exgymnasts (EX/GYM) were defined as girls who had participated in at least 5 h per week (hours per week) of gymnastic activity for at least 2 years between age 8 years and menarche, including both elite and nonelite gymnasts. All subjects within the EX/GYM group had participated in gymnastics through early puberty or later (to at least 4 months premenarche). Subjects who discontinued gymnastics at an earlier maturity phase were excluded from analyses (n=3, ceased gymnastics 4.7, 1.8, and 1.7 years premenarche). This ensured that all subjects in the EX/GYM group were exposed to gymnastics in the context of increasing estrogen exposure, coincident with accelerated perimenarcheal bone mineral accrual [21].

All subjects had participated in the longitudinal DXA study for the previous 5–10 years [8]. Nongymnasts were recruited from local private schools, athletic groups, and the university community. At initial enrollment, nongymnasts were matched for age, maturity, and body size to gymnasts from local clubs (future ex-gymnasts n=6 and gymnasts n= 10). Semiannual data were collected, as follows [8]. Stature (in centimeters) was measured using wall-mounted rulers. Calcium intake was assessed using food frequency questionnaires; estimated mean intake was calculated for the period 18 months prior to and including the pQCT scan. Selfassessed Tanner breast stage was recorded. Gynecological age (years postmenarche) was calculated relative to self-reported menarche date. Annual means for self-reported gymnastic activity (current gymnasts only) and total weight-bearing activity (nongymnasts and ex-gymnasts) were calculated for the year up to and including the pQCT scan, based on semiannual questionnaires.

Early in the longitudinal study, gymnasts‘ self-reported annual physical activity means were validated against coaches‘ training logs (r>0.97, p<0.001, unpublished results).

Densitometric data were analyzed from a single session of contemporaneous DXA and pQCT scans. A whole-body DXA scan [Hologic QDR 4500W, software 8.26a, coefficient of variation (CV) <1.0%] measured total body FFM (in kilograms).

Forearm pQCT scans were performed on the nondominant arm (Norland-Stratec

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XCT 2000). Machine in vivo forearm pQCT scan precision was determined in an unrelated adult sample at the 4% metaphysis and 30% diaphysis. Using the analysis protocol detailed below, coefficients of variation for pQCT parameters were as follows: metaphyseal total CSA=2.44%; metaphyseal total vBMD=2.15%; metaphyseal trabecular CSA=3.41%; metaphyseal trabecular vBMD=1.21%; metaphyseal cortical-subcortical CSA=2.29%; metaphyseal IBS=2.22%; diaphyseal total CSA=0.96%; diaphyseal total vBMD= 0.50%; diaphyseal corticalsubcortical CSA=0.94%; diaphyseal cortical vBMD=0.63%; diaphyseal IMCSA=2.34%; diaphyseal polar SSI=2.96%.

Scout views were performed for reference line placement (Fig. 2). For metaphyseal assessments, scans were performed at 4% of ulnar length from the reference line, set at the proximal border of the physis or physeal scar on the ulnar side of the radius [22]. Positioning relative to the physis has been recommended to improve agreement of metaphyseal scans between individuals, as the degree of metaphyseal inwaisting and maturity of bone tissue varies according to distance from the physis [23–25]. Ulnar length (mm) was measured from the olecranon to the ulnar styloid with a ruler and rounded to the nearest 5 mm increment (CV=4%). To assess metaphyseal bone geometry and vBMD throughout the bone cross-section, 4% scans were analyzed based upon vBMD thresholds (contour mode 3, peel mode 4, inner threshold 450 g/cm3, threshold 169 mg/cm3, and peel by 5%) [22]. This contrasts with analysis modes that only analyze the central 45% of the trabecular compartment [24]. For diaphyseal assessments, scans were performed at 33% of ulnar length from a distal articular reference (Fig. 2), as this region of interest is less variable, and the tissue is more uniformly mature than at the metaphysis [22– 25]. For analysis of 33% region scans, we used analysis modes as previously reported (CALCBD: contour mode 1, peel mode 2, inner threshold 540 mg/cm3, threshold 711 mg/cm3; CORTBD and strength-strain index (SSI): threshold 711, separation mode 2) [22]. Cortical vBMD was measured at the 33% site; mean cortical thickness exceeded 2.5 mm (>4 mm), limiting the influence of partial volume effects [23].

Fig. 2 A scout view is shown to depict pQCT scan reference line placement for 33% scans (articular reference, A) and 4% scans (physeal/scar reference, B)

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Cortical thickness may be low at the 4% site and therefore more strongly influenced by partial volume effects [23]. Nonetheless, 4% cortical CSA was measured for comparison with other studies [15, 26]. Similarly, the utility of total vBMD has been questioned as a meaningful index of bone strength at the diaphysis, and we note that total vBMD may vary independently of bone strength indices, depending upon the underlying bone geometric adaptation. For example, high cortical CSA combined with low intramedullary CSA is associated with thick cortices, yielding high total vBMD and SSI. In contrast, high cortical CSA combined with high intramedullary CSA may be associated with relatively thin cortices, yielding low total vBMD but high SSI. It is important to consider this phenomenon when interpreting DXA areal BMD for the radial diaphysis, as it may mask differences in theoretical bone strength and hamper evaluation of fracture risk. Therefore, we report diaphyseal total vBMD results to illustrate this underlying variability and yield a means of comparison with other skeletal sites. To evaluate metaphyseal bone strength, index of structural strength in axial compression (IBS) was calculated as total CSA×vBMD2 (elsewhere, bone strength index) [15, 22, 23, 27]. To assess theoretical resistance to fracture in the event of a low trauma fall, fall strength was calculated using polar SSI (33%) or IBS (4%) divided by the product of forearm length and total body weight (fall SSI, fall IBS)[10, 22, 25, 28]. Throughout the paper, cortical vBMD represents the mean vBMD for the cortical compartment only, whereas cortical CSA represents cortical/subcortical cross-sectional area (such that total CSA=intramedullary CSA + cortical CSA).

Variables were screened for normality; natural logarithmic transformation was applied to nonnormal distributions [33% intramedullary cross-sectional area (IMCSA) only]. To evaluate bone traits attributed to gymnastic loading during growth, gymnasts and ex-gymnasts were grouped together (EX/GYM) for comparison against nongymnasts (NON). To specifically evaluate the influence of gynecological age on physeal (4% reference) location and bone outcomes, Pearson correlations were applied to all outcomes except 33% IMCSA (Spearman correlations, ln-transformed data; alpha=0.05). To account for potential variation in biological maturity and body size, analysis of covariance (ANCOVA) adjusted for gynecological age and stature, accounting statistically for the linear correlations between these covariates and each outcome. The resultant adjusted means, standard errors, effect sizes (Cohen‘s d [29]) and significance are reported (alpha=0.05).

Power analyses were based on forearm areal BMD comparisons for ex-gymnasts vs. nongymnasts at approximately 18 months postmenarche, in order to gauge

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effect sizes for maturity-specific group differences [30]. On this basis, minimum cell size for 80% power was determined to be seven; cell sizes of n=16 and n=13 were deemed adequate to detect significant differences if effect sizes were similar for pQCT and DXA differences. Post hoc power analyses using the pQCT comparisons of Eser et al. (2010, [20]) indicate that cell sizes of n=16 and n=13 should be adequate to detect significant differences for total CSA (4% and 66%/33%), 66%/33% medullary CSA, and 66%/33% SSI with 80% power [31].

However, to detect differences of Eser‘s observed magnitude, cell sizes of 33 to 63 would be required for 4% trabecular vBMD and 66% cortical CSA and cortical vBMD; cell sizes of over 2,000 would be required for 4% total vBMD (80% power).

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Go to: Results Subjects included 16 EX/GYM and 13 NON, with a mean chronological age of 16.5 years (13.3 to 20.4 years) and a mean gynecological age of 3.5 years (0.25 to 7.3 years). During 5 to 8 years of observation prior to the pQCT scans, all subjects reported normal health, barring occasional sports injuries. NON and EX/GYM were well matched, only differing significantly by physical activity history (see Table 1). Self-assessed Tanner breast stage distributions were not significantly different between groups (NON TB3= 15%, TB4=31%, TB5=54%; EX/GYM TB3=19%, TB4=44%, TB5=38%). Rates of oral contraceptive use were similar between groups [NON 3/13 (23%); EX/GYM 2/16 (13%)]. All subjects were white except one nongymnast (1 Asian). All EX/GYM were exposed to gymnastics prior to puberty and continued gymnastics to at least 4 months before menarche. The majority of EX/GYM continued gymnastics up to or beyond menarche (81%), with mean exposure to 1.25 years post-menarche [standard deviation (SD)=1.3 years].

All EX/GYM had participated in gymnastics (>5 h/week) for at least 2 of the past 10 years (3–9 years). The grand mean for gymnastic participation per year of gymnastic activity (mean of all annual means of all EX/GYM) was 13.3 h/week (6.6–17.9 h/week). Ex-gymnast gymnastic exposure (at level ≥5 h/week) averaged 5.1 years (SD=1.7, 3–8 years), at an average of 13.7 h/week (SD=3.2, 10–17.9 h/week). Current gymnasts had been exposed to gymnastics (at level ≥5 h/week) for 6.1 years (SD=1.5, 4–9 years), at an average of 12.9 h/week (SD=3.0, 6.6–16.1 h/week).

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Table 1

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Subject characteristics by gymnastic exposure group Nongymnasts were active in various physical activities during late childhood and perimenarcheal growth; most participated in multiple activities in a given year.

Similarly, ex-gymnasts also participated in a variety of activities after cessation of gymnastic training (during peri-/postmenarcheal growth). For the year prior to the pQCT scan, nongymnasts and ex-gymnasts did not differ for annual mean weightbearing activity (Table 1, p=0.64).

For the pQCT scans, quality was generally high; nonetheless, for the 33% site, two scans were excluded for movement errors (one gymnast, one nongymnast). For the 4% site, reference distance (distance of scan reference line from articular surface) was correlated with gynecological age (r=+0.45, p<0.02); there was a strong trend for a positive correlation between gynecological age and 4% scan distance (distance of scan site from the articular surface, r=+0.31, p<0.11). Forearm length, 4% reference distance, and 4% scan distance were compared for EX/GYM and NON. There were no significant gymnastic group differences in any of these parameters by analysis of variance (ANOVA) or ANCOVA adjusting for gynecological age (although for scan distance from the articular reference, ANOVA p=0.07, ANCOVA p=0.05, EX/GYM > NON).

Diaphysis, 33% site At the diaphysis, EX/GYM adjusted means were higher than NON for total, cortical, and intramedullary CSA (p<0.005; Table 2, pFigs. 1a, c and and3).3).

Accordingly, SSI and fall SSI were higher in EX/GYM than NON (ANCOVA <0.001). Conversely, NON had higher 33% total vBMD than EX/GYM (ANCOVA p<0.02); significant differences in 33% cortical vBMD were not detected (p>0.30). Gynecological age correlated with total and cortical vBMD (r=+0.43, p< 0.02; r=+0.79, p<0.000, respectively), acting as a significant

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covariate for these parameters. No other diaphyseal parameter correlated with gynecological age, but lnIMCSA suggested a negative trend (rho=−0.32, p=0.11).

Dr Mouwafak Majeed Mola Documents | 2012-2013

Table 2

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Adjusted bone parameters by gymnastic exposure group (ANCOVA)

Fig. 3 Percent advantages for ex/gymnasts relative to nongymnasts are depicted for each pQCT parameter at the 33% site. Means are adjusted for gynecological age and height; bars represent 95% confidence intervals. For all parameters, ANCOVA p<0.05, except (more ...)

Metaphysis, 4% site At the metaphysis, compared with NON, EX/GYM adjusted means were higher for CSA (total, trabecular, and cortical/subcortical compartments), SSI, fall SSI, and IBS (ANCOVA p<0.03; Table 2, pFigs. 1b and and4).4). Trabecular vBMD was also higher in EX/GYM than NON (ANCOVA <0.03), but differences in total vBMD were not detected (small effect size d=0.21). Gynecological age was positively correlated with total vBMD, IBS, and IBS fall strength (r=+0.64, p< 0.000; r=+0.51, p=0.005; r=+0.42, p<0.03, respectively). In contrast, gynecological age was negatively correlated with total CSA and trabecular CSA (r=−0.38, p< 0.05; r=−0.46, p<0.02, respectively). Gynecological age was a significant covariate for 4% total CSA, total vBMD, trabecular CSA, and IBS.

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Fig. 4 Percent advantages for ex/gymnasts relative to nongymnasts are depicted for each pQCT parameter at the 4% site. Means are adjusted for gynecological age and height; bars represent 95% confidence intervals. For all parameters, ANCOVA p<0.05, except (more ...)

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Dr Mouwafak Majeed Mola Documents | 2012-2013

Discussion In these postmenarcheal girls, distal radius bone size and strength were at least 20% greater for EX/GYM compared with NON, at both metaphyseal and diaphyseal sites. At the diaphysis, gymnastic loading was associated with marked intramedullary cavity expansion and moderate cortical shell expansion, reflected by lower total vBMD in EX/GYM compared with NON (no cortical vBMD difference was detected). Similarly, at the metaphysis, EX/GYM did not exhibit an advantage over NON for total vBMD, despite trabecular vBMD and cortical CSA advantages of approximately 20%. Overall, exposure to pre- and perimenarcheal gymnastic loading was associated with greater theoretical bone strength; this advantage resulted from larger bone geometry at both diaphyseal and metaphyseal sites, with unaltered cortical vBMD and high metaphyseal trabecular vBMD. Our group has previously noted that both high mineral content and efficient mineral distribution underlie gymnast advantages in bone geometry and bone strength indices [10, 16].

Aside from our muscle index work [16], studies by Dyson, Ward et al., and now Eser et al. (2010) are the only published reports that have used pQCT to compare the radii of gymnasts and nongymnasts [17–20]. In contrast to our postmenarcheal subjects, both Dyson and Ward et al. evaluated subjects who were, on the whole, prepubertal (Ward et al.=Tanner I at baseline; Dyson et al.=majority Tanner I/some Tanner II) [17–19]. Our EX/GYM and the adult ex-gymnasts of Eser et al. [20] were also exposed to gymnastic loading during late childhood/early puberty, but loading exposure was extended, continuing into perimenarcheal growth. This additional loading, over a more advanced maturational phase, would be expected to either increase gymnast/nongymnast differentials or induce maturity-specific differences.

At the metaphysis, our postmenarcheal results contrast with Dyson/Ward premenarcheal results and are similar to those of Eser et al. [17, 18, 20].

Specifically, differentials varied for metaphyseal total CSA and vBMD. Dyson‘s

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premenarcheal results suggested some gymnast advantage in total CSA over nongymnasts, although the differential was smaller than observed postmenarcheal advantages (gymnast advantage, Dyson=11%, not significant (NS); EX/GYM=26%, p<0.05; Eser=25%, p<0.05) [17, 20]. In contrast, Ward‘s gymnasts and nongymnasts did not differ for total CSA (gymnast advantage, Ward=−0.4%, NS) [18]. For total vBMD, both Dyson and Ward et al. reported significant premenarcheal gymnast advantages, whereas no significant postmenarcheal difference has been detected (Dyson=20%; Ward=17%; EX/GYM=3%, NS; Eser=−1.1%, NS) [17, 18, 20]. For trabecular vBMD, Dyson‘s and Ward‘s premenarcheal gymnasts demonstrated greater advantages than either postmenarcheal cohort (Ward=21%; Dyson=27%; EX/GYM= 19%, p<0.05; Eser=9%, NS; absolute differences: 40–44 mg/cm3 vs. 12–17 mg/cm3) [17, 18, 20].

We observed a gymnast advantage in trabecular compartment CSA. Dyson et al. noted similar findings in their discussion, but Dyson, Ward, and Eser et al. do not report trabecular CSA results for comparison [17, 18, 20].

At the metaphysis, discrepancies between pre- and postmenarcheal results may stem from at least two hypothetical sources. Relative to prepubertal loading, continued gymnastic loading during puberty may have induced greater metaphyseal expansion in all compartments. This emphasis on geometric expansion may limit total vBMD advantages due to wider distribution of bone mass, so that prepubertal advantages in vBMD appear larger. In addition, during puberty, nongymnasts may have experienced maturity-specific increases in total vBMD, partially offsetting earlier loading advantages in postmenarcheal gymnasts.

Eser et al. examined adult ex-gymnasts to specifically evaluate maintenance of benefits 3+years after discontinuation of gymnastics (mean 6 years; 3–18 years).

Their metaphyseal vBMD advantages were lower than advantages in the younger pre- and postmenarcheal gymnast/ex-gymnast cohorts, suggesting partial deterioration of benefits after gymnastic cessation [20].

Ward et al. reported significant advantages in diaphyseal parameters at the 50% midradius in their premenarcheal cohort of girls and boys. However, compared with postmenarcheal gymnast advantages, Ward‘s gymnast advantages were lower for total CSA (Ward=9%, p<0.05; EX/GYM= 32%, p<0.05; Eser=32%, p<0.05), cortical CSA (Ward= 8%, p<0.05; EX/GYM=22%, p<0.05; Eser=13%, p<0.05), and intramedullary CSA (Ward=10%, NS; EX/GYM=79%, p<0.05; Eser=56%, p<0.05), particularly compared with our EX/GYM [18, 20]. In our postmenarcheal cohort, the large advantages in intramedullary cavity expansion are particularly striking. This differential is corroborated in the adult sample of Eser et al. [20], but it is not significant in Ward‘s mixed cohort of prepubertal males and females [18].

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The coupling of large intramedullary cavities with large periosteal cross-sectional areas occurs with peripheral distribution of diaphyseal BMC from the bone centroid. Theoretically, this efficient and effective adaptation yields higher bending/torsional strength independent of BMC, increasing skeletal strength even if mineral resources are limited (mean calcium intake <1,200 mg).

On the whole, discrepancies between Ward‘s and Dyson‘s Tanner I/II comparisons and the postmenarcheal results of our group and Eser et al. [10, 18, 20] suggest a heightened geometric response to mechanical loading during perimenarcheal growth. However, the noted discrepancies may also be partially attributed to site difference (50% vs. 33% and 66%) and/or Ward‘s representation of males and females. Alternatively, in Ward‘s and Dyson‘s younger subjects, loading exposure may have been too short to accumulate the high levels of adaptation observed in postmenarcheal subjects. Further research is necessary to examine the relative importance of mechanical loading during specific developmental phases.

Loading-enhanced geometric expansion has been described in other populations [13–15, 26, 32]. In particular, adult females exposed to weight lifting (WTLIFT) for 6.5 to 14 years (apparently postmenarche) exhibited similar patterns and magnitudes of distal radius adaptation to our postmenarcheal EX/GYM [26].

Diaphyseal advantages were comparable for cortical CSA (WTLIFT=26%, EX/GYM=25%; unadjusted WTLIFT=16.4mm2, EX/GYM=20.9mm2) and cortical vBMD (WTLIFT =−0.3%, EX/GYM =−0.7%; unadjusted WTLIFT=−3.7 mg/cm3, EX/GYM=−11.1 mg/cm3). For the metaphysis, EX/GYM loading advantages were similar to weight lifters for total CSA (WTLIFT=19%, EX/GYM=26%; unadjusted WTLIFT=45.1 mm2, EX/GYM=48.5 mm2) and SSI (WTLIFT=41%, EX/GYM=43%; unadjusted WTLIFT=91.6 mm3, EX/GYM =112.4 mm3) but were slightly lower in EX/GYM for cortical CSA (WTLIFT=38%, EX/GYM=25%; unadjusted WTLIFT=27.4 mm2, EX/GYM=15.7 mm2). In contrast, EX/GYM trabecular vBMD relative and absolute advantages were more than double the weight lifter advantages (WTLIFT=9%, EX/GYM=19%; unadjusted WTLIFT=17.8 mg/cm3, EX/GYM= 40.4 mg/cm3). Unfortunately, intramedullary CSA was not reported for comparison [26].

Bone geometric advantages have also been reported for the playing vs. nonplaying arm in postmenarcheal racquet sport players (mean ages 14.5 to 26.5 years.), with lower advantages than in our postmenarcheal EX/GYM [13–15]. Compared with postmenarcheal tennis players (started tennis premenarche), EX/GYM distal radius advantages were two to ten times higher than playing arm advantages for diaphyseal radius cortical geometry [14, 15] and diaphyseal radius/humerus total

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geometry [13–15]. At the radial metaphysis, EX/GYM advantages for trabecular vBMD and strength (IBS) were 2.5 to four times the playing arm advantage in older tennis players [15]. EX/GYM advantages in distal radius diaphyseal strength were 1.5 to three times greater than playing arm advantages at the diaphyseal humerus [13, 15].

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Trends toward differences in cortical vBMD were strikingly similar for comparisons involving tennis players (playing vs. nonplaying arm: 50% humerus −0.7%, NS [15]; distal humerus −2.2% [32]; distal radius −0.8% [33]), weight lifters (distal radius: −0.3%) [26], premenarcheal gymnasts (mid-radius: −0.9%, NS) [18], our postmenarcheal EX/GYM (distal radius: −0.7%, NS) and Eser‘s adult ex-gymnasts (proximal radius: −2.6%, p<0.05). These similarities imply minimal cortical vBMD adaptation in response to loading across maturational levels and loading modalities. Alternatively, because pQCT cannot discern variation in tissue microarchitecture or composition, it is possible that cortical vBMD adaptations to loading may have escaped detection in most studies. The results of Eser et al. suggest that mechanical loading may actually reduce cortical vBMD [20]; our study and the others discussed may have been under-powered to detect loading-related differences in cortical vBMD. Further human research is necessary to elucidate the nature of bone adaptation to loading at the microarchitectural level.

Overall, the large (79%) EX/GYM advantages in intramedullary canal dimensions are the most intriguing findings reported here (Fig. 1c). Furthermore, intramedullary CSA was hypervariable, as indicated by large confidence intervals for the gymnast advantage, suggesting genetic diversity for this parameter. This observation was corroborated by both Eser and Ward et al. In contrast, Ward et al. did not corroborate our large, significant EX/GYM advantages in intramedullary dimensions [18]. Certainly, sexual dimorphism may explain this disparity, as Ward‘s sample included both genders, and they discuss strong, nonsignificant trends toward both a sex interaction and a female gymnast advantage (+22%) [10, 18]. However, we surmise that discordance between our intramedullary results and Ward‘s is primarily due to maturity-specific variation in loading response, with midpubertal loading promoting intramedullary canal expansion. This hypothesis is supported by the results of Eser et al., which demonstrated large gymnast advantages in IMCSA. Nonetheless, within the limited maturity range represented by our subjects (gynecological age, 0.25 to 7.33 years), gynecological age was not significantly correlated with 33% radius IMCSA and did not act as a significant covariate in IMCSA ANCOVA. However, as our analyses did not include prepubertal girls, we cannot rule out a relationship between these variables across a

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broader maturational spectrum. Clearly, in our young postmenarcheal girls, the significant correlations between gynecological age and other bone outcomes highlight the importance of accounting for this variable in this maturity group.

Racquet sport athletes demonstrate variable advantages in intramedullary dimensions [14]. At the distal radius, Ducher et al. reported a moderate playing arm advantage in adult tennis players for intramedullary volume (MRI, 13.3%) [14]. In contrast, at the midhumerus, Bass et al. demonstrated playing arm advantages in IMCSA of only 3–4% in premenarcheal (pre/early pubertal) tennis players, with no advantage at the distal humerus [13]. Postmenarcheal comparisons (mean age 14.5 years) indicated smaller intramedullary dimensions in the loaded humerus at both distal and middiaphyses, leading Bass et al. to infer that peri- and postmenarcheal loading induce endocortical contraction [13]. In a study of adult racquet sport players (loaded premenarche), Kontulainen et al. detected no significant difference, but reported a trend toward lower mid-humeral intramedullary dimensions [15]. Corroborating results from all three studies, Haapasalo evaluated adult male tennis players, demonstrating no playing arm advantage at the midhumerus, but significant intramedullary expansion at the 30% radius (26%) [32]. Furthermore, comparisons of dominant arm advantages for players vs. controls indicated relative intramedullary expansion in the impactloaded radius (23%) but a trend toward relatively lower intramedullary expansion in the humerus [32]. Similarly, Eser‘s results in adult ex-gymnasts demonstrate no significant advantage in humeral intramedullary width (+3.9%, p>0.58), but cortical thickness was greater (+14.7%, p<0.0001); at the radius, ex-gymnasts had larger intramedullary cavities (56%, p<0.05), without thicker cortices (−4.6%, p>0.28) [20]. All of the above suggest a bone-specific response to loading, in which the humerus exhibits intracortical contraction or limited intramedullary expansion, contrasting with marked radial intramedullary expansion.

The large advantages in bone parameters exhibited by our EX/GYM are particularly striking because our sample is comprised of both elite and nonelite gymnasts. In addition, many EX/GYM (44%) are no longer active gymnasts; 31% of EX/GYM retired more than 5 years (5.4 to 7.6 years) prior to the pQCT scans, with recent physical activity patterns similar to those of the nongymnast group. Of the ex-gymnasts, all retired circum-menarche (4 months premenarche to 16 months postmenarche), suggesting that pre- and perimenarcheal gymnastic exposure may generate benefits that persist over the short to medium term, transcending continued growth and maturation. It is possible that greater benefits would be observed in elite gymnasts who maintain loading exposure throughout development. However, the similar scale of advantages demonstrated by the ex-

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gymnasts of Eser et al. suggests that postpubertal loading may not contribute substantively to adult benefits. It should be noted that artistic gymnastics provides an excellent model of mechanical loading but is not recommended as a widespread intervention to improve bone health.

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Limitations

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Caution should be exercised with respect to the interstudy comparisons made in this discussion, as different pQCT methodologies for scan placement and analysis may generate discrepant results. Scan position may be particularly influential for pQCT of the radial metaphysis. Specifically, we evaluated pQCT positional variation in the context of physical maturity. Gynecological age was positively correlated with 4% scan distance from the articular reference, suggesting continued physeal growth/bone lengthening in the early postmenarcheal years. Use of a physeal reference should have accounted for this maturational variability.

However, if developmental differences were inadequately addressed by this technique, girls of higher gynecological ages may have been measured closer to the diaphysis, lowering CSA results. Our adjusted results account for gynecological age, and by proxy, scan placement. Supplemental ANCOVAs, substituting scan distance for gynecological age, identified similar or larger gymnast advantages for all comparisons except fall IBS (p=0.14), supporting use of the physis/scar reference in this cohort. Finally, Eser‘s results, using an articular reference in older postmenarcheal subjects, corroborate our large gymnast advantages. In future work, the use of two metaphyseal scans may further improve reliability of metaphyseal assessment [34].

The relatively small number of subjects in this analysis should be considered a limitation. A larger sample size might have yielded differences with narrower confidence intervals and a lower likelihood of both type I and II errors. Sample size calculations based on Eser‘s results suggest that our metaphyseal vBMD comparisons were underpowered (required sample size 2000). However, Eser‘s negligible effect sizes indicate no actual difference between adult retired gymnasts and non-gymnasts for this variable. As previously noted, in a slightly larger sample, Ward et al. demonstrated a significant total vBMD advantage in prepubertal gymnasts. These contrasting results suggest that during puberty, there is a counterbalance between geometric expansion and enhancement of total vBMD in gymnasts. Our cohort is postpubertal (lower gynecological age than Eser‘s cohort) and is comprised of both active and retired gymnasts (low mean retirement interval vs. Eser‘s cohort). In this context, our intermediate results for metaphyseal vBMD (small effect) may reflect pubertal expansion effects and/or partial maintenance of

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benefit due to lower mean post-retirement interval. A moderately larger sample size may support this hypothesis.

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In our observational study, causality cannot be determined by correlations and observed interindividual differences. Genetic differences, self-selection bias, or unmeasured variables may explain some of the variation attributed to gymnastic exposure in this cohort. Finally, actual growth processes cannot be assessed effectively by this cross-sectional design. Future longitudinal studies should examine maturity-specific growth under contrasting loading conditions in a large number of subjects, applying consistent pQCT protocols and observing the same individuals over time.

Go to: Conclusion These results demonstrate advantages in bone geometry, density, and theoretical strength for postmenarcheal girls exposed to gymnastic loading during childhood and perimenarcheal growth. In particular, perimenarcheal gymnastic exposure appears to generate large advantages in radius intramedullary cavity dimensions that had not been previously reported in gymnasts but have recently been corroborated by Eser et al. [20]. These results suggest that continued mechanical loading through menarche is particularly advantageous, enhancing bone development to yield larger bones with greater theoretical strength. Additional research is necessary to evaluate mode of adaptation and persistence of skeletal benefits attributed to mechanical loading during specific phases of growth.

The prevalence of painful incidents among young recreational gymnasts Chrystal Coates, BSc(Hons), C Meghan McMurtry, BA(Hons), Patricia Lingley-Pottie, BNRN CCRC, and Patrick J McGrath, OC PhD FRSC Author information ► Copyright and License information ► Go to: Abstract BACKGROUND: Although children experience pain during their daily life, research has generally focused on medical pain. Sport-related pain has not been widely

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studied in children and research has not examined the occurrence of painful incidents in gymnastics. The prevalence of painful incidents among children in recreational gymnastics classes and accompanying coach responses were recorded.

METHODS:

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Sixty-one children between five and 10 years of age were observed at a gymnastics club. A checklist was used to record painful incidents as well as coach and child responses.

RESULTS: The rate of painful incidents was 0.17 per child per hour observed. The floor apparatus was the most common site of incidents, while bumping into equipment was the most common incident. Based on observer ratings, most incidents were mild to moderate in severity and, on average, the child‘s reaction to these mild to moderate incidents lasted for 8.5 s. Forty per cent of the children had a mild to moderate painful experience.

Coaches reacted to more than 60% of the painful incidents, usually asking how the child was and what had happened. A significant difference was found between the mean severity ratings of painful incidents that were followed by coach response and incidents followed by no response.

CONCLUSION: Most children who attend recreational gymnastics classes will likely experience at least one mild to moderate painful experience for every 6 h of class. Coaches are more inclined to react to a painful incident than not.

Moreover, a difference was found that suggests coaches responded to more painful incidents.

Keywords: Coaches‘ responses, Gymnastics, Pediatric pain, Recreational sport Go to: Résumé HISTORIQUE :

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Même si les enfants ressentent des douleurs dans leur vie quotidienne, les recherches portent généralement sur les douleurs d‘importance médicale.

Les douleurs liées au sport n‘ont pas fait l‘objet d‘études généralisées chez les enfants, et les recherches n‘ont pas abordé l‘occurrence d‘incidents douloureux en gymnastique. Les chercheurs ont saisi la prévalence d‘incidents douloureux chez les enfants qui suivent des cours de gymnastique et les réponses des entraîneurs accompagnateurs.

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MÉTHODOLOGIE : Les chercheurs ont observé 61 enfants de cinq à dix ans à un club de gymnastique. Ils ont utilisé une liste de vérification pour enregistrer les incidents douloureux ainsi que les réponses des entraîneurs et des enfants.

RÉSULTATS : Le taux d‘incidents douloureux observé s‘élevait à 0,17 par enfant à l‘heure. Les appareils au sol étaient le lieu d‘incidents le plus courant, tandis que se cogner dans du matériel constituait le principal incident.

D‘après les évaluations des observateurs, la plupart des incidents étaient de gravité légère à modérée et, en moyenne, la réaction de l‘enfant à ces incidents durait 8,5 secondes. Quarante pour cent des enfants ont subi une expérience douloureuse légère à modérée. Les entraîneurs ont réagi à plus de 60 % des incidents douloureux, demandant généralement comment était l‘enfant et ce qui s‘était passé. Les chercheurs ont constaté une différence significative entre les taux de gravité moyens des incidents douloureux qui ont suscité la réponse d‘un entraîneur et les incidents qui n‘en ont pas suscité.

CONCLUSION : La plupart des enfants qui suivaient des cours de gymnastique récréative subiront probablement au moins une expérience douloureuse légère à modérée par tranche de six heures de cours. Les entraîneurs sont plus enclins à réagir à un incident douloureux qu‘à ne pas y réagir. De plus, les chercheurs ont constaté une différence selon laquelle les entraîneurs réagiraient aux incidents les plus douloureux.

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The understanding of pain develops during childhood when the most common painful experiences children have are the minor bumps and scrapes they encounter during their normal daily routines (1,2). Studies conducted on everyday pain in daycares have indicated that children experience a painful incident approximately once every 3 h during active play (1,2). Sixty per cent of these incidents were self imposed, while 40% were linked to the deliberate actions of other children (1,2). Even at this young age, the responses of adults differed by sex of the child; following a painful incident, girls received more physical comfort from the adults than boys and also vocalized more intensely (1,2).

Although children experience pain during their daily life, research has generally focused on medical pain. Medical pain includes the pain encountered during medical procedures, such as immunizations, as well as pain encountered by children after injury or disease that requires assistance from health care professionals. Within the context of painful medical procedures, research has demonstrated that the behaviour of adults can influence the way children react to pain. For example, studies (3,4) have shown that common adult behaviours, such as apologies, criticism, giving control to the child, reassurance and distraction, are related to the child‘s level of pain and distress during painful procedures, such as lumbar punctures, bone marrow aspirations and immunizations.

Specifically, it was found that child distress was positively correlated with adult reassurance, apology and empathy, whereas nonprocedural talk (verbal distraction), humour and commands to engage in a coping strategy were associated with child coping (3,4). Adult-child interactions during pediatric procedural pain have been frequently studied (3,5–7), but little is known about these interactions in response to pediatric pain sustained during common activities such as recreational sports.

The everyday pain that children experience is far more common than medical pain. Little is known about the prevalence of pain in gymnastics and no research has examined this issue in recreational gymnastics.

Gymnastics is a popular children‘s sport that presents numerous opportunities for painful experiences and has one of the highest injury rates in popular children‘s sports (8). The most common types of pain that gymnasts sustain while training are associated with the wrists, hands, spine, knees and ankles (9), which can result in persistent pain following practice. Often we only know about significant painful incidents that result

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in a prolonged duration of discomfort, but little is known about painful incidents of short duration that occur during gymnastics classes.

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Research by Nemeth et al (10) showed that there were age differences in competitive gymnasts‘ understanding of pain, their use of pain descriptors and recognition of pain from exertion. Due to limited research in this area, the frequency of painful incidents experienced by young gymnasts is unclear. Moreover, the severity of the experiences and the reaction of the gymnastic coach to the painful incidents sustained by the gymnast are unknown. Given the influence that adult-child interactions have on a child‘s pain experience during medical procedures, there is reason to expect that a coach‘s response to a painful event sustained during class activities may have an impact on the child‘s pain experience.

Although the work by Nemeth et al (10) provided interesting data on competitive gymnasts, the majority of children participating in gymnastics are recreational rather than competitive athletes. The present study was developed to determine the frequency, intensity and duration of painful incidents among five- to 12-year-old children during recreational gymnastics classes, and to explore coach reactions to the painful incidents.

Go to: METHODS Participants The present study has an observational study design. Participants were pediatric members of a recreational gymnastics club located in Dartmouth, Nova Scotia, who were attending beginner classes or summer gymnastics camp; their coaches were also included. Regular gymnastics classes were observed for six weeks, followed by a week of recreational summer day camp. The information and informed consent forms were sent home with every child eligible for the study. For children who were not present at the time the forms were distributed, the parents were approached at the club.

All children were given the opportunity to participate, with the following exclusion criteria: any child outside the age group of five to 12 years and above a beginner skill level of gymnastics; any child enrolled in a beginner gymnastics class in which the coach or apprentice did not consent to participate in the study; and any child who did not have an authorization

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form signed by their parents. The Research Ethics Board of the IWK Health Centre (Halifax, Nova Scotia) approved the present study.

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Before beginning observation, written informed consent was obtained from coaches and verbal assent was obtained from the children, with written authorization from their parents. Sixty-one children (48 girls and 13 boys) ranging in age from five to 10 years (mean [± SD] age 7.2±1.3 years) participated. One male and 10 female coaches (mean age 20.6±8.2 years) who taught the classes and the summer camp were included in the present study.

Observational checklist Before undertaking any observations, a checklist was developed for a child experiencing a physically painful incident while participating in a recreational gymnastics class (Appendix A). This checklist was developed based on research by Fearon et al (1) and von Baeyer et al (2). The checklist was designed to record information describing the physically painful incident and the behaviours of coaches and children following the incident.

Observers were trained to use the checklist in a one-on-one session with the first author. There were six observers: five women and one man. Four of the observers were undergraduate students and two were graduate students. Observers used the checklist to record the type of painful incident the child sustained, the observational rating of the severity and duration of the incident, the body part affected, and the behavioural responses of both the child and the coach. Demographic information on both the child and the coach (eg, age and sex) were obtained by an observer at the time of consent.

Duration of the incident was operationalized as the time from the beginning of the incident until normal activity was resumed. Thus, the duration included both the painful stimulus (eg, bumping a knee) as well as the child‘s and coach‘s behavioural responses. Based on the observed responses of the child, the perceived physical severity of the incident was rated by observers on a scale of 1 to 10, with 1 indicating a mild incident and 10 indicating a very severe incident. The child response(s) were coded into nine categories: crying; a pain face; reporting the incident to the coach; running to the parents; screaming; holding or touching the affected area;

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hitting or pushing others; ignoring the incident; or ‗other‘. More than one category could be assigned to fully capture the child‘s responses. The coach‘s behavioural response to the observed child‘s painful incident was recorded, not using a priori categories, but in a descriptive manner to allow for exploratory analysis. In addition, the type of event equipment (balance beam, vault, floor apparatus, uneven bars, trampoline or rings) on which the incident occurred was recorded.

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Procedure After obtaining consent and assent, participants were observed during their regular gymnastics class or summer camp program. Participants were asked to follow their ordinary routines and activities planned for their class or day camp. A typical gymnastics class would contain between one and eight children per coach. However, researchers observed a maximum of four children per class at once. Some children in the regular gymnastics program were observed for more than one class and, therefore, could have been observed for 1 h to 3 h. Because the children involved in summer camp participated in gymnastics for 3.5 h each day, they were observed for lengths of time between 3.5 h and 14 h over a maximum of four days.

The gymnastics club‘s event equipment included six balance beams, one vault, one floor apparatus, two sets of uneven bars, two trampolines and one set of rings. During each gymnastics class or camp, the gymnasts participated in all events for approximately equal periods of time. When possible, each apparatus was typically set up in a circuit format in which each child was able to continuously practise his or her gymnastics skills.

Certain events (vault, uneven bars, trampoline and rings) allowed only one child at a time to practise his or her gymnastics skills. In contrast, two to three children could practise on the same balance beam at once. On the floor apparatus, the setup was such that only one child would be practising each gymnastics skill at any given time.

At all times, two observers independently watched the children to allow for inter-rater reliability calculations. The observers recorded any incident of pain, its apparent cause and the subsequent coach-gymnast interaction.

They observed at a distance of approximately 2 m and ensured that all activities were in front of them and could be easily viewed without disturbing the participants. Observers interacted as little as possible with the participants and observed all activities. Because the participants were

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completing circuits, there may have been times when a child was waiting in line rather than performing an activity. Thus, observers simply scanned all the participants in a class rather than fixating on any particular individual.

Observers followed the groups of participants as they moved from event to event.

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Data analysis Frequency analysis was used to determine the type, duration and perceived severity of each painful incident the children experienced, as well as the event equipment associated with the incident. Means were used to describe the number of painful incidents experienced by age. After data collection, codes were created for the coaches‘ responses based on the data. Content and frequency analysis were used to describe child and coach responses to the painful incidents. Post hoc, independent t tests were used to explore any differences between coach response and no response. All statistics were calculated using SPSS 14.0 (SPSS Inc, USA).

Go to: RESULTS Inter-rater reliability was calculated via per cent agreement as the amount of agreement between observers for each category on the checklist. The purpose of the present study was not to discover meaningful differences between participants but rather to describe the painful incidents observed during a recreational gymnastics class. Therefore, if observers recorded the severity of the painful incident within ±1 rating of each other, then agreement was considered to be achieved. Similarly, agreement was achieved if the observers‘ scores for the duration of the painful incident were within ±5 s. Observers had 91% to 98% agreement in each category on the checklist (eg, type of painful incident, severity, duration, and coach and child responses to the painful incident). In cases of disagreement between observers, the mean rating of the two observers‘ scores was used for analysis. If there was disagreement about the child and coach responses, all recorded responses were used in the analysis.

One child participated in both the classes and the camp; therefore, the camp data were removed from analyses. In addition, data collected on a child with a significant mental health disorder who demonstrated extreme

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behavioural reactions to four painful incidents were deleted. This yielded a total of 61 participants.

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Frequency of painful incidents

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All participants reported previous experience with gymnastics, except for one child in the camp program. This child did not experience any painful incidents. Overall, painful incidents occurred at a rate of 0.17 incidents per child per hour observed (45 incidents in 262 child hours of observation) and were experienced by 24 different children (39%). No painful incidents were observed for 37 children (61%). Girls experienced an average of 0.18 painful incidents per child hour (35 incidents for 48 girls in 194 female child hours). Boys experienced an average of 0.15 painful incidents per child hour (10 incidents for 13 boys in 68 male child hours). No significant difference in the frequency of painful incidents was found between younger (five- to seven-year-olds) and older (eight- to 10-year-olds) children, (t[59]=0.177, P=0.860). Table 1 contains the frequency of incidents in each age group.

TABLE 1 Painful incidents experienced in each age group over 262 total child hours of observation Frequency analysis showed that the most common painful incidents (24.4%; 11 incidents) occurred as a result of bumping into equipment, while 15.6% (seven incidents) occurred from falling off equipment and stubbing toes (Table 2). One incident resulting in a laceration required first aid intervention (ie, application of an adhesive bandage). Participants experienced the greatest number of painful incidents on the floor apparatus (21/45) followed by the balance beam (7/45), uneven bars (6/45), vault (5/45), trampoline (5/45) and rings (1/45).

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TABLE 2

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Type and frequency of painful incidents experienced by the children over 262 total child hours of observation Duration of painful incidents The majority of the observed painful incidents lasted for 10 s or less (75.6%; 34 incidents), while 13.3% of painful incidents (six incidents) lasted from 11 s to 30 s, and only 11.1% of the incidents (five incidents) lasted for longer than 30 s.

Severity of painful incidents Observers did not rate any incidents of perceived severity above a moderate rating of 4 (ie, the overall range was 1 to 4 of 10). The majority of painful incidents were mild, with severity ratings of 1 or 2 (86.7%; 39 incidents), while the remainder had severity ratings of 3 or 4 (13.3%; six incidents).

Child and coach reactions to the painful incidents The majority of the young gymnasts‘ reactions to the painful incidents included verbal exclamations, holding or touching the affected area, or facial pain responses. Table 3 shows the type and frequency of the children‘s responses to the painful incidents.

TABLE 3

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Type and frequency of the children‘s responses to the painful incidents occurring over 262 total child hours of observation Post hoc independent t tests were conducted to explore possible mean differences in severity and duration of incidents followed by coach response versus no response. Significant differences were found when comparing coach response versus no response to the severity of the painful incident (t[43]=2.21, P=0.03); on average, incidents that coaches responded to had a higher severity rating than incidents that were followed by no response. However, there were no significant differences found between coach response and no response for the duration of the painful incident (t[43]=0.82, P=0.42) (Table 4).

TABLE 4 Comparison between coach response and no response to the painful incident and the severity (0 to 10) and duration of the painful incident Content analysis revealed common responses made by coaches to the painful incidents. Table 5 shows the type and frequency of coach responses. The observed responses included no response at all, inquiry about whether the child was all right, inquiry about what happened, and/or instruction or demonstration of the proper technique for the skill. Coaches also listened to the children retell their versions of the painful incidents and gave assistance or comfort.

TABLE 5 Type and frequency of the coach response to the painful incidents occurring in 262 total child hours of observation Go to: DISCUSSION

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Gymnastics is an active sport during which children may sustain injuries resulting in painful experiences. The present study described the point prevalence of painful incidents in children while participating in recreational gymnastics classes and the coaches‘ responses to these painful incidents.

In these beginner gymnastics classes, 39% of the children experienced a painful incident. Thus, 61% of participants did not experience a painful incident. The prevalence of painful incidents observed in the present study suggests that a child attending a recreational gymnastics class has the likelihood of sustaining at least one mild to moderate painful event per 6 h of class activity. Thus, in a typical beginner gymnastics class, most children do not experience a painful incident.

The highest number of painful incidents observed resulted from children bumping into equipment, perhaps because they were distracted. Painful incidents most commonly occurred on the floor apparatus (a 40 ft × 40 ft square foam mat on top of springs attached to plywood), balance beam and uneven bars. The finding that most painful incidents occurred on the floor apparatus was interesting because the trampoline appears to be a more likely apparatus for painful incidents (11). The number of painful incidents on the floor apparatus may have been artificially increased because there were a greater number of children on the floor apparatus at any one time compared with other event equipment. Anecdotal observations revealed that coach procedures for managing the children‘s behaviour during trampoline activities were stricter than during floor apparatus activities. Increased coach control may explain the lower incident rate associated with the trampoline. Perhaps enhanced coach supervision and direction during other gymnastic activities would decrease the prevalence of painful incidents.

Children typically responded to a painful incident with a verbal exclamation, holding or touching the affected area, or a pain face. Although one of the most common coach reactions to the child‘s painful incident was no response (36.5%), this did not seem to hinder the flow of the class. It is difficult to know whether these incidents were actually unnoticed or whether the coaches were actively ignoring the children. The coaches‘ responses could be considered entirely appropriate because the children typically encountered only minor incidents of pain (observer-rated severity of 4 or less of 10).

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When coaches did respond to the child‘s pain event, it was often to query whether the child was all right. Coaches who reacted to the painful incidents seemed to respond to the child with patience. The patience the coach demonstrated was usually successful in encouraging the child to continue his or her participation in the class. Also, instruction or demonstration by the coach of the proper skill technique may have helped decrease the occurrence of painful incidents when the child attempted the skill a second time.

The comparison of mean severity ratings between coach response versus no response shows that coaches respond differently depending on the severity of the child‘s pain experience. Coaches were more likely to respond to painful incidents of higher severity than lower severity.

However, the direction of causation is unclear. It is possible that a coach response to a child‘s painful incident may influence a child‘s reaction to pain as has been found in the medical literature (12).

Further research is needed to explore whether the results of the present study may be replicated in a study designed to evaluate self-report of pain, and also whether the pain persists after the class. Additionally, it would be valuable to find out whether a parent would perceive this prevalence as a meaningful concern. Future research could also investigate the prevalence of painful incidents and adult/coach responses in other recreational ball sports such as baseball, soccer, basketball, football and volleyball. A future study designed to record the child‘s self-reported pain experience while controlling for coach response to painful events would provide further insight into any influence that coach responses may have on the child‘s pain experience. Interactions between adults and athletes have not been studied within the context of sport-related pain.

The findings of a study by Chambers et al (12) indicated that maternal behaviour directly influenced girls‘ subjective reports of pain but not their pain affect, facial activity or heart rate. Boys were not affected by maternal behaviour. Thus, a study examining the impact of coach behaviour on a child‘s self-reported pain experience that explored sex differences would help to elucidate how children cope with pain incidents during recreational gymnastic activities.

A future study exploring the understanding of pain among nonathletes, and recreational and competitive gymnasts, could help coaches succeed in

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accurately assessing their athletes‘ level of pain tolerance. Results could be compared with the study conducted by Nemeth et al (10), which explored the understanding of pain by competitive athletes. These researchers investigated competitive child gymnasts‘ understanding of pain by analyzing their knowledge of different types of sport-related pain, such as pain from conditioning versus acute pain versus chronic pain, their use of pain descriptors, and their expectations for adult help following painful incidents. The study found that gymnasts reacted differently to various types of pain, and that there were age differences in the understanding and use of descriptors for pain. In contrast to younger gymnasts, older gymnasts could distinguish between pain that was too severe to continue training from pain that they would be willing to endure, especially when it was going to help with physical gain (eg, the pain experienced during conditioning). Therefore, in the future, it would be interesting to use selfreports from the gymnasts and coaches to investigate the experience of painful incidents in gymnastics classes.

One limitation of the present study was that the severity and duration ratings of the children‘s pain experience were observational and limited to class time. Without knowing the children‘s self-reported experience, we do not know whether the observers‘ perceived severity and duration ratings were commensurate with the children‘s actual experience. A second limitation was that the exploratory study design did not allow for follow-up with participants to discuss their pain experience after the gymnastics class. The objective of the present initial study was to investigate the prevalence of painful incidents that occurred during the class. However, future research could address these issues.

The present study was observational in nature and demonstrated that participating in recreational gymnastics classes does expose children to the possibility of experiencing a mild to moderately painful incident. The results of the present study also suggest that a positive, constructive coach response to a painful event may provide encouragement to the child. With coach supervision, instruction and encouragement, children can potentially learn basic motor skills and coordination, and gain confidence during gymnastic activities, which may lead to decreased future incidents.

The present study provides evidence that gymnastics is not as dangerous a sport as some believe it to be (8) and young children can participate in the sport without experiencing serious pain. Specifically, the overall rate of

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painful incidents in the present study was low. Pain from conditioning and from acute and chronic injury may be more common at the elite, competitive levels of gymnastics, when children spend far more hours at the gymnasium, become more fatigued and practise riskier manoeuvres (10). At the recreational level, it seems unlikely that a child will encounter a severely painful incident, suggesting that recreational gymnastics may not be as precarious as one expects (8).

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Acknowledgments

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A grant to the first author from the IWK Health Centre, Dr McGrath‘s Canada Research Chair and a grant from Neuroscience Canada to Dr McGrath provided support for this study. These data were presented in part at the Canadian Pain Society Annual Conference (Halifax, Nova Scotia, May 2005). The authors thank the Titans Gymnastics and Trampoline Club (Dartmouth, Nova Scotia) for their support and use of the facilities for data collection. The authors also thank B Ernst, D Kempster, D Nugyen and M MacLeod for their assistance.

Go to: APPENDIX A Click on image to zoom

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Go to: Footnotes NOTE: This work originated from the Centre for Research in Family Health at the IWK Health Centre.

Go to: REFERENCES

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1. Fearon I, McGrath PJ, Achat H. ‗Booboos‘: The study of everyday pain among young children. Pain. 1996;68:55–62.[PubMed] 2. von Baeyer CL, Baskerville S, McGrath PJ. Everyday pain in three- to five-year-old children in day care. Pain Res Manage. 1998;3:111–6.

3. Blount RL, Corbin SM, Sturges JW, Wolfe VV, Prater JM, James LD. The relationship between adults‘ behaviour and child coping and distress during BMA/LP procedures: A sequential analysis. Behav Ther.

1989;20:585–601.

4. Manimala MR, Blount RL, Cohen LL. The effects of parental reassurance versus distraction on child distress and coping during immunizations. Child Health Care. 2000;29:161–77.

5. Blount RL, Piira T, Cohen LL. Management of pediatric pain and distress due to medical procedures. In: Roberts MC, editor. Handbook of Pediatric Psychology. 3rd edn. New York: Guilford; 2003. pp. 216–33.

6. Blount RL, Sturges JW, Powers SW. Analysis of child and adult behavioral variations by phase of medical procedure. Behav Ther.

1990;21:33–48.

7. Chambers CT. The role of family factors in pediatric pain. In: McGrath PJ, Finley GA, editors. Pediatric Pain: Biological and Social Context.

Seattle: IASP Press; 2003. pp. 99–130.

8. Singh S, Smith GA, Fields SK, McKenzie LB. Gymnastics-related injuries to children treated in emergency departments in the United States, 1990– 2005. Pediatrics. 2008;12:e954–60.[PubMed] 9. Zetaruk MN. The young gymnast. Clin Sports Med. 2000;19:757– 80.[PubMed] 10. Nemeth RL, von Baeyer CL, Rocha EM. Young gymnasts‘ understanding of sport-related pain: A contribution to prevention of injury.

Child Care Health Dev. 2005;31:615–25.[PubMed] 11. Smith GA. Injuries to children in the United States related to trampolines, 1990–1995: A national epidemic. Pediatrics. 1998;101:406– 12.[PubMed] 12. Chambers CT, Craig KD, Bennett SM. The impact of maternal behaviour on children‘s pain experiences: An experimental analysis. J Pediatr Psychol. 2002;27:293–301.[PubMed Descriptive Epidemiology of Collegiate Women's Gymnastics Injuries: National Collegiate Athletic Association Injury Surveillance System, 1988– 1989 Through 2003–2004

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Stephen W Marshall, PhD,* Tracey Covassin, PhD, ATC,† Randall Dick, MS, FACSM,‡ Lawrence G Nassar, DO, ATC,† and Julie Agel, MA, ATC§ Author information ► Copyright and License information ► This article has been cited by other articles in PMC. Go to: Abstract

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Objective: To review 16 years of National Collegiate Athletic Association (NCAA) injury surveillance data for women's gymnastics and identify potential areas for injury prevention initiatives.

Background: In the 1988–1989 academic year, 112 schools were sponsoring varsity women's gymnastics teams, with approximately 1550 participants. By 2003–2004, the number of varsity teams had decreased 23% to 86, involving 1380 participants. Significant participation reductions during this time were particularly apparent in Divisions II and III. Main Results: A significant annual average decrease was noted in competition (−4.0%, P < .01) but not in practice (−1.0%, P = .35) injury rates during the sample period. Over the 16 years, the rate of injury in competition was more than 2 times higher than in practice (15.19 versus 6.07 injuries per 1000 athlete-exposures; rate ratio = 2.5, 95% confidence interval [CI] = 2.3, 2.8). A total of 53% of all competition and 69% of all practice injuries were to the lower extremity. A participant was almost 6 times more likely to sustain a knee internal derangement injury in competition than in practice (rate ratio = 5.7, 95% CI = 4.5, 7.3) and almost 3 times more likely to sustain an ankle ligament sprain (rate ratio = 2.7, 95% CI = 2.1, 3.4). The majority of competition injuries (approximately 70%) resulted from either landings in floor exercises or dismounts.

Recommendations: Gymnasts with a previous history of ankle sprain should either wear an ankle brace or use prophylactic tape on their ankles to decrease the risk of recurrent injury. Preventive efforts may incorporate more neuromuscular training and core stability programs in the off-season and preseason conditioning to enhance proper landing and skill mechanics. Equipment manufacturers are encouraged to reevaluate the design of the landing mats to allow for better absorption of forces.

Keywords: athletic injuries, injury prevention, knee injuries, ankle injuries

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T he National Collegiate Athletic Association (NCAA) conducted its first women's gymnastics championship in 1982. In the 1988–1989 academic year, 112 schools were sponsoring varsity women's gymnastics teams, with approximately 1550 participants. By 2003–2004, the number of varsity teams had decreased 23% to 86, involving 1380 participants. 1 Significant participation reductions during this time were particularly apparent in NCAA Divisions II and III. Go to:

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SAMPLING AND METHODS Over the 16-year period from 1988–1989 through 2003– 2004, an average of 21.1% of schools sponsoring varsity women's gymnastics programs participated in annual NCAA Injury Surveillance System (ISS) data collection ( Table 1).The sampling process, data collection methods, injury and exposure definitions, inclusion criteria, and data analysis methods are described in detail in the ―Introduction and Methods‖ article in this special issue. 2

Table 1 School Participation Frequency (in Total Numbers) by Year and National Collegiate Athletic Association (NCAA) Division, Women's Gymnastics, 1988– 1989 through 2003–2004* Go to: RESULTS Competition and Practice Athlete-Exposures The average annual numbers of competitions, practices, and athletes participating for each NCAA division, condensed over the study period, are shown in Table 2.

The 3 divisions averaged a similar number of annual competition and practice participants. Annually, Divisions I and II averaged approximately 14 more practices and 1 more competition than Division III.

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Table 2

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Average Annual Competitions, Practices, and Athletes Participating by National Collegiate Athletic Association Division per School, Women's Gymnastics, 1988–1989 Through 2003–2004 Injury Rate by Activity, Division, and Season Competition and practice injury rates over time combined across divisions with 95% confidence intervals (CIs) are displayed in Figure 1. A significant average annual decrease was seen in competition (−4.0%, P < .01) but not in practice (−1.0%, P = .35) injury rates over the sample period. Over the 16 years of the study, the risk of injury in a competition was more than 2 times higher than the risk of injury in practice (15.19 versus 6.07 injuries per 1000 athlete-exposures [A-Es], rate ratio = 2.5, 95% CI = 2.3, 2.8).

Figure 1 Injury rates and 95% confidence intervals per 1000 athlete-exposures by competitions, practices, and academic year, women's gymnastics, 1988–1989 through 2003–2004 (n = 495 competition injuries and 2244 practice injuries).

Competition (more ...)

The total number of competitions and practices and associated injury rates condensed over years by division and season (preseason, in season, and postseason) are presented in Table 3. Over the 16-year period, 495 injuries from more than 3300 competitions and 2244 injuries from more than 30 000 practices were reported. Competition injury rates were higher in Division I than in Division III (16.61 versus 7.55 injuries per 1000 A-Es, rate ratio = 2.2, 95% CI = 1.5, 3.1, P < .01). Across all divisions, in-season competition injury rates were higher than postseason rates (15.55 versus 10.82 injuries per 1000 A-Es, rate ratio = 1.4, 95% CI = 0.98, 2.12, P = .07).

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Table 3 Competition and Practice With Associated Injury Rates by National Collegiate Athletic Association Division and Season, Women's Gymnastics, 1988–1989 Through 2003–2004* Body Parts Injured Most Often and Specific Injuries The frequency of injury to 5 general body areas (head/neck, upper extremity, trunk/back, lower extremity, and other/system) for competitions and practices with years and divisions combined is shown in Table 4. A total of 69.3% of all competition and 52.8% of all practice injuries were to the lower extremity. Upper extremity injuries accounted for another 11.5% of competition injuries and 17.8% of practice injuries. Injuries to the head and neck represented 6.7% of competition injuries and 5.6% of practice injuries.

Table 4 Percentage of Competition and Practice Injuries by Major Body Part, Women's Gymnastics, 1988–1989 Through 2003–2004 The most common injured body part and injury type combinations for competition and practices with years and divisions combined are shown in Table 5. All injuries that accounted for at least 1% of reported injuries over the 16-year sampling period were included. In competitions, knee internal derangements (20.0%) and ankle ligament sprains (16.4%) accounted for the majority of injuries. In practices, ankle ligament sprains (15.2%), knee internal derangements (8.7%), and low back strains (6.1%) accounted for most of the reported injuries. Concussions represented 2.3%

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of practice injuries and 2.6% of competition injuries. A participant was nearly 6 times more likely to sustain a knee internal derangement in competition than in practice (3.04 versus 0.53 per 1000 A-Es, rate ratio = 5.7, 95% CI = 4.5, 3.4) and almost 3 times as likely to sustain an ankle ligament sprain in competition as in practice (2.48 versus 0.93 per 1000 A-Es, rate ratio = 2.7, 95% CI = 2.1, 3.4).

Table 5 Most Common Competition and Practice Injuries, Women's Gymnastics, 1988–1989 Through 2003–2004* Mechanism of Injury The 2 injury mechanisms, other contact with an object (such as apparatus or floor) and no contact, in competitions and practices with division and years combined, are displayed in Figure 2. The majority of competition injuries (70.7%) resulted from other contact, primarily during landings. This category was also the leading mechanism for practice injuries.

Figure 2 Competition and practice injury mechanisms, all injuries, women's gymnastics, 1988–1989 through 2003–2004 (n = 495 competition injuries and 2244 practice injuries). “Other contact” refers to contact with items such as the (more ...)

Severe Injuries: 10+ Days of Activity Time Loss

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The top injuries that resulted in at least 10 consecutive days of restricted or total loss of participation and their primary injury mechanisms combined across divisions and years are presented in Table 6. For this analysis, time loss of 10+ days was considered a measure of severe injury. A total of 39.0% of competition and 32.0% of practice injuries restricted participation for at least 10 days. In both competitions and practices, knee internal derangements and ankle ligament sprains accounted for the highest percentage of more severe injuries. A total of 25% of ankle sprains were recurrences (data not shown).

Table 6 Most Common Competition and Practice Injuries Resulting in 10+ Days of Activity Time Loss, Women's Gymnastics, 1988– 1989 Through 2003–2004 Competition Injuries The competition event or apparatus used at the time of injury combined over the years is shown in Figure 3. Floor exercise and vault accounted for the largest number of competition injuries. The competition event or apparatus used at the time of injury, the most common types of injuries associated with those activities, and whether the injuries occurred during mounting, the routine, or the dismount are described in Table 7. Knee internal derangement was the most common injury in all events, most often occurring during the dismount, except in tumbling routines during floor exercise.

Figure 3 Competition apparatus or event at time of injury, women's gymnastics, 1988– 1989 through 2003–2004 (n = 495)

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Table 7

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Most Common Competition Injuries Associated With An Apparatus or Event, Women's Gymnastics, 1988–1989 Through 2003–2004 (n = 495)* Go to:

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COMMENTARY Overall, competition injury rates in collegiate women's gymnastics during the past 16 years have significantly decreased (by 4% per year, on average) for competitions. A total of 36.4% of all injuries in competitions were knee internal derangements or ankle ligament sprains. In practices, 23.9% of all injuries are knee internal derangements or ankle ligament sprains. Gymnasts were 6 times more likely to sustain a knee internal derangement and almost 3 times more likely to sustain an ankle ligament sprain in competition than in practice. Female gymnasts had a 3-times-greater rate of injury during preseason practices compared with inseason practices. Almost one third of all competition injuries occurred during the floor routine. For nonfloor events, dismounts accounted for most of the injuries.

These results are consistent with those from previous research on women's gymnastics, although direct comparisons are difficult because of variations in study methods. The lower extremity was the injured body site reported most often by certified athletic trainers, which is consistent with previous findings. 3–8 Kolt and Kirkby 3 noted that elite gymnasts reported the most common location of injury to be the ankle and foot (30.7%), followed by the knee (16.3%), elbow and forearm (12.4%), and wrist and hand (9.8%). Almost all investigators studying women's gymnastics reported that most injuries were incurred in the ankle and foot. 3–8 Caine and Nassar 5 found that ankle sprains were the most commonly reported injury by gymnasts participating in the 2002–2004 USA Gymnastics National Women's Artistic Championships. The majority of ankle injuries resulted from falls on dismounts and tumbling during floor routines. Gymnasts constantly land from great heights while twisting and rotating, leading to the high rates of both initial and recurrent ankle injuries. One recommendation may be for gymnasts with a previous history of ankle sprains to wear either an ankle brace or prophylactic tape on the ankle to try and decrease the risk of injury. In addition, athletes with a

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previous history of ankle sprains should either brace or tape their ankles during competitions to try and decrease the injury rates during competition. 9 Time loss due to injury is difficult to measure because gymnasts tend to modify their training to avoid potential physical deconditioning. 3 Kolt and Kirkby 3 reported that elite gymnasts modified a significantly greater number of practice sessions than did subelite gymnasts, either because of pressure from coaches or fear of physical deconditioning. In the current study, 39% of competition and 32% of practice injuries restricted participation for at least 10 days, with knee internal derangements and ankle ligament sprains accounting for the highest percentage of time-loss injuries. Similarly, Caine et al 4 reported that 33.3% of injuries had a time loss of between 8 and 21 days, and 25.9% had a time loss of more than 21 days.

Another area of injury concern in female gymnasts is the lower back. Gymnasts place a considerable amount of stress on the lower back as a result of repetitive flexion, hyperextension, rotation, and compressive loading of the spine on landings. Several researchers 10–12 have suggested that anterior column spine problems, such as anterior vertebral endplate fractures, are more common than posterior column spine problems. However, these specific types of injuries cannot be distinguished in the ISS data, so we cannot determine if they are more common in NCAA gymnasts. Low back strains were the third most common practice injury, accounting for 6.1% of all practice injuries and 3.2% of competition injuries.

However, these data may not fully capture the entire burden of low back injuries in gymnastics, because for many chronic low back problems, the athlete may not be restricted (no time loss) and, thus, the injury would not be captured by the timeloss definition used in the ISS. The new Web-based ISS has been adapted to capture both time-loss and non–time-loss injuries; future analyses may provide a better picture of the epidemiology of low back injuries in this population.

During the regular season, competition injury rates were 4 times higher than practice injury rates. Sands et al 13 suggested that increased competition injuries may be due to the higher level of fatigue athletes develop when performing full routines in season. In another study, Sands 14 proposed that gymnasts may be more protected in practices than in competitions because during practice, they often land in foam pits, on softer mats, or with the aid of spotting belts and bungee devices.

Although spotting is now allowed in competition, the higher injury incidence in competition than in practice warrants a reevaluation of competition rules and performance environment. When one reviews the judging of the competition, the trend over the years has been to reward a higher degree of tumbling, creating a need for the gymnast to add more saltos and full twists. This has caused a decrease

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in the artistic aspect of gymnastics, and dance skills have been devalued. If the artistic aspect and dance skills were to be given greater value, then gymnasts would have an option to perform fewer high-risk skills and still have the potential for high scores.

The risk of injury was 2 times greater during preseason than in-season practice sessions. Preseason practice is typically the time to learn new skills for the competition season. These new skills may contribute to an increase in injuries over in-season practice sessions. Gymnasts not fully recovered from injuries during the preseason may decrease their practice time and repetition of skills during in-season practices, which may in turn decrease injury rates. Another explanation for the increased injury rate in the preseason may be decreased physical conditioning and fatigue from increased training intensity. Gymnasts may begin the preseason in a deconditioned state, compared with their fitness levels at the end of the previous season. Strength and conditioning coaches should provide gymnasts with a physical conditioning program during the off-season to maintain their fitness level year-round. As a result, gymnasts should begin the preseason in good physical condition, allowing coaches to implement a progressive training program that includes practicing old skills, learning new skills, modifying routines, and then performing full routines.

The results of this study are consistent with those of previous researchers, 4, 13, 15, 16 who reported that floor exercise was associated with the greatest number of injuries. One would expect to see this finding in gymnasts who either compete in the all-around or specialize in floor exercise as a result of the repetitive landings that occur in floor exercise routines. Furthermore, gymnasts spend a considerable amount of time training in tumbling, completely separate from other floor components. The forces at the ankle that are required during tumbling take-offs and landings range from 5.0 to 17.5 times a gymnast's body weight, which may contribute to increased incidence and severity of ankle injuries. 17 The vault also contributes to more than one quarter of all gymnastic injuries. Most injuries occur to the knee and ankle during vault dismounts. During the 2002–2003 season, the vault horse was switched to the vault table. The design of the new vault table allows gymnasts to propel themselves higher up and further out, creating the potential for more difficult and risky vaults to be attempted and executed.

Therefore, an increase in ankle and knee injuries may be due to greater ground reaction forces during landing. Wrist injuries may decrease because the vault table does afford a greater ―sweet spot‖ for hand contact on the table than the horse.

Overall, we expect to see a decrease in injuries on the preflight due to hand contact

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and an increase in injuries on the postflight due to foot contact. However, research on the safety of the current vault table design and its influence on injuries has yet to be conducted.

Although injury rates over the past 16 years have declined for competitions, further prevention interventions are needed. Over the past decade, the use of the ―sting mat‖ has been approved in competitions as a way to soften landings. When a gymnast lands on a new landing mat, she tends to skip on top of the mat and then sink into the mat, producing a very fast oscillatory action of the feet before sinking into the mat. With the use of the sting mat, the athlete avoids the skipping aspect because the soft mat absorbs some of the forces. Bruggemann 10 reported that sting mats reduced the compressive forces on the spine during landings by 20%.

Equipment manufacturers may assist in reducing injuries by reevaluating the landing mats and changing the surface of the mat to one that incorporates the absorption properties of a sting mat as a top layer on the landing mats.

The majority of injuries in collegiate gymnasts are suffered during the dismount. In gymnastics, bonus points are scored for more difficult maneuvers and can enhance the routine's start value. This leads us to question the risk:benefit ratio of this system. A greater deduction for a fall on the dismount might encourage better and safer landing strategies and improvement in overall task execution. Increasing the penalty for poorly performing the skill reduces the gymnast's desire to perform the more difficult skills until she is confident in performing the skill.

The results of this study have potential with regard to the development of preventive measures as well as for numerous future research studies. First, investigators should examine the vibration components of the floor exercise platform and beam, vault, and uneven bars dismount safety mats to improve the absorption of the repetitive impacts from landings. Second, further study is needed in the design of the balance beam to assist in the absorption of forces. The balance beam has been improved from the original wood beam to a padded beam with reflex shock absorption in the legs of the beam to help absorb the forces applied through this piece of equipment. However, few authors have examined the optimal stiffness and shock-absorbing capacity of the apparatus. Third, future researchers need to examine the new vaulting table to determine if it has decreased the number of injuries compared with the old vault horse.

In conclusion, overall injury rates during the past 16 years have decreased for competitions. The ankle, knee, and lower back appear to be the most commonly injured areas in collegiate female gymnasts, with athletes facing a 6-times-greater

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likelihood of sustaining knee internal derangement in competition than in practice.

Most injuries occur during dismount or tumbling during the floor routine.

Preventive efforts may incorporate more neuromuscular training programs and core stability programs in the off-season and preseason conditioning to enhance proper landing and skill mechanics. In addition, many sports incorporate the use of taping and bracing to prevent ankle injuries. It may be beneficial for the sport of gymnastics to encourage this method of assisting in injury prevention. Equipment manufacturers are encouraged to reevaluate the design of landing mats to allow for better absorption of landing forces.

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Go to:

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DISCLAIMER The conclusions in the Commentary section of this article are those of the Commentary authors and do not necessarily represent the views of the National Collegiate Athletic Association.

Go to: REFERENCES 1. National Collegiate Athletic Association. 1981/82–2004/05 NCAA Sports Sponsorship and Participation Rates Report. Indianapolis, IN: National Collegiate Athletic Association; 2006.

2. Dick R, Agel J, Marshall SW. National Collegiate Athletic Association Injury Surveillance System commentaries: introduction and methods. J Athl Train. 2007;42:173–182.

3. Kolt GS, Kirkby RJ. Epidemiology of injury in elite and subelite female gymnasts: a comparison of retrospective and prospective findings. Br J Sports Med. 1999;33:312–318. [PMC free article][PubMed] 4. Caine D, Cochrane B, Caine C, Zemper E. An epidemiologic investigation of injuries affecting young competitive female gymnasts. Am J Sports Med. 1989;17:811–820.[PubMed] 5. Caine D, Nassar L. Gymnastics injuries. In: Caine D, Maffulli N, eds.

Epidemiology of Pediatric Sports Injuries: Individual Sports. Vol 48. Basel, Switzerland: Karger; 2005:18–58 .

6. Dixon M, Fricker P. Injuries to elite gymnasts over 10 yr. Med Sci Sports Exerc. 1993;25:1322–1329.[PubMed]

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7. Kerr G. Injuries in artistic gymnastics. J Can Athl Ther Assoc. April 1991:19–21.

8. Lindner KJ, Caine DJ. Injury patterns of female competitive club gymnasts.

Can J Sport Sci. 1990;15:254–261.[PubMed] 9. Olmsted LC, Vela LI, Denegar CR, Hertel J. Prophylactic ankle taping and bracing: a numbers-needed-to-treat and cost-benefit analysis. J Athl Train.

2004;39:95–100. [PMC free article][PubMed] 10.Bruggemann GP. Biomechanics in gymnastics. Med Sport Sci. 1987;25:142–176.

11.Katz DA, Scerpella TA. Anterior and middle column thoracolumbar spine injuries in young female gymnasts: report on seven cases and review of the literature. Am J Sport Med. 2003;31:611–616.

12.Sward L. The thoracolumbar spine in young elite athletes: current concepts on the effects of physical training. Sports Med. 1992;13:357–364.[PubMed] 13.Sands WA, Shultz BB, Newman AP. Women's gymnastics injuries: a 5-year study. Am J Sports Med. 1993;21:271–276.[PubMed] 14.Sands W. Injury prevention in women's gymnastics. Sports Med. 2000;5:359–373.[PubMed] 15.Lowry CB, Leveau BF. A retrospective study of gymnastics injuries to competitors and noncompetitors in private clubs. Am J Sports Med. 1982;10:237–239.[PubMed] 16.Leglise M. Limits on young gymnast's involvement in high-level sport.

Technique. 1998;18:8–14.

17.McNitt-Gray J. The influence of joint flexion, impact velocity, rotation, and surface characteristics on the forces and torques experienced during gymnastics landings. Federation International de Gymnastics Scientific/ Medical Symposium Proceedings, September 12, 1991; Indianapolis, IN: USA Gymnastics; 1991:17–19 .

Comparison of Static and Dynamic Balance in Female Collegiate Soccer, Basketball, and Gymnastics Athletes Eadric Bressel, EdD,* Joshua C Yonker, MS, LAT, ATC,† John Kras, EdD,* and Edward M Heath, PhD* Author information ► Copyright and License information ► This article has been cited by other articles in PMC. Go to: Abstract

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Context: How athletes from different sports perform on balance tests is not well understood. When prescribing balance exercises to athletes in different sports, it may be important to recognize performance variations.

Objective: To compare static and dynamic balance among collegiate athletes competing or training in soccer, basketball, and gymnastics.

Design: A quasi-experimental, between-groups design. Independent variables included limb (dominant and nondominant) and sport played.

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Setting: A university athletic training facility.

Patients or Other Participants: Thirty-four female volunteers who competed in National Collegiate Athletic Association Division I soccer (n = 11), basketball (n = 11), or gymnastics (n = 12).

Intervention(s): To assess static balance, participants performed 3 stance variations (double leg, single leg, and tandem leg) on 2 surfaces (stiff and compliant). For assessment of dynamic balance, participants performed multidirectional maximal single-leg reaches from a unilateral base of support.

Main Outcome Measure(s): Errors from the Balance Error Scoring System and normalized leg reach distances from the Star Excursion Balance Test were used to assess static and dynamic balance, respectively.

Results: Balance Error Scoring System error scores for the gymnastics group were 55% lower than for the basketball group (P = .01), and Star Excursion Balance Test scores were 7% higher in the soccer group than the basketball group (P = .04).

Conclusions: Gymnasts and soccer players did not differ in terms of static and dynamic balance. In contrast, basketball players displayed inferior static balance compared with gymnasts and inferior dynamic balance compared with soccer players.

Keywords: proprioception, postural control, ankle injury, motor learning, attention Key Points 

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Female basketball players demonstrated inferior static balance compared with gymnasts and inferior dynamic balance compared with soccer players.

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No differences in static or dynamic balance were seen between gymnasts and soccer players.

Specific sensorimotor challenges, rather than general sport activity, appear to be important in developing optimal balance.

Athletic trainers often prescribe exercises in an attempt to enhance an athlete's postural control or balance and perhaps reduce the risk of injury. Unipedal balance tasks on progressively challenging surfaces (eg, firm floor to ankle disc) are examples of exercises that have improved the balance of athletes after ankle sprains.1–3 Differences in ankle and knee proprioception between trained athletes and matched controls suggest that sport participation, by challenging sensorimotor systems, may enhance balance.4,5 What seems to be lacking from this line of research is an appreciation of how athletes from different sports perform on balance tests. With this insight, athletic trainers may prescribe balance exercises more effectively to athletes from different sports.

Postural control or balance can be defined statically as the ability to maintain a base of support with minimal movement and dynamically as the ability to perform a task while maintaining a stable position.6 Factors that influence balance include sensory information obtained from the somatosensory, visual, and vestibular systems and motor responses that affect coordination, joint range of motion (ROM), and strength.7–10 Some evidence in the literature suggests that superior balance among experienced athletes is largely the result of repetitive training experiences that influence motor responses and not greater sensitivity of the vestibular system.11 Others argue that superior balance is the result of training experiences that influence a person's ability to attend to relevant proprioceptive and visual cues.12 Although experts may not agree on the mechanism, research suggests that changes in both sensory and motor systems influence balance performance.

Each sport likely requires different levels of sensorimotor processes to perform skills and protect the neuromuscular system from injury. Gymnasts often perform leaping and tumbling maneuvers as well as static poses while barefoot on surfaces that vary in stiffness. Many of their skills require great strength and sometimes exaggerated joint ROM.13 In contrast, basketball players often perform upper extremity passing, shooting, and dribbling skills while wearing shoes on flat, stiff surfaces. Their skills require great joint accelerations from jump landings and cutting maneuvers.14 Soccer players often perform lower extremity passing, shooting, and dribbling skills while wearing cleated or noncleated shoes on variable turf conditions.15 The skill requirements and environmental demands of these aforementioned sports likely pose different challenges to the sensorimotor

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systems that cumulatively may influence the balance abilities of trained athletes.

To our knowledge, studies comparing balance abilities among athletes competing in different sports do not exist. Therefore, our purpose was to compare static and dynamic balance among collegiate athletes currently competing or training in soccer, basketball, and gymnastics. We hypothesized that postural control would be different among athletes in these sports. An appreciation of postural control among athletes from different sports may give insight into whether sport demands influence balance and may help athletic trainers prescribe balance exercises more effectively.

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Go to: METHODS Subjects All female student-athletes from 3 sports (soccer, basketball, and gymnastics) at a National Collegiate Athletic Association (NCAA) Division I university were asked to volunteer to participate in this study. Thirty-four student-athletes (soccer, n = 11; basketball, n = 11; gymnastics, n = 12) met the inclusion criteria and agreed to participate. We chose female collegiate athletes to better represent a population that displays high rates of ligamentous injuries compared with male collegiate athletes in soccer and basketball.16 To be included in the study, participants had to be currently competing in only 1 sport for the previous 3 years and not be involved in a balance training program outside of their typical sport training. Participants were excluded if they had a lower extremity injury, vestibular problems (eg, vertigo), visual problems (eg, blind in one eye), or a concussion in the 12 weeks before the study. These exclusions were assessed by questioning the participants and not through physical tests. Participants signed an informed consent document approved by the university ethics committee (which also approved the study) and were asked to refrain from any exercise for 2 hours before testing. The participants' mean age and leg length (mean of both limbs), respectively, were 20.4 ± 1.1 years and 84.3 ± 2.9 cm for soccer, 21.6 ± 1.9 years and 94.8 ± 6.1 cm for basketball, and 21.2 ± 1.7 years and 82.04 ± 4.0 cm for gymnastics.

Protocol Participants attended a university athletic training facility for 1 test session that included assessment of static balance, dynamic balance, and leg length. For assessment of leg length, we used a tape measure to determine the distance (to the

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nearest millimeter) between the anterior superior iliac spine and the medial malleolus of the same leg.17 Both legs were measured, and limb dominance was determined by asking the participant which leg she preferred for kicking a ball.

Static balance and dynamic balance were then randomly evaluated using the equipment and procedures described later.

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Equipment Static balance was assessed using the Balance Error Scoring System (BESS) described by Riemann et al.18 The unstable surface consisted of a 50 × 41 × 6 cm closed-cell foam Airex Balance Pad (Alcan Airex AG, Sins, Switzerland). The stable surface was low-pile carpeting. Dynamic balance was assessed using the Star Excursion Balance Test (SEBT) described by Gribble and Hertel.17 The testing grid consisted of 8 lines, each 120 cm in length extending from a common point at 45° angle increments (Figure 1), and was created using standard white athletic tape placed on a firm, textured tile surface. The middle of the grid was marked with a small dot that athletes were asked to center the stance foot over during testing. The grid was marked at 1-cm increments from the center outward to facilitate scoring during testing. Researchers have reported high intertester reliability (intraclass correlation coefficients = .78 to .96) and fair to good validity (r = .42 to .79) coefficients for the BESS18 and high intratester reliability for the SEBT (intraclass correlation coefficients = .78 to .96).19 Although no validity coefficients are available for the SEBT, authors20 have provided evidence that the SEBT is sensitive for screening various musculoskeletal injuries.

Figure 1 Top view of Star Excursion Balance Test grid. The grid displays directional terms for right leg dominance. Directional terms were mirrored for left leg dominance, and poses represent techniques for posterior and lateral directions Procedures

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The procedures for the BESS test involved 3 stance positions each on the stable and unstable surfaces for the dominant and nondominant limbs. The 3 stance positions were double-leg stance with feet together, single-leg stance on test limb with contralateral knee in approximately 90° of flexion, and tandem stance with the foot of the test limb in line and anterior to the foot of the contralateral limb (ie, the heel of the test foot touching the toes of the back foot). Each position was held with eyes closed and hands on hips for 20 seconds in duration, and scoring was determined by recording of errors. Errors included (1) opening eyes; (2) lifting hands from hip; (3) touchdown of non-stance foot; (4) step, hop, or other movement of the stance foot or feet; (5) lifting forefoot or heel; (6) moving hip into more than 30° of flexion or abduction; and (7) remaining out of position for longer than 5 seconds.18 The different stances, surfaces, and limb conditions produced 10 separate BESS tasks that were randomly assigned. The double-leg stance condition was not repeated for dominant and nondominant limbs.

The SEBT protocol described by Gribble and Hertel17 requires participants to maintain a stable single-leg stance with the test leg and to reach for maximal distance with the other leg in each of the 8 directions (Figure 1). Participants were asked to execute a touchdown without using the reach leg for support. If it was determined that the reach leg was used for support or the stable base of support was compromised, the trial was repeated. The leg tested (dominant, nondominant) and order of reach direction were randomly selected before testing, and a 5-second rest with a 2-footed stance was required between reach attempts. Three trials were performed for each limb, with a 120-second rest period between trials. Before testing, participants were given 180 seconds to familiarize themselves with the SEBT grid and were asked to practice reaching in each direction. This latter period resulted in 6 trials for most directions. Subjects were instructed to reach behind the stance leg when performing trials in the posterior directions (Figure 1). Visual cues, such as objects on the floor and people not involved in the study, were removed from the testing area to help reduce visual and auditory influences. No encouragement or further instruction was given to the participants throughout testing. Reach distance was marked with chalk on the floor immediately next to the athletic tape that corresponded to the site of touchdown. The distance from the center of the grid to the point of touchdown was measured with a tape measure, the value was recorded to the nearest millimeter, and the chalk mark was removed after each reach to reduce visual cues.

Data Analyses

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All scoring was performed by the same tester. The error scores from the BESS test were summed for each limb, and the distance scores (cm) for each direction of the SEBT grid were averaged over the 3 trials and normalized to leg length (reach distance/leg length × 100 = percentage of leg length).17 The normalized distances in each direction were then summed for both the dominant and nondominant leg.

We summed the values to reduce the number of statistical tests and minimize inflation of type I error.

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Statistical Design The independent variables in this study were the type of sport played (soccer, basketball, or gymnastics) and limb used during testing (dominant or nondominant). The dependent variables (errors and normalized distances) were each examined for main effects and interactions with a 3 (sport played) × 2 (limb) analysis of variance with repeated measures on the limb factor. Follow-up multiple comparisons were performed on the sport played factor. The analysis of variance was performed twice, once for each dependent variable. The probability associated with a type I error was set at 0.05 for all observations, and the conservative Scheffé model was used for multiple comparisons to help control for inflation of alpha. We used SPSS (version 13.0; SPSS Inc, Chicago, IL) to analyze our data.

Go to: RESULTS Measures of central tendency and spread for BESS and SEBT data are reported in the Table. No sport-by-limb interactions were noted for either the BESS (F2,31 = 1.46, P = .25, partial η2 = .09, 1 − β = .29) or the SEBT (F2,31 = 1.12, P = .34, partial η2 = .07, 1 − β = .23). Similarly, no main effects were seen for the limb factor for either the BESS (F1,32 = .028, P = .87, partial η2 = .001, 1 − β = .05) or the SEBT (F1,32 = 2.86, P = .10, partial η2 = .08, 1 − β = .37).

Balance Scores of the Soccer, Basketball, and Gymnastics Athletes*.

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Main effects were observed for the sport factor for the BESS (F2,31 = 5.25, P = .01, partial η2 = .25, 1 − β = .80) and the SEBT (F2,31 = 3.54, P = .04, partial η2 = .20, 1 − β = .62). Multiple comparisons revealed that BESS scores were different between basketball and gymnastics (P = .01, effect size = .86). Additionally, a difference between soccer and basketball was observed for SEBT scores (P = .04, effect size = 1.0). The BESS error scores for the gymnastics group were 55% lower than for the basketball group (Figure 2), and SEBT scores were 7% greater in the soccer than in the basketball group (Figure 3).

Figure 2 Balance Error Scoring System (BESS) values (mean ± SEM) for soccer, basketball, and gymnastics athletes. Values are the means for the dominant and nondominant limbs. *Indicates that gymnasts committed fewer errors than basketball players (more ...)

Figure 3 Star Excursion Balance Test (SEBT) values (mean ± SEM) for soccer, basketball, and gymnastics athletes. Values represent the means for the dominant and nondominant limbs. *Indicates that soccer players displayed greater reach distances (more ...)

Go to: DISCUSSION We hypothesized that static and dynamic balance scores would be different among collegiate athletes competing in different sports. Female basketball players demonstrated inferior static balance compared with gymnasts and inferior dynamic balance compared with soccer players. No differences were noted between gymnasts and soccer players. Although the idea that sport involvement improves balance is not new,4,5 our study extends this knowledge to particular sports and

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suggests that specific sensorimotor challenges, rather than just general sport activity, are important for the development of optimal balance.

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Our static balance scores for soccer players (12.5 ± 1.1) closely match the static balance scores reported by Riemann et al18 (12.2 ± 8.7) that included NCAA football, soccer, lacrosse, and wrestling athletes. The SEBT scores were more difficult to compare with those in the literature because of the different techniques used in analyzing data (eg, normalized versus nonnormalized).

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Within our study, the statistical differences observed among sports may, in part, be related to the unique sensorimotor challenges imposed by each sport. For example, gymnasts often practice motionless balance skills on the balance beam, similar to skills required in the BESS. Hence, gymnasts may develop superior attention focus on cues that alter balance performance, such as small changes in joint position and acceleration.12 In contrast, basketball players rarely balance motionless on one leg and often attend to ball and player position cues. Their static balance might be less developed than that of gymnasts, as supported by the results of this study. With respect to dynamic balance, soccer players often perform single-leg reaching movements outside their base of support during passing, receiving, and shooting, which may in part explain why their dynamic balance was better than basketball players' although no direct evidence supports this contention. Because static and dynamic balance scores were not different between soccer players and gymnasts, some sensorimotor challenges may be common in these 2 sports, or it may be that the BESS and SEBT were not sensitive enough to pick up the differences.

The specific changes in sensorimotor systems that result from sport participation are multifaceted. Some indirect evidence suggests the probability of detecting a change in joint position (proprioception) is improved after skill training21 and that learning to pay attention to biomechanical cues (eg, joint acceleration) may be the mechanism for this change.12 Training experiences that improve neuromuscular coordination, joint strength, and ROM are also likely mechanisms that lead to improved balance.5,11,22 Although strength and ROM data were not available for our groups, ground reaction force data from previous researchers suggest that soccer players and gymnasts experience greater forces than basketball players for some skill maneuvers.23–25 Hence, it may be that balance scores were different among groups in our study simply because of differences in joint strength. Future researchers may benefit from examining specific components of balance (eg, proprioception, vision, joint ROM, and strength) in athletes participating in different sports to determine which sensorimotor systems are more affected.

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Intuitively, balance training reduces the risk of some musculoskeletal injuries, such as ankle sprains, especially if one or more balance components (eg, proprioception and joint ROM) are not optimal at the start. The literature seems to support this contention in that athletes in different sports displayed fewer ankle sprains and other musculoskeletal injuries than control subjects after static and dynamic balance training.26–28 Athletic trainers will find a variety of balance training programs that may be effective at improving balance, including unipedal balance exercises on progressively challenging surfaces.1–3 In addition to knowing which balance training programs are effective, athletic trainers would benefit from knowing which athletes require more balance training to reduce musculoskeletal injuries. Because we observed inferior balance scores among basketball players and inferior balance scores may be a strong predictor of future ankle sprains,29 athletic trainers may find it useful to prescribe more balance training to basketball players than to soccer players and gymnasts. This is not to say that soccer players and gymnasts would not benefit from balance training but that balance exercises may be more necessary for basketball players.

The BESS and SEBT assessments may be considered limitations of this study.

Postural sway variables from a force platform have often been considered the ―gold standard‖ for measuring static balance,18 and although no gold standard has been defined for dynamic balance, more sophisticated techniques, such as the Dynamic Postural Control Index30 and the time-to-stabilization test, are available.31 Accordingly, a variety of balance tests exist and we therefore chose 2 tests that are reliable and considered by some to be valid.18,19 Practically, the BESS and SEBT require minimal equipment and are clinically ―friendly,‖ particularly when conducted with fewer trials or reach directions.32 Given that we observed differences in balance among athletes in 2 sports, an additional application of this study may be that athletic trainers will use these tests on athletes in sports that were not tested to help expedite the prescription of balance exercises.

Within these limitations, we can conclude that soccer players and gymnasts did not differ in terms of static and dynamic balance on the BESS or SEBT. In contrast, basketball players displayed inferior static balance to gymnasts and inferior dynamic balance to soccer players.

Go to: REFERENCES

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1. Gauffin H, Tropp H, Odenrick P. Effect of ankle disk training on postural control in patients with functional instability of the ankle joint. Int J Sports Med. 1988;9:141–144.[PubMed] 2. Rozzi SL, Lephart SM, Sterner R, Kuligowski L. Balance training for persons with functionally unstable ankles. J Orthop Sports Phys Ther.

1999;29:478–486.[PubMed] 3. Wester JU, Jespersen SM, Nielsen KO, Neumann L. Wobbleboard training after partial sprains of the lateral ligaments of the ankle: a prospective randomized study. J Orthop Sports Phys Ther. 1996;28:332–336.

4. Aydin T, Yildiz Y, Yildiz C, Atesalp S, Kalyon TA. Proprioception of the ankle: a comparison between female teenaged gymnasts and controls. Foot Ankle Int. 2002;23:123–129.[PubMed] 5. Lephart SM, Giraldo JL, Borsa PA, Fu FH. Knee joint proprioception: a comparison between female intercollegiate gymnasts and controls. Knee Surg Sports Traumatol Arthrosc. 1996;4:121–124.[PubMed] 6. Winter DA, Patla AE, Frank JS. Assessment of balance control in humans.

Med Prog Technol. 1990;16:31–51.[PubMed] 7. Grigg P. Peripheral neural mechanisms in proprioception. J Sport Rehabil.

1994;3:2–17.

8. Nashner LM, Black FO, Wall C., 3rd. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci.

1982;2:536–544.[PubMed] 9. Palmieri RM, Ingersoll CD, Cordova ML, Kinzey SJ, Stone MB, Krause BA. The effect of a simulated knee joint effusion on postural control in healthy subjects. Arch Phys Med Rehabil. 2003;84:1076–1079.[PubMed] 10.Palmieri RM, Ingersoll CD, Stone MB, Krause BA. Center-of-pressure parameters used in the assessment of postural control. J Sport Rehabil.

2002;11:51–66.

11.Balter SGT, Stokroos RJ, Akkermans E, Kingma H. Habituation to galvanic vestibular stimulation for analysis of postural control abilities in gymnasts.

Neurosci Lett. 2004;366:71–75.[PubMed] 12.Ashton-Miller JA, Wojtys EM, Huston LJ, Fry-Welch D. Can proprioception really be improved by exercises? Knee Surg Sports Traumatol Arthrosc. 2001;9:128–136.[PubMed] 13.Hay JG. The Biomechanics of Sports Techniques. 4th ed. Englewood Cliffs, NJ: Prentice Hall; 1993:528.

14.McClay IS, Robinson JR, Andriacchi TP. A kinematic profile of skills in professional basketball players. J Appl Biomech. 1994;10:205–221. et al.

15.Orchard J. Is there a relationship between ground and climatic conditions and injuries in football? Sports Med. 2002;32:419–432.[PubMed]

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16.Agel J, Arendt EA, Bershadsky B. Anterior cruciate ligament injury in National Collegiate Athletic Association basketball and soccer: a 13-year review. Am J Sports Med. 2005;33:524–530.[PubMed] 17.Gribble PA, Hertel J. Considerations for normalizing measures of the Star Excursion Balance Test. Measure Phys Educ Exerc Sci. 2003;7:89–100.

18.Riemann BL, Guskiewicz KM, Shields EW. Relationship between clinical and forceplate measures of postural stability. J Sport Rehabil. 1999;8:71–82.

19.Hertel J, Miller JS, Denegar CR. Intratester and intertester reliability during the Star Excursion Balance Tests. J Sport Rehabil. 2000;9:104–116.

20.Olmsted LC, Carcia CR, Hertel J, Shultz SJ. Efficacy of the Star Excursion Balance Tests in detecting reach deficits in subjects with chronic ankle instability. J Athl Train. 2002;37:501–506. [PMC free article][PubMed] 21.Fry-Welch D. Improvement in Proprioceptive Acuity with Training [dissertation] Ann Arbor, MI: University of Michigan; 1998.

22.Paterno MV, Myer GD, Ford KR, Hewett TE. Neuromuscular training improves single-limb stability in young female athletes. J Orthop Sports Phys Ther. 2004;34:305–316.[PubMed] 23.McClay IS, Robinson JR, Andriacchi TP. A profile of ground reaction forces in professional basketball. J Appl Biomech. 1994;10:222–236. et al.

24.McNitt-Gray JL. Kinematics and impulse characteristics of drop landings from three heights. Int J Sport Biomech. 1991;7:201–224.

25.Smith N, Dyson R, Hale T, Janaway L. Contributions of the inside and outside leg to maintenance of curvilinear motion on a natural turf surface.

Gait Posture. In press.

26.Caraffa A, Cerulli G, Projetti M, Aisa G, Rizzo A. Prevention of anterior cruciate ligament injuries in soccer: a prospective controlled study of proprioceptive training. Knee Surg Sports Traumatol Arthrosc. 1996;4:19– 21.[PubMed] 27.Emery CA, Cassidy JD, Klassen TP, Rosychuk RJ, Rowe BH. Effectiveness of a home-based balance-training program in reducing sports-related injuries among healthy adolescents: a cluster randomized controlled trial. CMAJ. 2005;172:749–754. [PMC free article][PubMed] 28.McGuine TA, Keene JS. The effect of a balance training program on the risk of ankle sprains in high school athletes. Am J Sports Med. 2006;34:1103– 1111.[PubMed] 29.McGuine TA, Greene JJ, Best T, Leverson G. Balance as a predictor of ankle injuries in high school basketball players. Clin J Sport Med. 2000;10:239–244.[PubMed]

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30.Wikstrom EA, Tillman MD, Smith AN, Borsa PA. A new force-plate technology measure of dynamic postural stability: the dynamic postural stability index. J Athl Train. 2005;40:305–309. [PMC free article][PubMed] 31.Ross SE, Guskiewicz KM. Time to stabilization: a method for analyzing dynamic postural stability. Athl Ther Today. 2003;8((3)):37–39.

32.Hertel J, Braham RA, Hale SA, Olmsted-Kramer LC. Simplifying the Star Excursion Balance Test: analysis of subjects with and without chronic ankle instability. J Orthop Sports Phys Ther. 2006;36:131–137.[PubMed]

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MEASURING FITNESS IN FEMALE GYMNASTS: THE GYMNASTICS FUNCTIONAL MEASUREMENT TOOL Mark D. Sleeper, MS, PT, OCS,1 Lisa K. Kenyon, PT, PhD, PCS,2 and Ellen Casey, MD34 Author information ► Copyright and License information ► Go to: Abstract Purpose/Background: A reliable and valid method of measuring and monitoring a gymnast's total physical fitness level is needed to assist female gymnasts in achieving healthy, injury-free participation in the sport. The Gymnastics Functional Measurement Tool (GFMT) was previously designed as a field-test to assess physical fitness in female competitive gymnasts. The purpose of this study was to further develop the GFMT by establishing a scoring system for individual test items and to initiate the process of establishing the test-retest reliability and construct validity of the GFMT. Methods: A total of 105 competitive female gymnasts ages 6-18 underwent testing using the GFMT. Fifty of these subjects underwent re-testing one week later in order to assess test-retest reliability. Construct validity was assessed using a simple regression analysis between total GFMT scores and the gymnasts' competition level to calculate the coefficient of determination (r2). Test-retest reliability was analyzed using Model 1 Intraclass correlation coefficients (ICC). Statistical significance was set at the p<0.05 level.

Results:

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The relationship between total GFMT scores and subjects' current USAG competitive level was found to be good (r2 = 0.60). Reliability testing of the GFMT total score showed good test-retest reliability over a one week period (ICC=0.97).

Test-retest reliability of the individual component items was good (ICC = 0.800.92).

Conclusions:

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The results of this study provide initial support for the construct validity and testretest reliability of the GFMT. Go to: INTRODUCTION Women's competitive gymnastics is a multifaceted sport that requires a high level of physical fitness and skill to succeed. Speed,1–4 strength,2,3,5,6 endurance,5 agility,7 flexibility,3,8–12 balance,2,13 and power8,14–16 are all physical abilities that play a role in the success of a competitive gymnast. A gymnast's physical abilities may also be related to the ability to sustain injury free participation in the sport.7,17–19 As such, it is imperative that the coaches, trainers, and therapists involved in the sport be able to monitor an individual gymnast's physical abilities and overall fitness level as a means of promoting healthy, injury-free participation in the sport.

Traditionally, field-testing has been done in a variety of sports in an effort to measure sport-specific physical abilities.20–28 For example, speed, power and agility are physical abilities needed for success in the sport of soccer. Field-tests have been developed in an attempt to quantify each of those physical abilities.26,29,30 Some field-tests, such as the hop test31 or the agility T-test,32 focus on a specific aspect of sport function. Other tests, such as the Functional Movement Screen™ (FMS™),33,34 include a battery of individual items designed to assess an athlete's abilities across multiple aspects of function.

Within the United States Association of Gymnastics (USAG), a system of competitive levels ranging from a low of 4 to a high of 10 is used to rank the skills and abilities of individual gymnasts. To move from one competitive level to the next, a gymnast must achieve a specific all-around score and be able to perform specific skills that increase in difficulty as the competitive level increases.

Individual tests for flexibility, strength, endurance, and power have been suggested as useful tools to gauge gymnastic potential.35–38 These physical abilities are included in the USAG Talent Opportunity Programs (TOPs) Test, a multi-test

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battery designed to measure a gymnast's basic skill in addition to the physical abilities of strength, endurance, power, and flexibility.39 Although the TOPs protocol has changed a number of times since its development by William Sands,37 it is used primarily with young club gymnasts ages 7-10 years of age to identify competitive potential and aid in the development of the United States competitive gymnastics program. The TOPs was thus not designed to address the needs of gymnasts of all ages or those who compete through high school or collegiate programs. While specialized training is needed to administer the TOPs and the number of people deemed qualified to administer the test is limited, the reliability and validity of the TOPs test have not been reported.

Currently there is not a reliable and valid measurement tool to evaluate the specific physical fitness abilities needed for successful competition in either men's or women's gymnastics. Previous studies have examined possible correlations between a gymnast's level of competition or intensity of training and various singular physical fitness traits.3,12,40 Nelson and co-workers3 investigated the relationship between gymnasts' flexibility and strength and varying training intensity levels. The gymnasts at the highest level of training were reported to be the most flexible, had a slender body type, weighed less, and demonstrated higher amounts of both functional and absolute strength especially in the upper body. In 1989, Faria et al41 examined the relationship between anthropometric and physical characteristics of male gymnasts and overall competitive performance success.

These researchers concluded that the top gymnasts were stronger in both absolute upper body strength and upper body strength relative to bodyweight, possessed greater overall flexibility through the hip region, shoulder girdle, and back, and possessed the least percentage of body fat.41 Neither of these studies used a standardized measurement tool to determine an overall fitness score or explore the relationship between age or body weight and physical abilities.

Without a reliable and valid field-test for measuring gymnasts' physical abilities, fitness evaluation and training are often left to the tradition-driven ways of individual coaches. As stated by Sands,19 ―…. Gymnasts often simply ‗trick‘ themselves into shape meaning they perform skills over and over until they acquire the fitness and skill to perform the movement‖.(p.367) This may lead to an athlete who is simply fit to do certain skills but who does not have the overall fitness level necessary for prolonged participation in the sport. With the consistent increases in the complexity and difficulty of the gymnastics elements being performed during competition,7 a reliable and valid method of measuring and monitoring gymnast's total physical fitness levels is needed to collectively measure the physical abilities of gymnasts and monitor their physical state.

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Establishing the reliability and validity of a measurement tool is a multi-step and complex process that must be investigated within the context of the tool's intended use. Various types of validity must be considered when evaluating a new measurement tool. Construct validity, or the ability of a tool to measure the abstract concept it is intended to evaluate, is one type of validity that must be assessed. Methods of construct validation include convergence and discrimination, factor analysis, the known groups method, criterion validation, and hypothesis testing.42 Methods related to hypothesis testing are based on the ability of a measurement tool to reflect specific assumptions that form the framework underlying the theoretical basis of the construct. Given that a single study cannot definitively verify a theory, construct validation is considered to be an on-going process.

Various forms of reliability such as intra-rater reliability, inter-reliability and testtest reliability must also be considered when evaluating a measurement tool. Testretest reliability is used to establish that a tool will obtain the same results across repeated administrations of the same test. Intervals between test administrations must be long enough to avoid the impact of factors such as subject fatigue and learning effects but close enough to avoid true changes in the measured variable.

Overview of the GFMT The Gymnastics Functional Measurement Tool (GFMT) was developed to assess a gymnast's overall fitness level while minimizing the impact of gymnastic skill on testing scores.43,44 Identifying fitness deficits to be targeted for improvement as part of a gymnast's individual training regime may prove useful in injury prevention. As a field-test for female competitive gymnasts of all ages, the GFMT was designed to be carried out by coaches, trainers and therapists using equipment commonly found in any gymnastics gym (club, high school, collegiate, etc.).

Given that successful participation in women's competitive gymnastics requires a combination of abilities related to flexibility, speed, power, strength, muscular endurance, and balance,1–16 the individual items of the GFMT were developed based on knowledge of these requirements, a review of the literature, and consultation with experts in the field of women's gymnastics.43,44 The 10 items comprised in the GFMT are summarized in Table 1 and detailed in Appendix I.

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Table 1.

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Individual Items Comprising the GFMT.

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The purpose of this study was to continue developing the GFMT by establishing a scoring system for individual test items and initiating the process of establishing test-retest reliability and construct validity. Given the authors' belief that a gymnast's total GFMT score would vary based on her current USAG competitive level, construct validity was assessed using the known-groups method of construct validation.

Go to: METHODS Approval for the study was obtained from the Office for the Protection of Research Subjects at Northwestern University. Healthy competitive female gymnasts were recruited from gymnastics clubs throughout the Midwestern and Mid-Atlantic United States. Inclusion criteria required the subjects to be female, between 6 and 18 years of age, and competitive in gymnastics at USAG levels 4 to 10. Exclusion criteria included musculoskeletal pathology currently limiting the gymnast's ability to train or compete; a history of, or current systemic illnesses including cardiovascular or pulmonary disease; musculoskeletal disease or rheumatoid arthritis; and a lack of informed assent given by the participant or consent given by the parent/legal guardian. A total of 105 subjects participated in the study. Refer to Figure 1 for a flowchart reflecting subjects' participation in the study.

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Figure 1.

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Flowchart reflecting subject's participation in study.

All testing was performed in the subjects' home gyms or in a gym familiar to the subject. Subjects did not have prior knowledge or exposure to the specific items composing the GFMT. Each subject provided her own USAG competition level which was recorded by the testers. Prior to testing, subjects completed their regular, coach-directed warm-up routines without regard to the requirements of the GFMT. Given that field-tests composed of multiple items are often administered in stations each consisting of an individual item,43,44 subjects were placed into groups of 10 to 12 and moved through each of the 10 stations to complete the GFMT. Data was collected by second year Doctor of Physical Therapy students from Northwestern University and by gymnastics coaches with a minimum of 5 years of coaching experience. In an effort to simulate actual practice patterns,45–47 all data collectors were provided with a detailed set of instructions for administering each item on the GFMT but did not undergo any specialized or extensive training. Raw data for each item of the GFMT was recorded in units of measurement that were appropriate for the item tested. Units of measurement for the raw data of each item are listed in Table 1. Subjects were not intentionally masked as to their item scores.

Individual GFMT items were completed in the following order to help reduce the effects of regional fatigue: Rope Climb Test, Jump Test, Hanging Pikes Test, Shoulder Flexibility Test, Agility Test, Over-grip Pull-up Test, Splits Test, Pushup Test, 20-yard Sprint Test and Handstand Hold Test. Subjects were given a minimum of 5 to 10 minutes rest between administrations of each item of the GFMT. From the 105 total subjects, a convenience sample of 50 subjects was chosen to participate in test-retest reliability testing. These 50 subjects were retested with the GFMT one week after initial testing. Test conditions and administration were consistent between the 2 administrations of the GFMT including warm-up and item order. To help ensure that test-retest reliability rather than intra-rater reliability was

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assessed, testers administered different items from the GFMT on each of the 2 administration dates.

Go to: STATISTICAL METHODS

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Development of the Scoring System To develop the scoring system for the GFMT, raw scores in the appropriate units of measurement were recorded for each of the individual items on the GFMT. The raw scores for each item were used to calculate the range, mean, and standard deviation for each individual item of the GFMT (n=105). Data was then transformed to an ordinal scale using the following procedure. In an attempt to reduce the possibility of ceiling and floor effects, 5 percent of the total range of the raw scores was added to the high score of each item and 5 percent was subtracted from the low score of each item. The resulting range of scores for each individual item was then divided by 11 to create a 0 to 10 ordinal scale for each individual item on the GFMT.48–50 The ordinal scale for each item was used to create a total GFMT score out of a possible 100 points (10 points for each item). Based on these findings, the scoring for each individual item and for the total GFMT score were finalized and are provided in the GFMT Score Sheet found in Appendix II. Test-retest and Construct Validity: Test-retest reliability was analyzed using Model 1 Intraclass correlation coefficients (ICC).34 Although a process of systematic randomization was not employed in the study, a Model 1 ICC was used to reflect the concept that individual items on the GFMT were administered by different testers on each of the 2 test dates.42 The variance assessed was thus restricted to differences in the subjects' scores in the test-retest design and necessitated the use of a Model 1 ICC.42 Given that previous studies had reported a positive relationship between various singular fitness traits and a gymnast's level of competition,2,51,52 it was theorized that the total scores on the GFMT would vary with a gymnast's current competitive level. This was based upon the concept that at each increasing competitive level, a gymnast is required to perform increasingly difficult skills that require a related increase in the gymnast's physical abilities. Construct validity was thus evaluated based on the authors' belief that there would be a direct linear relationship between a gymnast's physical abilities as measured by the GFMT and the gymnast's current

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level of competition as reflected by the gymnast's USAG level. A simple regression analysis was performed using USAG competitive level to predict total GFMT score.42 The coefficient of determination (r2) was used to explore this relationship.42 Statistical significance was set at the p<0.05 level.

Go to:

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RESULTS Of the 148 subjects assessed for eligibility in this study, 105 subjects participated.

Forty-three of the recruited subjects were excluded from the study due to recent injury (n=38) or the lack of a signed informed consent or assent (n=5). The mean age of participating subjects was 12.64 years with these subjects reporting participation in competitive gymnastics for a mean of 5.4 years. Mean height and weight of the subjects were 42.76 kg and 149 cm respectively. Subject demographics, categorized by USAG competition level, are summarized in Table 2. Mean GFMT component test raw scores and standard deviations are presented in Table 3.

Table 2.

Subject Demographics by Competitive Level.

Table 3.

Mean and Standard Deviation of GFMT Individual Item Scores and GFMT Total Scores (n = 105).

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Raw scores for all items on the GFMT demonstrated a normal distribution with the exception of the Handstand Test, which presented with a right skew. This skew possibly reflects the complexity of this particular activity. The relationships between the subjects' current USAG competitive level and individual component raw scores are presented in Table 4. As indicated in Table 4, several of these relationships were statistically significant, however, r2 values demonstrated moderate to poor relationships between USAG competitive level and individual component raw scores (r2 = 0.05-0.47). The relationship between total GFMT scores (out of a possible score of 100) and the subjects' current USAG competitive level was found to be good (r2 = 0.62). Figure 2 demonstrates the relationship between USAG competitive level and total GFMT Scores. To rule out alternative explanations for the relationship between USAG competitive level and total GFMT scores, the relationships between total GFMT scores and age and total GFMT scores and bodyweight were also explored. Statistically significant relationships were identified between total GFMT score and age and between total GFMT score and bodyweight (r2 = 0.13). However, r2 values demonstrated a poor relationship between total GFMT score and age (r2 = 0.29) and between total GFMT score and bodyweight (r2 = 0.13).

Table 4.

Relationship between GFMT Individual Test Raw Score and Composite Score and the Subjects' Current Competitive Level, Body Weight and Age (n = 105).

Figure 2.

Relationship between USAG score and GFMT score.

Raw item scores were used to examine the test-retest reliability for each item on the GFMT. Test-retest reliability of total GFMT scores was also determined.

Reliability testing of the GFMT total score showed good test-retest reliability over

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a one week period (ICC=0.97). Test-retest reliability of the individual component tests was good to excellent (ICC = 0.80-0.92).42 Reliability coefficients are shown in Table 5. A statistically significant difference (p<0.05) between the first and second test scores was identified for the GFMT Total score and for the following test items: the Hanging Pikes Test, the Vertical Jump Test, and the Splits Test.

Table 5.

Score Means and Standard Deviations for Both Test Days and Intraclass Correlation Coefficients for Test Retest Reliability (n=50).

Go to: DISCUSSION The GFMT provides the coaches, trainers, and therapists who work with female gymnasts of any age or competitive level with a functional tool designed to assess the unique aspects of fitness that are necessary for safe and effective participation in the sport. Given that the GFMT was developed as a field-test that can be administered without extensive training using equipment readily available in a gymnastics gym, the authors believe that the GFMT can be easily incorporated into any gymnastics program. Identifying fitness deficits that can be targeted as part of a gymnast's individual training regime may prove useful in injury prevention.

Raw data collected in this study was used to develop the scoring system for the GFMT. Transformation of the raw data for each individual item to an ordinal scale allowed for a total GFMT score out of a possible 100 points (10 points for each item) and permitted raw data based on a variety of units of measurement to be considered within a total score. As reflected in Appendix I, the raw score for the Rope Climb item reflects both the amount of time needed to complete the climb and the qualitative analysis of the climbing technique used by the gymnast during the climb. Scoring for this item thus reflects a 0 to 5 ordinal scale for time developed using the procedures outlined above as well as a 0 to 5 score for climbing technique as outlined in Appendix I.

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The results of this study provide initial support for the construct validity and testretest reliability of the GFMT. Although construct validity is only one of the many forms of validity to be considered when evaluating a measurement tool,42,46 the relationship between a gymnast's total GFMT score and current USAG competitive level provides support for the concept that GFMT scores will vary based on a gymnast's current competitive level. Examining data from the individual items comprising the GFMT reveals that certain items such as the Jump Test, the Agility Test, and the 20-Yard Sprint Test relate more strongly to a gymnast's current competitive level than items such as the Shoulder Flexibility Test and the Splits Test. Despite the variations in the strength of the relationship between individual items and competitive level, the authors believe that all items on the GFMT must be administered to fully assess a gymnast's fitness across multiple domain areas (strength, flexibility, power, etc.). Maintaining a complete representation of fitness within the GFMT is necessary in order to adequately identify a gymnast's fitness deficits and aid in the development of a fitness program tailored to address individual fitness needs.

The procedures and methods used in this study allowed the researchers to evaluate the GFMT within the context of its intended use as a field-test to assess a gymnast's overall fitness level while minimizing the impact of gymnastic skill on testing scores.43,44 As such, testing was conducted in a manner consistent with the sport in an environment familiar to the individual athletes. Each item on the GFMT was administered at a separate station by different testers to reflect the common practices of field-test administration. Testers were intentionally provided with detailed instructions for administering each item but did not undergo extensive or additional training. Results are therefore felt to reflect the application of the GFMT within the setting for which it was intended to be used.

The intended purpose and use of a measurement tool dictate the relative importance of various forms of reliability. Given that the GFMT was designed as a physical fitness field-test, assessment of test-retest reliability was felt to be essential. The one week interval between test administrations attempted to control for factors such as fatigue or learning effects that may have impacted a gymnast's performance while trying to avoid enough passage of time to permit a true change in a gymnast's overall fitness.

This study was limited by several factors. The total number of participants at any given USAG level ranged from 9 to 21. Increasing these numbers to ≥30 participants at each USAG level may have yielded different results. Although methods such as using physical therapy students and coaches to collect the data

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may have helped to reflect the use of the GFMT within the context of its intended use, greater methodological control and therefore different results may have been obtained through the use of more stringent techniques such as employing highly trained, researching physical therapists to collect the data. While attempts were made in the test-retest procedures to decrease the possibility of a practice or learning effect, the authors' recognize that such factors may have impacted score differences between the first and second administrations of the GFMT. Further research is needed to continue the process of establishing the various types of reliability and validity of the GFMT. The possibility of correlations between total GFMT score and such factors as body composition/percentage of body fat and body mass index must be explored. Future studies should also explore the ability of the GFMT total score and individual item scores to identify a gymnast's risk for specific injuries and whether the GFMT could be used to help determine if and when an injured gymnast can safely resume high-level training and competition.

Finally, since the GFMT was developed exclusively for female gymnasts, a different tool that reflects the demands and specifications of men's competitive gymnastics should also be developed.

Go to: CONCLUSION Although the process of establishing the reliability and validity of any measurement tool is a complex and lengthy procedure, the results of this study provide initial support for the construct validity and test-retest reliability of the GFMT. Go to: APPENDIX 1: INSTRUCTIONS FOR ADMINISTRATION OF THE GFMT. Click on image to zoom

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Go to: APPENDIX 2 Click on image to zoom

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Go to: References

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1. Bradshaw E.Target-directed running in gymnastics: a preliminary exploration of vaulting. Sports Biomech. Jan 2004;3(1):125–144. [PubMed] 2. Lindner KJ, Caine DJ, Johns DP.Withdrawal predictors among physical and performance characteristics of female competitive gymnasts. J Sports Sci. Autumn 1991;9(3):259–272. [PubMed] 3. Nelson JK, Johnson BL, Smith GC.Physical characteristics, hip flexibility and arm strength of female gymnasts classified by intensity of training across age. J Sports Med Phys Fitness. Mar 1983;23(1):95–101. [PubMed] 4. Sands W, McNeal J, Borms J, Jemni M.Sprint characteristics of talent-selected female gymnasts age 9-11 years. International Science in Gymnastics Symposium.

Vol Annaheim, CA: USA-Gymnastics; 2003.

5. Bradshaw EJ, Le Rossignol P.Anthropometric and biomechanical field measures of floor and vault ability in 8 to 14 year old talent-selected gymnasts. Sports Biomech. Jul 2004;3(2):249–262. [PubMed] 6. Sands W, Caine D, Borms J.Scientific Aspects of Women's Gymnastics.

Medicine and Sports Science. 2003;45.

7. Daly RM, Bass SL, Finch CF.Balancing the risk of injury to gymnasts: how effective are the counter measures? Br J Sports Med. Feb 2001;35(1):8–18; quiz 19. [PMC free article][PubMed] 8. Delas S, Babin J, Katic R.Effects of biomotor structures on performance of competitive gymnastics elements in elementary school female sixth-graders. Coll Antropol. Dec 2007;31(4):979–985. [PubMed] 9. Kirby RL, Simms FC, Symington VJ, Garner JB.Flexibility and musculoskeletal symptomatology in female gymnasts and age-matched controls. Am J Sports Med. May-Jun 1981;9(3):160–164. [PubMed] 10. Knapik JJ, Bauman CL, Jones BH, Harris JM, Vaughan L.Preseason strength and flexibility imbalances associated with athletic injuries in female collegiate athletes. Am J Sports Med. Jan-Feb 1991;19(1):76–81. [PubMed] 11. Knapik JJ, Jones BH, Bauman CL, Harris JM.Strength, flexibility and athletic injuries. Sports Med. Nov 1992;14(5):277–288. [PubMed] 12. Maffulli N, King JB, Helms P.Training in elite young athletes (the Training of Young Athletes (TOYA) Study): injuries, flexibility and isometric strength. Br J Sports Med. Jun 1994;28(2):123–136. [PMC free article][PubMed] 13. Peltenburg AL, Erich WB, Bernink MJ, Huisveld IA.Selection of talented female gymnasts, aged 8 to 11, on the basis of motor abilities with special reference to balance: a retrospective study. Int J Sports Med. Feb 1982;3(1):37–42.

[PubMed] 14. Bencke J, Damsgaard R, Saekmose A, Jorgensen P, Jorgensen K, Klausen K.Anaerobic power and muscle strength characteristics of 11 years old elite and

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non-elite boys and girls from gymnastics, team handball, tennis and swimming.

Scand J Med Sci Sports. Jun 2002;12(3):171–178. [PubMed] 15. Delas S, Zagorac N, Katic R.Effects of biomotor structures on performance of competitive gymnastics elements in elementary school male sixth-graders. Coll Antropol. Jun 2008;32(2):443–449. [PubMed] 16. Jemni M, Sands WA, Friemel F, Stone MH, Cooke CB.Any effect of gymnastics training on upper-body and lower-body aerobic and power components in national and international male gymnasts? J Strength Cond Res. Nov 2006;20(4):899–907. [PubMed] 17. Fellander-Tsai L, Wredmark T.Injury incidence and cause in elite gymnasts.

Arch Orthop Trauma Surg. 1995;114(6):344–346. [PubMed] 18. Lindner K, Caine D.Injury predictors among female gymnasts' anthropometric and performance characteristics. In: Hermans G, Mosterd W, , editors. , eds.

Sports, Medicine and Health. Amsterdam: Excerpta Medica; 1990:136–141.

19. Sands WA.Injury prevention in women's gymnastics. Sports Med. Nov 2000;30(5):359–373. [PubMed] 20. Nimmerichter A, Williams C, Bachl N, Eston R.Evaluation of a field test to assess performance in elite cyclists. Int J Sports Med. Mar 2010;31(3):160–166.

[PubMed] 21. Chamari K, Chaouachi A, Hambli M, Kaouech F, Wisloff U, Castagna C.The five-jump test for distance as a field test to assess lower limb explosive power in soccer players. J Strength Cond Res. May 2008;22(3):944–950. [PubMed] 22. Gonzalez-Haro C, Galilea PA, Drobnic F, Escanero JF.Validation of a field test to determine the maximal aerobic power in triathletes and endurance cyclists. Br J Sports Med. Mar 2007;41(3):174–179. [PMC free article][PubMed] 23. Girard O, Chevalier R, Leveque F, Micallef JP, Millet GP.Specific incremental field test for aerobic fitness in tennis. Br J Sports Med. Sep 2006;40(9):791–796.

[PMC free article][PubMed] 24. Wonisch M, Hofmann P, Schwaberger G, von Duvillard SP, Klein W.Validation of a field test for the non-invasive determination of badminton specific aerobic performance. Br J Sports Med. Apr 2003;37(2):115–118. [PMC free article][PubMed] 25. Dabonneville M, Berthon P, Vaslin P, Fellmann N.The 5 min running field test: test and retest reliability on trained men and women. Eur J Appl Physiol. Jan 2003;88(4–5):353–360. [PubMed] 26. Wragg CB, Maxwell NS, Doust JH.Evaluation of the reliability and validity of a soccer-specific field test of repeated sprint ability. Eur J Appl Physiol. Sep 2000;83(1):77–83. [PubMed]

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27. Vanlandewijck YC, Daly DJ, Theisen DM.Field test evaluation of aerobic, anaerobic, and wheelchair basketball skill performances. Int J Sports Med. Nov 1999;20(8):548–554. [PubMed] 28. Laconi P, Melis F, Crisafulli A, Sollai R, Lai C, Concu A.Field test for mechanical efficiency evaluation in matching volleyball players. Int J Sports Med. Jan 1998;19(1):52–55. [PubMed] 29. Labsy Z, Collomp K, Frey A, De Ceaurriz J.Assessment of maximal aerobic velocity in soccer players by means of an adapted Probst field test. J Sports Med Phys Fitness. Dec 2004;44(4):375–382. [PubMed] 30. Nicholas CW, Nuttall FE, Williams C.The Loughborough Intermittent Shuttle Test: a field test that simulates the activity pattern of soccer. J Sports Sci. Feb 2000;18(2):97–104. [PubMed] 31. Gauffin H, Pettersson G, Tegner Y, Troop H.Function testing in patients with old rupture of the anterior cruciate ligament. Int J Sports Med. 1990;11(1):73–77.

[PubMed] 32. Pauole K, Madole K, Garhammer J, Lacourse M, Rozenek R.Reliability and validity of the T-test as a measure of agility, leg power, and leg speed in collegeaged men and womenJ Strength Condition Res. 2000;14(4):443–450.

33. Cook G, Burton L, Hoogenboom B.Pre-participation screening: the use of fundamental movements as an assessment of function - Part 1North Am J Sports Phys Ther. 2006;1(2):62–72. [PMC free article][PubMed] 34. Cook G, Burton L, Hoogenboom B.Pre-participation screening: the use of fundamental movements as an assessment of function - Part 2North Am J Sports Phys Ther. 2006;1(3):132–139. [PMC free article][PubMed] 35. Bajin B.Talent Identification Program for Canadian Female Gymnasts. In: Petiot B, Salmela JHHoshizaki TB, , editors. , eds. World Indentification Systems for Gymnastic Talent. Montreal: Sports Psyche Editions; 1987.

36. Ho R.Talent Identification in China. In: Petiot B, Salmela JHHoshizaki TB, , editors. , eds. World Identification Systems for Gymnastic Talent. Montreal: Sports Psyche Editions; 1987.

37. Sands W.Physical Abilities Profile - 1993 National TOPs testing. Technique.

Vol 141994:15–20.

38. Sands WA.Olympic Preparation Camps 2000 - Physical Ability Testing.

Technique. 2000;20(10):6–19.

39. USA-GymnasticsOfficial National Tops Testing Website. 2005; Forth: http://www.usa-gymnastics.org/women/pages/elite_preelite_tops.php Accessed March 5, 2010.

40. Sawczyn S, Zasada M.The Aerobic and Anaerobic Power of the Best Young Gymnasts - Indication of Training Endurance Capabilities. Research Yearbook.

2007;13(1):86–89.

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41. Faria IE, Faria EW.Relationship of the anthropometric and physical characteristics of male junior gymnasts to performance. J Sports Med Phys Fitness.

Dec 1989;29(4):369–378. [PubMed] 42. Portney L, Watkins M.Foundations of Clinical Research: Applications to Practice. third ed. Upper Saddle River, NJ: Pearson/Prentice Hall; 2009.

43. Sleeper M, Beers M, Erwin M, et al. The Gymnastics Functional Measurement Tool: An Instrument for the Physical Assessment of Competitive Gymnasts. Paper presented at: American College of Sports Medicine 2006; Denver, CO. 44. Sleeper M, Casey E.The Gymnastics Functional Measurement Tool: A Valid way of Measuring Gymnastics Physical Abilities. Paper presented at: American Physical Therapy Association Combined Sections Meeting 2010; San Diego, CA. 45. Blackburn M, van Vliet P, Mockett SP.Reliability of measurements obtained with the modified Ashworth scale in the lower extremities of people with stroke.

Phys Ther. Jan 2002;82(1):25–34. [PubMed] 46. Sechrest L.Validity of measures is no simple matter. Health Serv Res. Oct 2005;40(5 Pt 2):1584–1604. [PMC free article][PubMed] 47. Strauss ME, Smith GT.Construct validity: advances in theory and methodology. Annu Rev Clin Psychol. 2009;5:1–25. [PMC free article][PubMed] 48. Rothstein J, Campbell S, Echternach J, Jette A, Knecht H, Rose S.Standards for test and measurements in physical therapy practice. Physical Therapy.

1991;71(8):589–622. [PubMed] 49. Rothstein J, Echternach J.Primer on Measurement: An Introductory Guide to Measurement Issues. 1st ed. Alexandria, VA: American Physical Therapy Association; 1993.

50. Streiner D, Norman G.Health Measurement Sclaes: A Practical Guide to Their Development and Use. 3rd ed. Oxford, England: Oxford University Press; 2003.

51. Grabinar MD, McKelvain R.Implementation of a Profiling/Prediction Test Battery in the Screening of Elite Men Gymnasts. In: Petiot B, Salmela JHHoshizaki TB, , editors. , eds. World Identification Systems for Gymnastic Talent. Montreal: Sports Psyche Editions; 1987.

52. Regnier G, Salmela HH.Predictors of Success in Canadian Male Gymnasts. In: Petiot B, Salmela JHHoshizaki TB, , editors. , eds. World Identification Systems for Gymnastic Talent. Montreal: Sports Psyche Editions; 1987.

Articles from International Journal of Sports Physical Therapy are provided here Skeletal Geometry and Indices of Bone Strength in Artistic Gymnasts

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Jodi N. Dowthwaite, Ph.D. and Tamara A. Scerpella, M.D. Author information ► Copyright and License information ► The publisher's final edited version of this article is available free at J Musculoskelet Neuronal Interact See other articles in PMC that cite the published article.

Go to:

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Abstract This review addresses bone geometry and indices of skeletal strength associated with exposure to gymnastic loading during growth. A brief background characterizes artistic gymnastics as a mechanical loading model and outlines densitometric techniques, skeletal outcomes and challenges in assessment of skeletal adaptation. The literature on bone geometric adaptation to gymnastic loading is sparse and consists of results for disparate skeletal sites, maturity phases, gender compositions and assessment methods, complicating synthesis of an overriding view. Furthermore, most studies assess only females, with little information on males and adults. Nonetheless, gymnastic loading during growth appears to yield significant enlargement of total and cortical bone geometry (+10 to 30%) and elevation of trabecular density (+20%) in the forearm, yielding elevated indices of skeletal strength (+20 to +50%). Other sites exhibit more moderate geometric and densitometric adaptations (5 to 15%). Mode of adaptation appears to be site-specific; some sites demonstrate marked periosteal and endosteal expansion, whereas other sites exhibit negligible or moderate periosteal expansion coupled with endocortical contraction. Further research is necessary to address sex, maturity- and bone tissue-specific adaptation, as well as maintenance of benefits beyond loading cessation.

Keywords: gymnastics, bone geometry, bone strength, mechanical loading, growth Go to: Introduction Artistic gymnastics has been studied extensively as a model of skeletal adaptation to mechanical loading. Both retrospective and prospective studies suggest that bone mineral accrual during growth is increased in gymnasts relative to nongymnasts at most measured sites.1–7 DXA-measured skeletal parameters are elevated in female gymnasts versus non-gymnasts in childhood,1,8–10 during puberty,10–13 post-menarche and at college age.12–15 Gymnastic adaptation appears

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to be dose-dependent, increasing with training intensity.9,16 Furthermore, in college-age females, gymnastic exposure and withdrawal have been associated with training and de-training effects, respectively increasing and decreasing areal bone mineral density.17 Comparisons of adult former gymnasts versus nongymnasts suggest that skeletal advantages are maintained after activity cessation and may persist in adulthood.1,18–22 However, there is limited prospective evidence linking pediatric advantages with continued benefits in adulthood, beyond training cessation. 12–13

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Most gymnast versus non-gymnast comparisons use dual energy X-ray absorptiometry (DXA) to evaluate bone mineral content (BMC) and areal bone mineral density (aBMD). These DXA studies often focus on the femoral neck and lumbar spine, but there is also considerable evidence of bone adaptation in the upper extremity. 3,8–10,12–16 A subset of studies have assessed geometric adaptation underlying non-specific aBMD and BMC at appendicular sites;11,23–25 some have used pQCT to specifically assess cross-sectional bone geometry.22,26–29 Fewer studies have specifically investigated geometric adaptations at the lumbar spine and proximal femur.1,11,26,27 In contrast to weight-lifting and racquet sports, gymnastic activity applies impact loads that involve the total body mass, imparting high muscular loads and mass inertia to both upper and lower extremities.29 Gymnasts generate vertical ground reaction forces of approximately 3.5 to 10 times body weight (upper and lower extremities, respectively),30–31 rivaling lower extremity impact forces measured in other athletes.32–33 High resultant stresses in the bilateral upper extremities distinguish gymnastic from non-gymnastic loading, as most other activities preferentially load the dominant arm and generate lower stresses.

In simplified terms, gymnastic loading of the skeleton is dominated by axial compression and bending forces during tumbling, vaulting, beam and pommel horse work, while tension and torsion play a greater role during bar and ring work.

In reality, gymnastic loading generates a combination of compression, tension and shear stresses. ―Simple‖ axial compression generates bending forces in curved bones,34 resulting in compressive loads on the concave surface and tensile loads on the convex surface.35 Furthermore, compressive loads routinely generate shear stresses at a 45 degree angle to the loading axis.35 Accordingly, it is appropriate for assessment to include indices of skeletal strength related to axial compression, bending and torsion.

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It is difficult to summarize the body of knowledge regarding bone geometric adaptation to gymnastic loading, as the existing literature consists of results for disparate skeletal sites, maturity phases, gender compositions and assessment methods. The majority of published studies assess only females, with a preponderance of pediatric studies, and there are few reports discussing male or adult geometric adaptation. Consequently, this review focuses on females, but includes the sole published study involving males.27 A methodological context will be provided to outline current challenges and strategies for progress in this research area.

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Go to: Methodological Context In order to evaluate skeletal adaptation to gymnastic loading, it is important to isolate loading effects from unrelated sources of skeletal variation, including normal processes of growth and maturation. Effective research should compare individuals of similar physical maturity and account for variation in age, rate of maturation and body size. There is evidence that males and females differ in skeletal growth and geometric adaptation.36–40 The sole published study evaluating males and females did not detect significant interactions between sex and gymnastic activity for bone parameters in pre-pubertal subjects, except for diaphyseal cortical thickness at the radius (50% site).27 Due to the paucity of data on male gymnasts, this review will address only female adaptations.

Gymnastic studies are observational, because randomized controlled trials evaluating ―effects‖ of gymnastic exposure are unfeasible. To account for the limitations of observational studies, skeletal traits associated with gymnastic exposure are referred to in this review as ―gymnast advantages‖ (relative to nongymnasts), which may indicate higher (positive) or lower (negative) mean values.

Critically, studies are presented according to maturity status at the observation, but most gymnasts initiate training in childhood or early puberty. Accordingly, most results reflect loading during early development, with or without cumulative adaptation due to pubertal gymnastic exposure. To date, no studies reflect gymnastic exposure limited to later maturity phases.

In any context, in vivo assessment of the human skeleton is challenging. At present, the most thorough, sensitive and specific methods are limited by prohibitive costs, availability, radiation doses and other factors. Both quantitative computed tomography (QCT) and magnetic resonance imaging (MRI) evaluate

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skeletal geometry in three dimensions and allow isolation of the vertebral bodies from the posterior elements of the spine. For evaluation of distal sites, high resolution MRI (hrMRI) and hrQCT yield extremely detailed bone geometric results, including micro-architectural parameters (trabecular spacing, number, thickness, etc.).41 Peripheral QCT (pQCT) is a more readily available and feasible tool for assessment of cortical and trabecular cross-sectional geometry and density at distal appendicular sites (Figure 1a), with relatively low subject discomfort and radiation exposure.41 However, narrow pQCT regions of interest are sensitive to positional variation, as each 2mm slice provides a limited assessment of skeletal quality in a structure that may vary markedly between adjacent cross-sections.43,47–48 This issue is particularly influential in the growing metaphysis, where it is recommended that scans be positioned based on the physis or physeal scar to account for inter- and intra-individual structural variation.49–50 Unfortunately, determination of physeal references can be difficult and subjective, as appearance and location may vary between individuals, and from scan to scan within individuals.43

Figure 1 Figure 1a–b: (a) A schematic representation of pQCT images is presented for the distal radius (33% diaphysis, 4% metaphysis); (b) Schematic representations of simplified geometric models for derivations of geometric and strength indices are depicted (more ...)

In contrast, because DXA scans sample a broader length of bone, positional variation is less influential.43 However, standard DXA output represents a 2dimensional mean over the region of interest. Thus, higher BMC and aBMD values may indicate denser and/or larger bone and do not delineate tissue-specific geometry or density.10,43 In addition, fan beam magnification may affect scan results, although new generation DXA scanners have attempted to alleviate magnification error. In particular, supine lateral lumbar spine scans improve assessment of vertebral body BMAD and geometry. Nonetheless, magnification error and integrated spinal anatomy still pose problems in anteroposterior (AP) fan

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beam DXA studies of the proximal femur and spine that compare bodies of disparate or changing size.44–46 In contrast, at the distal radius, DXA-derived bone geometry and strength indices51 correlate well with pQCT-measures (strongest agreement for cortical CSA, Z/SSI, IBS: r=0.96, 0.92, 0.90; 33% total CSA, r=0.93, p<0.0001)43 (Table 1, Figure 1a and 1b); these derivations may provide a useful compromise between ―non-specific‖ DXA and overly-specific pQCT output, with favorable subject safety and comfort.43

Table 1 Skeletal Strength Indices Numerous skeletal strength indices have been utilized in studies of gymnastics and other loading modalities (Table 1). As noted previously, gymnastic loading generates bending, torsional and compressive loads. It is customary to evaluate bending/torsional strength at the diaphysis and axial compressive strength at the metaphysis; all three are relevant at the proximal femur. For the lumbar spine, vertebral body compressive strength assessment is most appropriate.52 Reports of section modulus (Z) are common, including non-density-weighted11,25,43 and density-weighted indices.27–29 Polar strength-strain index (SSI) is a volumetric density-weighted section modulus, reported as standard pQCT output for radial and tibial diaphyses.42 In contrast, non-density-weighted Z is approximated for the femoral neck and shaft using Beck‘s DXA hip structural analysis, incorporating observed cortical asymmetry for the femoral neck11,53 (Table 1, Figure 1b). Radial diaphysis Z may be derived using similar simplified geometric models (Figure 1b, Table 1).25,43,51 At metaphyseal sites, an index of structural strength in axial compression may be calculated (IBS or BSIc, Table 1).25,29,43,51 At present, generalization of findings is challenging due to inconsistent reporting of indices of skeletal strength..

Go to: Adaptations to Gymnastic Loading

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Distal Appendicular Sites (Figures 2a–d) As previously noted, gymnastic maneuvers apply loads to both upper extremities that rival lower extremity ground reaction forces during jumping.30–33 Because most other activities concentrate upper extremity loading on the dominant arm and do not involve total body mass impacts, the non-dominant forearm provides an excellent site for evaluating skeletal adaptation to gymnastic loading. As the distal radius bears the majority of axial compressive loads applied to the hand,54–55 it may serve as a particularly valuable indicator of gymnastic loading. In addition, the radius includes both cortical (diaphyseal) and trabecular (metaphyseal) regions of interest for bone tissue-specific assessment.25,41,43,48 In the lower extremity, the tibia provides a similar opportunity for bone tissue-specific evaluation of adaptation to high magnitude forces (ten times body weight).30–31 However, as tibial loading occurs with most sports and activities of daily life, gymnast vs. nongymnast contrasts may be less dramatic at this site than in the forearm. Finally, the peripheral nature of both the radius and tibia enables quantification of bone compartment densities and geometry using pQCT.41,43,48 Forearm Adaptations Observed in Childhood and Early Puberty (Tanner I, Tanner II)(Table 2a) At the radial metaphysis, significant enlargement of periosteal dimensions (10– 12% advantage)25–26 and significant elevation of total vBMD (11–20% advantage)25–26,27 and trabecular vBMD (21–27% advantage)26,27 have been reported in immature gymnasts relative to non-gymnasts (Figure 2a). These advantages in bone geometry and density appear to confer significant benefits in indices of skeletal strength (41–56% IBS advantage)(Figure 2a).25 One study reported a significant advantage in metaphyseal cortical vBMD;26 however, this result may be unreliable due to the probable influence of partial volume effects at this site.48 At the radial diaphysis (Figure 2b), studies have reported significant enlargement of periosteal dimensions (7–12%),25,27 and cortical CSA (8–23%)25,27 in Tanner I/II gymnasts relative to non-gymnasts. In contrast, cortical thickness results are mixed, with reports of both significant gymnast advantages (+10 to +16%, DXAderivation, digital radiogram)25,23 and no thickness differential (−2.7%, ns, pQCT)27. Gymnast advantages in diaphyseal bone geometry confer advantages in indices of skeletal strength (14% SSI, 24–38% Z).27,25 Associated advantages in muscle CSA (Ward et al.)27 and forearm lean mass (Nanyan et al.),23 suggest a link between muscular and skeletal parameters at the radial diaphysis.

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Laing et al. (2005) presented longitudinal evidence of geometric adaptation to prepubertal gymnastic loading at the forearm, but did not present the magnitude of gymnast advantages. They assessed skeletal changes semi-annually over two years, following initiation of training in gymnasts, compared to non-gymnasts.9 Groups were initially matched for age, but gymnasts were significantly shorter, lighter, leaner and had lower unadjusted BMC and bone area at all measured sites (baseline and Year 2).9 Nonetheless, compared to non-gymnasts, gymnasts exhibited larger two-year increases in forearm bone area. Furthermore, forearm area increased more in high- than low-level gymnasts (distinguished by frequency and difficulty of maneuvers), suggesting that bone geometry varies with loading dose (p<0.01). 9 It is possible that forearm area advantages were a function of increasing bone length (not reported), as area was not adjusted for this variable. In addition, bone growth velocity is not expected to decrease until after menarche, but decreasing velocity was artificially imposed upon all subject growth curves. The effect of this procedure on data interpretation is uncertain. Nonetheless, gymnastics initiation was associated with accelerated growth in forearm area, indicating skeletal adaptation to gymnastic loading that is not attributable to pre-existing characteristics.

Table 2a Gymnastic Loading Studies: Pre-puberty/Early Puberty Upper Extremity Adaptations Observed during Peri-menarcheal Growth (Table 2b) Two groups have evaluated DXA forearm area in gymnasts and non-gymnasts during puberty. Laing et al (2002, different cohort from Laing 2005) noted a 7.5% non-significant gymnast advantage in radius area; unfortunately, forearm area was not evaluated longitudinally in this 3-year study.6 In a different longitudinal analysis, our group compared forearm bone parameters in gymnasts, ex-gymnasts and non-gymnasts over 2–3 years of peri-menarcheal growth. Repeated measures ANOVA evaluated output from forearm DXA scans performed approximately one

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year pre-menarche and two years post-menarche, entering post-menarcheal gynecological age, height and lean mass as covariates.12–13 Extremely large effect sizes (Cohen‘s d) indicated meaningful advantages in forearm area for gymnasts over non-gymnasts at both time points (10–16%).12–13 Advantages were maintained by near parallel rates of peri-menarcheal growth for gymnasts and non-gymnasts, suggesting that geometric benefits were accrued during earlier growth and maintained during peri-menarcheal loading. Similarly, comparisons of exgymnasts (who quit gymnastics before menarche) vs. non-gymnasts suggest that geometric benefits of gymnastic loading were maintained for at least two years after training cessation (+7% to +10%). Furthermore, these results indicate that childhood gymnastic loading is associated with periosteal expansion at the forearm, with maintenance of this benefit beyond menarche.

Table 2b Gymnastic Loading Studies: Mixed maturity phases, Post-menarche and Adulthood Upper Extremity Adaptations Observed after Menarche (Table 2b) Several studies have evaluated post-menarcheal skeletal characteristics, comparing girls exposed to gymnastic loading during growth (gymnasts and/or ex-gymnasts) versus non-gymnasts.22,24,28–29 Gymnast populations differed slightly, as Liang evaluated current gymnasts (adult),24 our group evaluated a mixture of current and ex-gymnasts (late-adolescent),28–29 and Eser studied a broad age range of exgymnasts who ceased elite level gymnastics 3–18 years prior22. In the forearm, diaphyseal measurements were made using pQCT at the 66% site by Eser and the 33% site by our group; both protocols assessed the 4% metaphysis.22,28–29 Eser et al. also assessed diaphyseal properties at the 25% distal humerus; Eser‘s analyses were not adjusted for gynecological age or body size at any site, despite significant group differences in age at menarche and wide age variation.22 Our group used ANCOVA to adjust for gynecological age (years post-menarche) and height at both sites.28 Liang assessed distal ulna width and mid-ulna bending stiffness with

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Mechanical Response Tissue Analysis (MRTA), adjusting bending stiffness for body weight.24 As these studies were performed in post-menarcheal females, advantages may not be attributed to loading during a specific phase of development; loading benefits may have accumulated over multiple maturational phases.

At the 4% radial metaphysis (Figure 2a), ex-gymnasts and gymnasts exhibited large advantages in periosteal geometry22,28 and skeletal strength indices,28 with evidence of elevated trabecular vBMD22,28. Our work also demonstrated gymnast advantages in trabecular CSA (+20%, large effect size) and cortical CSA (+27%, large effect size), indicating global expansion of skeletal geometry.28 Neither study provided strong evidence for a total vBMD gymnast advantage,22,28 suggesting that geometric expansion may limit vBMD. Evidence for a trabecular vBMD advantage was strong in the younger cohort of active and ex-gymnasts (+18%, large effect size),28 whereas the older cohort of elite ex-gymnasts demonstrated only a strong trend (+9%, p=0.056)22. Comparison of these results may suggest greater long-term retention of geometric adaptations than vBMD advantages. On the whole, results from both cohorts suggest that gymnast metaphyses adapt via a combination of moderate global enlargement of bone geometry (periosteal, cortical and trabecular compartments) coupled with moderate elevation of trabecular density.

At forearm diaphyseal sites, gymnasts demonstrated large, significant advantages for periosteal geometry (~30%) and skeletal strength indices (36–58%) (Figure 2b).22,24,28 Of particular note, endocortical CSA was highly variable and, on average, more than 50% higher among gymnasts and ex-gymnasts versus nongymnasts.22,28 Cortical CSA advantages were larger and more pronounced in late adolescent current/ex-gymnasts (33% site)28 than in older ex-gymnasts (66% site)22. In contrast, gymnast advantages in cortical thickness22 and cortical vBMD22,28 have not been detected at the radial diaphysis. In fact, cortical vBMD was lower in gymnasts than non-gymnasts at the 66% radius (−2.6%, p<0.05).22 Overall, radial diaphyseal skeletal strength appears to be a function of geometric adaptation (coupled periosteal and endocortical compartment expansion).

Eser et al. also assessed the 25% distal humerus, where the pattern of diaphyseal adaptation differed from that observed at the radius. In contrast to the radius,22,28 humerus endocortical CSA was not larger in gymnasts vs. non-gymnasts (+3.9%, ns)22. In the absence of endocortical expansion, moderate periosteal enlargement (+20%, p<0.05) yielded significant advantages in humeral cortical thickness and CSA (+15%, +24%, respectively).22 As a result, in gymnasts, humeral advantages in theoretical skeletal strength (+38%, p<0.05) were more closely proportioned to

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BMC advantages (+24%, p<0.05). Differences in humeral cortical vBMD were not detected (−0.01%, ns).22

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Upper Extremity Muscle-Bone Relationship Strong relationships between upper extremity muscular parameters and skeletal indices have been reported in gymnasts and non-gymnasts of all age groups,22,23,27,29 indicating an influential muscle-bone unit. Thirty to sixty percent of variation in bone outcomes was explained by muscular parameters in two studies evaluating post-menarcheal ex/gymnasts and non-gymnasts.22,29 However, both reports also suggested that ―non-muscular‖ aspects of gymnastic loading may play an independent role in skeletal adaptation. In one study, gymnasts exhibited higher BMC than was expected from muscle CSA22; in the other study, after accounting for gynecological age, height and either muscle CSA or arm FFM, gymnastic exposure still explained 25–61% of the variation in bone outcomes.29 Further evidence of potential ―non-muscular‖ aspects of gymnastic loading is provided by Liang et al., who reported no correlation between ulnar bending strength and indices of muscular strength.24 In a site-specific example of the muscle-bone unit, Nanyan et al. reported cortical ring asymmetry at the distal radius.23 They hypothesized that the action of muscle attachments on the ulnar aspect of the radius may generate significant gymnast advantages in ulnar side cortical thickness, but not radial side thickness.23 Even in the absence of muscular loading, radial asymmetry may be stimulated by compressive loads applied at the hand which are transmitted along the ulnar aspect of the radius via the interosseous ligament55, suggesting a potential mode of nonmuscular adaptation at this site. Both types of stimuli may be influential in skeletal adaptation to gymnastic loading.

Upper Extremity Adaptations- Summary Upper extremity adaptations to gymnastic loading are site-specific. The radial diaphysis appears to adapt via expansion of the periosteal, cortical and endocortical (intramedullary) compartments, with no advantage in cortical vBMD.22,27,28 This geometric expansion produces large advantages in skeletal strength (~15–40%) which are underestimated by gross indices of bone mass (aBMD, BMC).24–25,29 At the radial diaphysis, distribution of the cortical ring over a wider area limits or even prevents cortical width advantages in both pre- and post-menarcheal gymnasts. In contrast, at the distal humerus diaphysis, the cortex is expanded primarily through periosteal apposition, with little endocortical expansion,

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increasing both cortical CSA and thickness. Endocortical CSA appears to be highly variable at all maturity levels, suggesting that strategies of endocortical expansion versus contraction may be genetically determined mechanisms for bone strength adaptation.

Although no published reports delineate skeletal changes across maturation, available studies at the radial diaphysis represent a range of maturity phases. Interstudy comparisons suggest maturity-specific adaptation at this site. Childhood adaptation yields diaphyseal advantages of approximately 10% for periosteal CSA and 20% for cortical CSA. During peri-menarcheal growth, continued gymnastic loading may accelerate endocortical resorption and periosteal expansion, as advantages in periosteal and endocortical dimensions appear greater in postmenarcheal gymnasts than in their pre-menarcheal counterparts (approximately 30% vs. 10%, periosteal; 60% vs. 10%, endocortical).12,13,22,24–25,27–28 In exgymnasts, upper extremity advantages in bone geometry and indices of skeletal strength appear to be maintained long-term, at least two years after activity cessation and into adulthood.12,13,22 Gymnast adaptations at the radial metaphysis are closely tied to gross indices of bone mass, as this site exhibits advantages in both skeletal geometry and density.

Periosteal and trabecular CSA are larger in post-menarcheal gymnasts, yielding greater geometric advantages than have been observed in childhood and early puberty (~20% vs. 5–10%) (Figure 2a). In contrast, post-menarcheal gymnast advantages in metaphyseal vBMD (total and trabecular) and indices of bone strength are not greater than Tanner I/II gymnast advantages. This phenomenon may be a consequence of geometric expansion. In the face of limited mineral resources, geometric expansion would occur at the expense of vBMD, limiting relative gains in axial compressive strength. Although calcium supplementation to augment mineral resources might be expected to yield further increases in vBMD and indices of skeletal strength, the results of Ward et al. suggest that calcium supplementation does not enhance bone accrual in pre- and early pubertal gymnasts; this has not been studied in later maturity phases.56 Tibial Adaptations Observed in Childhood (Tanner I, pre-puberty)(Table 2a) Ward‘s evaluation of pre-pubertal gymnastic adaptation included assessment of the tibia (Figure 2c,d). Gymnast advantages at this lower extremity site were less notable than radius advantages.27 At the tibial distal metaphysis and proximal diaphysis, there was no significant indication of loading-related periosteal expansion. However, total metaphyseal vBMD was significantly higher in

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gymnasts than non-gymnasts (+5.7%), with a trend toward higher metaphyseal trabecular vBMD (+4.5%, p=0.11)(Figure 2c).27 Strong trends were also exhibited toward increased diaphyseal cortical CSA, cortical thickness and SSI in gymnasts versus non-gymnasts (Figure 2d, p<0.15),27 apparently via reduced endocortical resorption or increased endocortical apposition. Female gymnasts exhibited no advantage in muscle CSA at the 66% tibia (−1.3%, p=0.73).27 It should be noted that non-gymnasts in this study were quite active, averaging over 6 hours per week of organized physical activity;27 less active non-gymnasts might have provided higher tibial loading contrast for detection of group differences.

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Tibial Adaptations Observed after Menarche (Table 2b) Tibial Metaphysis (Figure 2c) Two published studies evaluated the tibial metaphyses in adult gymnasts and exgymnasts.22,57 One study used hrMRI and DXA to evaluate the proximal metaphysis57 and the other used pQCT to evaluate the distal metaphysis22. Neither study detected a significant geometric advantage (projected area or CSA).

However, both identified gymnast advantages in trabecular vBMD (+7%, trabecular vBMD, distal; +16.1%, trabecular bone volume for compartment volume (BV/TV), proximal).22,57 At the proximal metaphysis, this architectural advantage appeared to be a function of higher trabecular number and lower trabecular separation (+7.8% and −13.7%, respectively, p<0.05), with some evidence of thicker trabeculae (+6.9%, NS).57 These studies suggest that adaptation to gymnastic loading at the tibial metaphyses occurs via enhanced trabecular structure rather than enlarged periosteal dimensions. In both studies, menarche occurred earlier in non-gymnasts, indicating lower physical maturity among gymnasts; statistical adjustment for physical maturity might have improved detection of gymnast advantages in bone geometry. Even so, reported gymnast advantages imply that mechanical loading trumps the negative influence of muted estrogen exposure upon trabecular structure. Ex-gymnasts appear to maintain significant long-term benefits in trabecular structure,22 but the observation of greater percent advantages in current gymnasts57 than in ex-gymnasts22 suggests some deterioration in trabecular tissue after loading cessation.

Tibial Diaphysis (Figure 2d) Tibial diaphyseal assessments were included in Eser‘s post-menarcheal pQCT study discussed above (Table 2b).22 Significant ex-gymnast tibial advantages ranged from +7% to +12%.22 The general pattern of tibial diaphyseal adaptation

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appears similar to that of the humerus; limited periosteal advantages with no significant advantage in cortical vBMD (−0.5%, ns) or endocortical CSA (+5%, ns) yield increased cortical thickness, cortical CSA and diaphyseal strength.22

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Liang et al. measured bending stiffness (EI) at the tibial mid-shaft in adult female gymnasts, swimmers and non-athletes using MRTA.24 The reported gymnast advantage for this unusual index of mid-tibial material and bending strength (+228%)24 markedly exceeds advantages observed at the tibia in other studies (different indices, +4% to +16%)22,27,57 and reported advantages at all other sites (+60% or less). It is likely that this disparity is a function of the unique nature of the index itself.

Tibial Adaptations-Summary On the whole, gymnast advantages are lower at the tibia than at the radius (<10% vs. 10–60%). High background loading of the lower extremities may reduce gymnast/non-gymnast loading differentials, limiting detection of tibial adaptations.

In childhood, loading appears to enhance tibial axial compressive strength via increased trabecular and total volumetric density, whereas significant advantages in periosteal dimensions have not been identified. Adult gymnasts and ex-gymnasts provide stronger evidence of tibial adaptation, with elevated indices of diaphyseal bending stiffness and strength, complemented by enhanced metaphyseal trabecular structure and density. In adult gymnasts, non-significant childhood patterns are amplified; cortical thickening is emphasized over periosteal and endocortical expansion, yielding significant advantages in cortical dimensions and indices of skeletal strength in proportion with BMC advantages. However, in contrast to childhood trends of endocortical contraction (−4%, ns), trends in adult exgymnasts suggest endocortical expansion during puberty (+4%, ns). Overall, continued high level loading from childhood through puberty may be necessary for development of significant advantages at the tibia.

Figure 2 Figure 2a–d: Percent advantages for gymnasts versus non-gymnasts are presented for comparable bone sites and outcomes, as follows: (a) Radial Metaphysis; (b)

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Radial/ulnar Diaphysis; (c) Tibial Metaphysis, (d) Tibial Diaphysis. Error bars indicate (more ...)

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Spine and Femur (Figures 3a–c, Tables 2a–b) The lumbar spine and femur serve major weight-bearing roles during daily life activities. Because the lumbar spine and proximal femur contribute strongly to rates of osteoporotic fracture and resultant morbidity and mortality, loading-related enhancement of these sites during childhood and adolescent growth may be particularly important. Compared to non-athletes, several groups of non-gymnast athletes have demonstrated increased densitometric and geometric parameters at these locations.14,58 To date, most reports have focused on aBMD or BMAD; evaluations of geometric adaptation at these sites are quite sparse.

Lumbar Spine Adaptations Observed in Childhood and Early Puberty (Tanner I, Tanner II) Bass et al. compared bone-age matched pre-pubertal gymnasts vs. non-gymnasts (Table 2a; Figure 3a).1 Gymnast advantages were demonstrated for spine aBMD, lumbar spine vertebral volumes and lumbar spine BMAD (p<0.05).1 Vertebral diameter was not specifically reported, but greater lumbar vertebral volume combined with shorter sitting height suggests expanded lumbar vertebral diameter in gymnasts. Over 12 months of follow-up, sitting height and vertebral volume increased less in gymnasts than non-gymnasts, but bone mass increased more, yielding a significant increase in vertebral BMAD in gymnasts, not non-gymnasts.1 As lumbar width was not reported at follow-up, geometric growth could not be assessed. Adjustment for body size differences may have yielded greater gymnast advantages, as gymnasts exhibited lower mean height, sitting height and fat mass (p<0.05).1 Lumbar spine advantages in pre-pubertal gymnasts are corroborated by two other studies (Figure 3a). Dyson et al. detected significant lumbar spine aBMD and BMAD advantages in female gymnasts.26 Ward et al. reported a non-significant elevation in lumbar spine projected area (+2.9% p=0.15) and significant advantages in BMC, aBMD and BMAD in pre-pubertal male and female gymnasts vs. non-gymnasts.27 Although further study is necessary to detail loading-related adaptations at the lumbar spine, these studies suggest a role for adaptation in both volumetric density and geometry,1,26,27 theoretically increasing vertebral resistance to axial compression.

Lumbar Spine Adaptations Observed during Puberty (Tanner I-V)

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Two groups evaluated lumbar spine adaptation to gymnastic activity during puberty.6,59–60 In a cross-sectional study, one group used DXA to compare gymnasts and non-athletes at different stages of physical maturity, reporting only qualitative differences.59 Significant gymnast advantages were observed for lumbar spine aBMD and BMC adjusted for area (statistical adjustment, distinct from aBMD), but not projected area.59 This group also performed one-year longitudinal aBMD analyses, adjusting for age, height, Tanner stage, baseline aBMD, and 1-yr height and weight growth rates; no significant differences were detected for aBMD accrual or growth in projected area.60 The second group evaluated bone area changes in adolescent gymnasts and non-gymnasts over a three-year period.6 Subjects were matched for age and body size, exhibiting similar pubertal status and maturation rates (mean skeletal age, Tanner stage). Bone area increased at parallel rates in gymnasts and non-gymnasts for the total body and lumbar spine, with no significant advantage in unadjusted lumbar spine bone area at ―baseline‖(Figure 3a).6 The limited evidence provided by these studies suggests elevated vBMD accrual but no enhancement of bone geometric growth at the lumbar spine during peri-pubertal gymnastic loading.

Femoral Adaptations Observed in Childhood and Early Puberty (Tanner I, Tanner II) There are only two studies evaluating gymnastic adaptation at the femur during these maturity phases. Neither study reports a gymnast advantage in pre-pubertal periosteal dimensions at the femur. At the femoral neck, Dyson et al. reported a significant gymnast advantage in femoral neck BMAD (Tanner I/II females)(Figure 3c), but did not report geometric indices.26 Bass et al. evaluated bone geometry at the mid-femur diaphysis (Figure 3b).1 Gymnasts exhibited lower mean endocortical diameter and higher mean bi-cortical width, yielding increased femoral shaft vBMD compared to non-gymnasts (p<0.05)(Figure 3b).1 Mid-shaft femoral periosteal diameters were not significantly different.1 As femoral shaft analyses were not adjusted for differences in height, weight or bone length, it is unclear whether gymnasts‘ periosteal and endosteal dimensions were low or high for body size. Bass concluded that decreased endosteal resorption or increased endocortical apposition produced cortical thickening in response to gymnastic loading.1 Leg aBMD and 1-year growth rate in leg aBMD were significantly higher in gymnasts than non-gymnasts, suggesting a loading response.1 Bone compartment dimensions were not compared at follow-up, so geometric and vBMD growth cannot be assessed.

Proximal Femur Adaptation Observed during Puberty (Tanner I-V)

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Two groups evaluated standard DXA parameters at the proximal femur in pubertal females.6,59–60 In their cross-sectional study, Lehtonen-Veromaa identified significant gymnast advantages for femoral neck aBMD and for femoral neck BMC adjusted for area, but not for area.59 In their longitudinal analysis, aBMD accrual at the femoral neck and greater trochanter was significantly higher for gymnasts than non-athletes over one year of growth.60 No significant differences were observed for growth in proximal femur projected area.60 Similarly, over three years, Laing et al. (2002) reported parallel rates of increase in bone area for gymnasts and non-gymnasts at the femoral neck and total hip.6 Furthermore, at these sites and the greater trochanter, gymnasts exhibited no significant advantages in unadjusted bone area at ―baseline‖ (Figure 3c).6 Results from these analyses suggest minimal geometric adaptation to continued gymnastic loading at the proximal femur during pubertal development.

Faulkner et al. applied DXA hip structural analysis to evaluate bone geometric and theoretical strength parameters at the femoral narrow neck and proximal shaft (2 cm distal to lesser trochanter).11 At the narrow neck (Figure 3c), gymnasts exhibited significantly lower sub-periosteal width and endosteal diameter than nongymnasts, but higher cortical CSA, BMC and Z (p<0.05) (Figure 3a).11 At the proximal femoral shaft (Figure 3b), gymnasts demonstrated significantly higher bone geometric and strength indices, except for endosteal diameter (Figure 3b).

Although the authors reported equal numbers of pre-pubertal girls in each activity group, non-gymnasts were overrepresented in advanced pubertal stages (Tanner pubic stages IV/V: non-gym=40% vs. gym=17%).11 Thus, between-group maturational variability may have confounded analyses, underestimating gymnasts‘ geometric and densitometric advantages; this effect may have been partially mitigated by adjustment for height and weight. On the whole, gymnasts‘ proximal femur cortical bone geometry and indices of skeletal strength were enhanced for their physical maturity and body size, highlighting the association between cortical thickening and mechanical loading.

Distal Femur Adaptations Observed in Adults (Post-menarcheal Exgymnasts)(Figure 3b) In their evaluation of adult ex-gymnasts at the 4% distal femoral metaphysis, Eser et al. reported non-significant trends toward ex-gymnast advantages in BMC (+7%, p=0.07), total vBMD (+4%, p=0.08) and trabecular vBMD (+5%, p=0.07), with little evidence of periosteal expansion in response to loading (total CSA, +2%, ns).

The absence of significant ex-gymnast advantages at the distal femur metaphysis

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may indicate loss of benefit after activity cessation or insufficient contrast between gymnastic loading and non-gymnast background loading.

At the 25% distal femoral diaphysis, geometric adaptation dominated, echoing radial diaphyseal patterns and contrasting with femoral metaphyseal patterns.

Despite a strong trend toward lower cortical vBMD (−1%, p<0.06) and no advantage in cortical thickness (−0.3%, ns), ex-gymnasts demonstrated significant advantages in total CSA (+10%) and endocortical CSA (+14%), yielding elevated diaphyseal bending strength (SSI, +14%, p<0.05). Compared to the radial shaft, distal femoral diaphysis cortical CSA advantages were muted (+6%, p<0.20) and geometric and strength advantages were more proportional to the BMC advantage (+11%, p<0.05). On the whole, endocortical and periosteal expansion appear to be the predominant modes of gymnastic adaptation at the distal femoral diaphysis.

Lumbar Spine and Femur Summary In summary, results are limited and disparate for lumbar spine and femur geometric adaptation. Lumbar spine loading appears to increase vertebral volumetric density in children and adolescent girls (+8 to +12%); limited evidence suggests that axial compressive strength may also be increased through vertebral body geometric expansion (2–12%). Proximal femur adaptation includes cortical thickening, with increases in BMAD (15–20%) and aBMD. These cortical thickness/CSA advantages (12–15%) appear to result from endocortical contraction, with little or no enlargement of proximal femur periosteal dimensions.

In contrast, distal femur diaphyseal adaptation may rely primarily upon periosteal expansion with low endocortical resorption to maximize advantages in skeletal bending strength (10–20%). Discrepancies in observed patterns of skeletal adaptation at the proximal femur in immature active gymnasts1,11 versus the distal femur in adult ex-gymnasts22 may indicate site-specific variation, maturity-specific variation or deterioration of benefits after gymnastic cessation.

At the femur and lumbar spine, significant gymnast advantages are fewer and of lower magnitude (absolute value=4% to 24%) than upper extremity advantages (absolute value=7% to 58%). This observation supports the view that upper extremity sites provide greater sensitivity to evaluate loading adaptation. Use of improved methodology (supine lateral lumbar spine DXA, DXA HSA, MRI, QCT) is necessary to delineate tissue-specific adaptations to loading of the vertebral bodies and femur. Additional longitudinal studies with well-matched non-gymnast ―controls‖ and statistical adjustment for body size will generate more definitive information regarding geometric adaptation to gymnastic loading during growth.

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Figure 3

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Figure 3a–c: Percent advantages for gymnasts versus non-gymnasts are presented for comparable bone sites and outcomes, as follows: (a) Lumbar spine; (b) Femoral diaphysis; (c) Femoral neck. Error bars indicate 95% Confidence Intervals for the (more ...)

Go to: Conclusion Skeletal adaptation to gymnastic loading during growth appears to be sex-, maturity-, site- and bone-tissue specific, with upper extremities providing the most sensitive regions of interest for skeletal evaluation. Furthermore, there is accumulating evidence of benefit persistence after activity cessation and into adulthood.

Detailed evaluations of the tibia and forearm support the concept that skeletal adaptations to gymnastic loading are bone tissue- and site-specific. Metaphyseal sites are comprised of a large proportion of cancellous bone and adapt predominantly by increasing bone volume per trabecular compartment volume (~10% greater vBMD), likely through increased trabecular number and size.

Gymnast advantages in periosteal dimensions are not significant at the proximal or distal tibial metaphyses. However, at the distal radial metaphysis, moderate geometric expansion (10–20%) contributes to increased skeletal resistance to bending, torsion and axial compression in gymnasts. Similarly, concomitant geometric expansion and metaphyseal vBMD elevation have been observed in racquet sport players and weight-lifters,61–63 although adaptations are generally more striking in gymnasts.

In contrast to metaphyseal sites, adaptation to gymnastic loading of the radial and tibial diaphyses is dominated by geometric enlargement. In gymnasts, expanded cortical, endocortical and periosteal dimensions (10–20%, 10–60%, 10–30%, respectively) yield greater indices of skeletal strength (20–60%) at these predominantly cortical sites. These gymnast advantages parallel those associated with other loading modalities, where enlarged cortical CSA improves bending and torsional strength,61–62,64–67 particularly when expansion occurs around a widened

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intramedullary cavity.65,67–69 In gymnasts, comparisons of different regions of interest within radial, humeral, tibial and femoral diaphyses suggest that the mode of diaphyseal adaptation (endocortical expansion vs. contraction) may be a function of skeletal site, varying from bone to bone and within a single bone. High variability in diaphyseal endocortical dimensions also suggests the potential for genetic influence. Finally, site-specificity in adaptive patterns for periosteal CSA, endocortical CSA, cortical CSA and cortical thickness may generate variable observations in diaphyseal total vBMD, highlighting the importance of reporting these geometric outcomes.

Limited evidence for lumbar spine adaptation to axial compressive loading includes potential expansion in vertebral width (2–12%) and observed increases and advantages in vBMD (~10%). Similarly, at the proximal femur (neck and shaft), gymnast advantages in both cortical bone geometry (12–15%) and total vBMD (15–20%) have been identified, theoretically improving resistance to bending (10–20%) and axial compression (not assessed). Gymnast advantages in proximal femoral cortical dimensions likely result from endocortical contraction, with limited evidence of femoral shaft periosteal expansion during puberty and no reports of femoral neck periosteal expansion at any maturity level. This enlargement of proximal femoral cortical dimensions corroborates loading adaptations observed in runners and high- and odd-impact athletes.64,58 In contrast, at the distal femoral shaft, simultaneous periosteal and endocortical compartment expansion, without enlargement of cortical CSA or thickness, appears to yield improvements in skeletal strength that persist after activity cessation.

Although awareness and understanding of geometric responses to skeletal loading have increased dramatically in recent years, much additional work remains. Further research should elucidate skeletal loading dose-response curves and the sex- and maturity-dependence of skeletal adaptation, detailing the micro- and macroarchitectural characteristics of anatomical sites with varied tissue compositions.

These research goals will be accomplished through application of modern techniques to evaluate bone geometric adaptation across childhood and adolescence, evaluating maintenance of benefits into adulthood.

Go to: Acknowledgments We are grateful to Dr. Frank Rauch for his invitation to present this review. We would like to thank Dr. Kate Ward, as well as Professors C.J. Blimkie and R.A.

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Faulkner for their prompt responses to our queries and for their intellectual generosity, assisting our efforts to interpret their work. Funding for this work was provided by the National Institute of Arthritis, Musculoskeletal and Skin Diseases.

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49. Rauch F, Neu C, Manz F, Schönau E. The development of metaphyseal corteximplications for distal radius fractures during growth. J Bone Miner Res. 2001;16:1547–55.[PubMed] 50. Rauch F, Schonau E. Peripheral quantitative computed tomography of the distal radius in young subjects- new reference data and interpretation of results. J Musculoskelet Neuronal Interact. 2005;5(2):119–126.[PubMed] 51. Sievänen H, Kannus P, Nieminen V, Heinonen A, Oja P, Vuori I. Estimation of various mechanical characteristics of human bones using dual energy x-ray absorptiometry: methodology and precision. Bone. 1996;18:17S–27S.[PubMed] 52. Carter DR, Bouxsein ML, Marcus R. New approaches to interpreting projected bone densitometry data. J Bone Miner Res. 1992;7(2):137–145.[PubMed] 53. Beck TJ. Program Copyright 2000. Johns Hopkins University, School of Medicine; Hip Structural Analysis (HSA) Program (BMD and Structural Geometry Methodology) 54. Palmer AK, Werner FW. Biomechanics of the distal radioulnar joint. Clin Orthop. 1984;187:26–35.[PubMed] 55. Pfaeffle HJ, Fischer KJ, Manson TT, Tomaino MM, Woo SLY, Herndon JH. Role of the forearm interosseous ligament: Is it more than just longitudinal load transfer? J Hand Surg [Am] 2000;25(4):683–68.

56. Ward KA, Roberts SA, Adams JE, Lanham-New S, Mughal MZ. Calcium supplementation and weight bearing physical activity- Do they have a combined effect on the bone density of prepubertal children? Bone. 2007;41:496– 504.[PubMed] 57. Modlesky CM, Majumdar S, Dudley GA. Trabecular bone microarchitecture in female collegiate gymnasts. Osteoporosis Int. 2008;19:1011–1018.

58. Nikander R, Sievanen H, Heinonen A, Kannus P. Femoral neck structure in adult female athletes subjected to different loading modalities. J Bone Miner Res. 2005;20(3):520–528.[PubMed] 59. Lehtonen-Veromaa M, Mottonen T, Svedstrom E, Hakola P, Heinonen OJ, Viikari J. Physical activity and bone mineral acquisition in peripubertal girls.

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62. Kontulainen S, Sievänen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: A peripheral quantitative computed tomography study between young and old starters and controls. J Bone Miner Res. 2003;18(2):352–9.[PubMed] 63. Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I. Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: A peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone. 2000;27(3):351–57.[PubMed] 64. Duncan CS, Blimkie CJR, Kemp A, Higgs W, Cowell CT, Woodhead H, Briody JN, Howman-Giles R. Mid-femur geometry and biomechanical properties in 15- to 18-yr old female athletes. Med Sci Sports Exerc. 2002;34(4):673– 81.[PubMed] 65. Ducher G, Courteix D, Même S, Magni C, Viala JF, Benhamou CL. Bone geometry in response to long-term tennis playing and its relationship with muscle volume: A quantitative magnetic resonance imaging study in tennis players. Bone.

2005;37(4):457–66.[PubMed] 66. Wang QJ, Suominen H, Nicholson PHF, Zou LC, Alen M, Koistinen A, Cheng S. Influence of physical activity and maturation status on bone mass and geometry in early pubertal girls. Scand J Med Sci Sports. 2005;15:100–106.[PubMed] 67. Forwood MR, Baxter-Jones AD, Beck TJ, Mirwald RL, Howard A, Bailey DA. Physical activity and strength of the femoral neck during the adolescent growth spurt: A longitudinal analysis. Bone. 2006;38:576–583.[PubMed] 68. Nikander R, Sievanen H, Uusi-Rasi K, Heinonen A, Kannus P. Loading modalities and bone structures at nonweight-bearing upper extremity and weightbearing lower extremity: A pQCT study of adult females. Bone. 2006;39:886– 94.[PubMed] 69. Liu L, Maruno R, Mashimo T, Sanka K, Higuchi T, Hayashi K, Shirasaki Y, Mukai N, Saitoh S, Tokuyama K. Effects of physical training on cortical bone at midtibia assessed by peripheral QCT. J Appl Physiol. 2003;95:219–224.[PubMed] MR imaging of overuse injuries in the skeletally immature gymnast: spectrum of soft-tissue and osseous lesions in the hand and wrist Jerry R. Dwek, 1 Fabiano Cardoso,2 and Christine B. Chung2 Author information ► Article notes ► Copyright and License information ► Go to: Abstract

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Background In the pediatric gymnast, stress-related physeal injuries have been well described with characteristic imaging findings. However, a spectrum of overuse injuries, some rarely reported in the literature, can be encountered in the gymnast‘s hand and wrist.

Objective

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To demonstrate the MR appearance of a spectrum of overuse injuries in the skeletally immature wrist and hand of pediatric gymnasts.

Materials and methods A total of 125 MR exams of the hand and wrist in skeletally immature children were performed at our institution during a 2-year period. Clinical histories were reviewed for gymnastics participation. MR studies of that subpopulation were reviewed and abnormalities tabulated.

Results Of the MR studies reviewed, ten gymnasts were identified, all girls age 12–16 years (mean age 14.2 years) who presented with wrist or hand pain. Three of these children had bilateral MR exams. Abnormalities included chronic physeal injuries in three children. Two girls exhibited focal lunate osteochondral defects.

Triangular fibrocartilage tears were present in three girls, one of whom had a scapholunate ligament tear. Two girls manifested metacarpal head flattening and necrosis.

Conclusion A variety of soft-tissue and osseous lesions can be encountered in the skeletally immature gymnast. Familiarity with these stress-related injuries is important for accurate diagnosis.

Keywords: Gymnastics, MRI, Overuse, Children Go to: Introduction

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Gymnastics has become a common and popular sport in the world today. In addition to those who partake in this sport for recreational purposes, there is a subpopulation of high-performance child athletes that strive for the ultimate goal of being an Olympian. During practice, skills or routines are learned and then repeated over and over in search of perfection. Many of these skills place extraordinary stress on the growing ends of the radius and ulna but also on the carpal bones and the bones of the hand and the many ligaments that stabilize these structures. At our institution we have encountered a variety of stress-related injuries in the skeletally immature gymnast, some of which have not been previously described in this patient population. The goal of this study was to document and review stress-related injuries sustained by young gymnasts in the wrist and hand.

Go to: Material and methods We retrospectively reviewed the reports and histories of all wrist and hand MRIs at our institution for the 2-year period from March 2006 to February 2008. The total number of exams reviewed was 125. From that group, all exams in which the history given by the referring physician or by the patient included gymnastics were retrieved into the study group.

All MR imaging was performed on a GE (General Electric Healthcare, Milwaukee, WI, USA) 1.5-T HDx platform. Children were placed prone with arm extended, and pronated (palm down) in the ―superman‖ position.

Standard wrist MR imaging included coronal T1 (TR 300–330 msec, TE 13–17 msec), T2 fat-saturated (TR 2,850–3,300 msec, TE 60 msec,), GRE (TE 15 msec TR 360–400 msec flip angle 15°), sagittal T1 and T2 fat-saturated, and axial T1 and T2 fat-saturated sequences. The slice thickness in all exams and sequences was 3 mm. When intravenous gadolinium (Magnevist Bayer Healthcare Pharmaceuticals, Wayne, NJ, USA) was administered imaging included postcontrast axial, sagittal and coronal T1 fat-saturated (TE 14–16 msec TR 400–530 msec) sequences.

MR arthrography was preceded by an injection of dilute gadopentate dimeglumine (Magnevist) (1 mm/L concentration) contrast agent via a dorsal approach into the radiocarpal joint under fluoroscopy. The clinical indication for MR arthrography was wrist pain with suspicion of ligamentous injury.

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MR arthrographic sequences included coronal T1 (TE 13–17 msec, TR 300–330 msec), T1 fat-saturated (TE 14–16 msec TR 400–530 msec), and T2 fat-saturated (TE 60 msec, TR 2,850–3,300 msec), sagittal T1 and T2 fat-saturated and axial T1, T1 fat-saturated and T2 fat-saturated sequences as well as a 3-D SPGR fatsaturated cartilage sequence (TR 20–21, TE 3–4.4 flip angle 35–45). Again the slice thickness was 3 mm in all sequences.

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MR imaging in the hand included both T1 (TR 300–330 msec, TE 13–17 msec) and T2 fat-saturated (TR 2,850–3,300 msec, TE 60 msec) sequences in all three planes. Slice thickness was again 3 mm throughout. If IV gadolinium contrast agent was given, post-contrast T1 fat-saturated (TE 14–16 msec TR 400–530 msec) imaging was performed in all three planes. Intravenous gadolinium contrast agent was administered in cases of osseous abnormality to help assess for osteonecrosis.

The images were reviewed by two attending musculoskeletal radiologists (JRD and CBC), each with more than 9 years of experience, for the presence of osseous, ligamentous and cartilaginous injuries. The physes of the distal ulna and radius were assessed for bony bridges as well as for foci of abnormal extension of physeal cartilage into the metaphyses. Agreement was by consensus. Other imaging was also reviewed if available. The ulnar variance of each individual was measured by one of the authors (JRD) using the average of three measurements from the conventional radiograph with the use of electronic calipers available on our PACS workstation (Amicas, Cambridge, MA, USA). The method used was that described

by Hafner et al. [1] for skeletally immature individuals using method ―A,‖ which is the more accurate method for comparative analysis. Ulnar variance according to this method is determined by measuring the distance from the most proximal point of the ulnar metaphysis to the most proximal point of the radial metaphysis. In the individual whose growth plates were fused, the method used was that described by Gelberman et al. [2, 3]. In this method, ulnar variance is determined by measuring the distance between a line drawn from the ulnar side of the distal articular surface of the distal radius and a line drawn along the carpal surface of the distal ulna. In either case, ulnar positivity is present when the ulnar articular surface is lying distal to the line marking the measured point of the distal radius. Ulnar negativity is the converse. The measurement is given as a positive number for ulnar-positive variance and negative numbers for ulnar-negative variance. The general demographics of sex and age were also recorded. Surgical records and clinical history were reviewed when available.

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At our institution, radiology retrospective reviews are deemed exempt from institutional review board approval.

Go to: Results

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A total of ten children were retrieved from the retrospective review. Three had bilateral examinations, resulting in the review of 13 MR imaging studies. All were girls age 12–16 years (mean age 14.2 years) at presentation. The lone 16-year-old girl also had an exam on the contralateral wrist at 18 years old (Table 1).

Table 1 Review of records of ten children Of the ten girls, 8/10 had MR exams of the wrist and 2/10 had MR exams of the hand. One girl who had an MR imaging study of the hand also had a CT examination using a 64-slice MDCT (GE LightSpeed VCT, Waukesha, WI, USA).

All patients had conventional radiographs. Of the eight children with wrist exams, three had bilateral MR exams and four had MR arthrograms.

Intravenous gadolinium contrast agent (Magnevist) was also administered to one patient with otherwise standard wrist imaging, and in that case the patient had MR exams done bilaterally 2 years apart both with IV contrast administration.

MR imaging of the hand was performed in two girls. Gadolinium contrast agent was given intravenously in one child.

Physeal injuries Three girls exhibited abnormally high T2 signal intensity with widening of the distal radial physis. There were no bridges. The appearance was typical of what has

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been termed gymnast wrist, with fraying, widening and irregularity of the physis (Fig. 1) [4].

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Fig. 1 Coronal T1-W MRI of patient 1, a 12-year-old girl with chronic physeal injury.

The distal radial physis is wide and irregular. Note low-signal intrusions into metaphysis typical of focal failure of ossification of physeal cartilage (arrow) Ligamentous injuries Three girls had TFCC tears, one of whom had TFCC tears bilaterally. All were the central communicating type. Additional findings included stripping of the ulnar collateral ligament from its distal ulnar insertion in two patients. One patient also had a scapholunate ligament tear, with contrast agent passing through the scapholunate joint from the radiocarpal to the midcarpal compartment (Fig. 2).

Fig. 2 Ligamentous injury. a Normal triangular appearance of the scapholunate ligament (arrow) in a 14-year-old girl. Note that no bright gadolinium contrast is present in the midcarpal row (arrowheads). b Coronal T1-W MRI of a 13-year-old girl (patient 2). (more ...)

Osseous injuries Two girls showed an ovoid area of low T1 signal that was mildly hyperintense on T1 in the lunate at the scapholunate articulation. In both girls the scapholunate

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ligament was intact. In one girl the lunate abnormality was present toward the dorsal half of the bone. This lesion measured 6 × 3 mm and 3 mm in depth. In the other case, the abnormality was at the central portion and measured 5 × 3 mm and 3.5 mm in depth. This second girl was surgically explored. The focal area of abnormality in the lunate was described as filled with soft white material. The overlying articular cartilage had a reticulated appearance. The scapholunate ligament was described as intact but abnormal. Significantly, there was no abnormal motion at the scapholunate joint, with passive ranging of the carpus.

Histological analysis showed a fibrocartilaginous matrix most consistent with chondromalacia. There were no necrotic elements to indicate Keinbock disease.

This girl was initially examined at 16 years old on her right wrist, and she returned 2 years later at 18 years old with an identical injury to the left wrist and identical MR appearance (Fig. 3).

Fig. 3 Patient 10. a Right wrist coronal GRE MRI of a 16-year-old girl. Focal bright signal in the lunate is consistent with an osteochondral defect proved by biopsy. b Same girl at age 18. Left wrist coronal GRE MRI. Focal bright signal in the lunate is identical (more ...)

Two children had abnormalities involving the metacarpal heads. In one child flattening of metacarpals two through five was noted, with irregularity of the articular surface. In one child flattening and focal defects of the articular surface of the fourth metacarpal were noted without involvement of the other metacarpals. In both children, bright T2 signal was noted at the articular surface in a subchondral location with clear flattening of the articular surface, and irregularity with focal defects of the articular surface was seen (Fig. 4). The child with changes limited to the fourth metacarpal head also had an MDCT exam, which portrayed the articular findings particularly well. The findings were typical of aseptic necrosis of the metacarpal head or Dieterich disease.

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Fig. 4

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Coronal T2-W MRI of a 14-year-old girl (patient 7). Flattening and bright signal of the second through fourth metacarpal heads consistent with osteonecrosis Measurements of ulnar variance showed a mean ulnar-negative variance measuring−0.18 mm (SD 1.28 mm, RANGE −2.0 mm to 2.8 mm, CI=−0.78). This includes both wrists of the slightly older individual who returned to our institution at 18 years of age after first presenting at 16 years old. The normative value taken from Hafner et al. [1] in this age group is −2.2 to −2.3 mm so that ulnar variance was significantly more positive (P = 0.05) than that of the general population.

Although the sample size was small, the ulnar variance was either neutral or positive in those patients 14 years or older and always positive in those 15 years or older.

Go to: Discussion Since high-profile athletes such as Nadia Comaneci and Olga Korbut showcased the sport of gymnastics on the worldwide stage, it has been growing in popularity.

It is a sport that requires many long hours of practice and repetition. A moment‘s consideration is sufficient to understand the enormous biomechanical stresses placed on the skeleton by this sport. The human body was not engineered to tumble end over end in a stunning combination of laybacks, twists and somersaults.

Inevitably, injuries occur, usually but not solely as a result of chronic repetitive micro- or macrotrauma [5, 6].

Chronic growth plate injuries in gymnasts have been described fairly extensively [4, 7–10]. Plain film findings include irregular widening of the physes as well irregularity and thickening of the zone of provisional calcification. On MR imaging, there is edema on the metaphyseal and epiphyseal sides of the physis.

Foci of cartilaginous ingrowth resulting from failure of ossification of physeal cartilage into the metaphyses attest to metaphyseal injury while bony bridging results from epiphyseal trauma [11, 12].

Gymnasts are known to have ulnar-positive variance, which almost certainly results from chronic injury to the growing distal radial physis [13–16]. Although the distal ulnar physis is sometimes abnormal, in general, the majority of stress changes and growth abnormalities are seen at the radius. Several theories have been advanced to explain this predilection. Although the actual cause might be

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multifactorial, the relative maturity of the radial physis and ulnar physis could be one contributor. When compared with the standards of the Gruelich and Pyle method of bone age measurement, the ulnar physis appears to lose its growth potential earlier than the distal radial physis. This has been in part confirmed by Ogden et al. [17], who found that in 2 out of 3 pathologic specimens the distal ulnar physis fused and lost its growth potential prior to the distal radius in children 13–14 years of age. Another important factor is the significantly greater crosssectional area of the distal radial physis as compared to that of the distal ulna. In the neutral position with neutral ulnar variance, 80% of an axial load is exerted by the radius and 20% by the ulna [18], such that far greater forces are exerted on the distal radial physis than on the distal ulnar physis. Ulnar negativity causes the load borne by the distal radius to rise to 96% [19]. Children normally tend to be ulnarnegative, which increases drastically the load on the distal radius. Furthermore, forearm supination causes a relative negative ulnar variance while ulnar positivity occurs during pronation [20]. Some exercises might be primarily performed with supination rather than pronation but no detailed biomechanical studies have been performed. The gymnastic predilection for ulnar-positive variance was reflected in our study, where the mean variance was only 0.18-mm negative. In contrast, most children 12–16 years of age have negative ulnar variance measuring −2.2 to −2.3 mm [1].

TFCC injuries are well described in gymnasts. Traumatic TFCC injuries are more common in those individuals who are ulnar-positive and indeed two of our three patients with TFCC injuries were ulnar-positive and the third was ulnar-neutral.

Because many gymnasts become ulnar-positive from chronic injury to the distal radial physis, the two injuries might be related.

Focal chondral injury to the lunate with a similar appearance to that of our two cases has been described by Earp et al. [21] in association with a scapholunate ligament tear. In our one surgically explored case the scapholunate ligament was abnormal but intact and no abnormal motion was demonstrated at the joint.

Because the articular cartilage over the area had a reticulated appearance and the ligament was described as abnormal, it is likely that this represents an osteochondral injury in association with a scapholunate ligament injury. Our second case of focal lunate chondromalacia had an identical appearance, with an intact scapholunate ligament by MR arthrographic imaging. However, this does not rule out a healed scapholunate ligament injury and resultant osteochondral injury.

Neither case had the typical appearance of Keinbock disease, which usually involves the entire lunate. Histological analysis of the one surgically proven case showed no necrotic elements consistent with Keinbock disease. In addition,

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Kienbock disease is more commonly associated with ulnar minus variance. One of our two patients with lunate changes was ulnar-neutral and the second was ulnarpositive. It is unclear whether this injury is related to ulnar-positive variance, because of the small sample size.

There were two children who had injuries to their metacarpal heads. This has not been described previously. During the gymnastic exercise the metacarpophalangeal joints are under great tension both in flexion and extension. Dieterich in 1932 described aseptic necrosis of the metacarpal head [22]. It can be idiopathic but has also been associated with trauma [23], systemic lupus erythematosus and steroid use [24]. Most commonly the third metacarpal head is involved. Wright et al. [25] have described the vascular anatomy and supply of the metacarpal heads. In 35% of people the vascular supply of the metacarpal heads depends on numerous small pericapsular arterioles. In the few cases of metacarpal head necrosis described in the literature, compression and low or absent flow possibly by a joint effusion have been postulated as possible causes but it would seem to be a tenuous association when considering the relative rarity of metacarpal head necrosis and the commonality of solely pericapsular vascular supply as is present in 35% of people.

In neither case did we observe abnormality of the stabilizing structures of the metacarpophalangeal joints including the fibrous joint capsule, collateral ligaments and overlying tendons. Although a discrete fracture line was not observed, an insufficiency fracture and subsequent osteonecrosis with flattening of the articular surface is a strong possibility.

It is tempting to consider the entire spectrum of the injuries we have described as a chronic impaction type of injury that is manifesting at various levels in the carpus and the hand, depending on the age of the patients and the type of exercise performed, affecting the kinetic chain of the hand and wrist at various locations.

Only physeal injuries manifested in the younger children, whereas the injury pattern shifted to osseous and ligamentous abnormalities in the older individuals.

To some extent this is to be expected. The physis is most vulnerable to injury during pubertal growth when the growth rate is maximal. Later, when growth plate closure is imminent the physis is stronger as it narrows and small bony bridges occur prior to complete fusion. Instead of the injuries manifesting at the growth plate level, the area of failure shifts to the ligamentous tissue of the carpus, especially but not limited to the TFCC. It is unclear why some children injured their TFCC while others injured their lunates and still others their metacarpal heads. The issue is complex and might be related to the different routines being performed by the different children and the

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specific osseous anatomy in each of the children and individual technique-related biomechanics. It is important to note that these injuries and specifically those in the metacarpal heads and in the lunate have not been previously described in gymnasts. A different emphasis or even method of training might affect the specific pattern of injuries produced. The radiologist must remain aware that sports injuries are dynamic, with multiple contributing factors including structural composition, technique-related biomechanics, and repetition, among other things.

Our study is limited by its retrospective nature and limited selection criteria. Only those individuals who gave a history of gymnastics or whose physicians gave such a history were included. There are likely to be other patients with a history of significant gymnastic exercise whose histories were incomplete.

In addition, certain conditions, especially chronic growth plate injuries, might be underrepresented. This diagnosis is usually evident by conventional radiography, and MR imaging is reserved for those with atypical or more severe pain.

Go to: Conclusion We have presented a set of injuries in gymnasts that span the gamut from growth plate injuries in the youngest children to articular injuries at various levels in individuals who, while still skeletally immature, have little growth potential remaining at the carpal level. Both the referring physician and the radiologist need to be aware of the range of injuries that can occur in the young gymnast. The term ―gymnast wrist,‖ usually associated with chronic physeal trauma, should probably be enlarged to include nonphyseal osseous, ligamentous and osteochondral injuries.

Go to: Acknowledgments Open Access This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Go to:

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References

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1. Hafner R, Poznanski AK, Donovan JM (1989) Ulnar variance in children— standard measurements for evaluation of ulnar shortening in juvenile rheumatoid arthritis, hereditary multiple exostosis and other bone or joint disorders in childhood. Skeletal Radiol 18:513–516. [PubMed] 2. Thienpont E, Mulier T, Rega F et al (2004) Radiographic analysis of anatomical risk factors for Kienbock‘s disease. Acta Orthop Belg 70:406–409. [PubMed] 3. Gelberman RH, Salamon PB, Jurist JM et al (1975) Ulnar variance in Kienbock‘s disease. J Bone Joint Surg Am 57:674–676. [PubMed] 4. Liebling MS, Berdon WE, Ruzal-Shapiro C et al (1995) Gymnast‘s wrist (pseudorickets growth plate abnormality) in adolescent athletes: findings on plain films and MR imaging. AJR 164:157–159. [PubMed] 5. Gabel GT (1998) Gymnastic wrist injuries. Clin Sports Med 17:611–621.

[PubMed] 6. Webb BG, Rettig LA (2008) Gymnastic wrist injuries. Curr Sports Med Rep 7:289–295. [PubMed] 7. Caine D, Roy S, Singer KM et al (1992) Stress changes of the distal radial growth plate. A radiographic survey and review of the literature. Am J Sports Med 20:290–298. [PubMed] 8. De Smet L, Claessens A, Fabry G (1993) Gymnast wrist. Acta Orthop Belg 59:377–380. [PubMed] 9. Ruggles DL, Peterson HA, Scott SG (1991) Radial growth plate injury in a female gymnast. Med Sci Sports Exerc 23:393–396. [PubMed] 10. Shih C, Chang CY, Penn IW et al (1995) Chronically stressed wrists in adolescent gymnasts: MR imaging appearance. Radiology 195:855–859. [PubMed] 11. Ecklund K, Jaramillo D (2002) Patterns of premature physeal arrest: MR imaging of 111 children. AJR 178:967–972. [PubMed] 12. Jaramillo D, Laor T, Zaleske DJ (1993) Indirect trauma to the growth plate: results of MR imaging after epiphyseal and metaphyseal injury in rabbits.

Radiology 187:171–178. [PubMed] 13. Chang CY, Shih C, Penn IW et al (1995) Wrist injuries in adolescent gymnasts of a Chinese opera school: radiographic survey. Radiology 195:861–864.

[PubMed] 14. De Smet L, Claessens A, Lefevre J et al (1994) Gymnast wrist: an epidemiologic survey of ulnar variance and stress changes of the radial physis in elite female gymnasts. Am J Sports Med 22:846–850. [PubMed] 15. DiFiori JP, Puffer JC, Mandelbaum BR et al (1997) Distal radial growth plate injury and positive ulnar variance in nonelite gymnasts. Am J Sports Med 25:763– 768. [PubMed]

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16. Mandelbaum BR, Bartolozzi AR, Davis CA et al (1989) Wrist pain syndrome in the gymnast. Pathogenetic, diagnostic, and therapeutic considerations. Am J Sports Med 17:305–317. [PubMed] 17. Ogden JA, Beall JK, Conlogue GJ et al (1981) Radiology of postnatal skeletal development. IV. Distal radius and ulna. Skeletal Radiol 6:255–266. [PubMed] 18. af Ekenstam FW, Palmer AK, Glisson RR (1984) The load on the radius and ulna in different positions of the wrist and forearm. A cadaver study. Acta Orthop Scand 55:363–365. [PubMed] 19. Palmer AK, Werner FW (1984) Biomechanics of the distal radioulnar joint.

Clin Orthop Relat Res 187:26–35. [PubMed] 20. Palmer AK, Glisson RR, Werner FW (1982) Ulnar variance determination. J Hand Surg [Am] 7:376–379 .

21. Earp BE, Waters PM, Wyzykowski RJ (2006) Arthroscopic treatment of partial scapholunate ligament tears in children with chronic wrist pain. J Bone Joint Surg Am 88:2448–2455. [PubMed] 22. Bjorkman A, Jorgsholm P, Burtscher IM (2005) Osteonecrosis of the metacarpal head in a patient with a prothrombin 20210A gene mutation. Scand J Plast Reconstr Surg Hand Surg 39:379–381 .

23. McElfresh EC, Dobyns JH (1983) Intra-articular metacarpal head fractures. J Hand Surg Am 8:383–393. [PubMed] 24. Weissman BN, Rappoport AS, Sosman JL et al (1978) Radiographic findings in the hands in patients with systemic lupus erythematosus. Radiology 126:313– 317. [PubMed] 25. Wright TC, Dell PC (1991) Avascular necrosis and vascular anatomy of the metacarpals. J Hand Surg [Am] 16:540–544 .

Influence of water immersion, water gymnastics and swimming on cardiac output in patients with heart failure Jean‐Paul Schmid, Markus Noveanu, Cyrill Morger, Raymond Gaillet, Mauro Capoferri, Matthias Anderegg, and Hugo Saner Author information ► Article notes ► Copyright and License information ► This article has been cited by other articles in PMC. Go to: Abstract Background Whole‐body water immersion leads to a significant shift of blood from the periphery to the intrathoracic circulation, followed by an increase in central

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venous pressure and heart volume. In patients with severely reduced left ventricular function, this hydrostatically induced volume shift might overstrain the cardiovascular adaptive mechanisms and lead to cardiac decompensation.

Aim To assess the haemodynamic response to water immersion, gymnastics and swimming in patients with chronic heart failure (CHF).

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Methods 10 patients with compensated CHF (62.9 (6.3) years, ejection fraction 31.5% (4.1%), peak oxygen consumption ( O2) 19.4 (2.8) ml/kg/min), 10 patients with coronary artery disease (CAD) but preserved left ventricular function (57.2 (5.6) years, ejection fraction 63.9% (5.5%), peak O2 28 (6.3) ml/kg/min), and 10 healthy controls (32.8 (7.2) years, peak O2 45.6 (6) ml/kg/min) were examined. Haemodynamic response to thermoneutral (32°C) water immersion and exercise was measured using a non‐invasive foreign gas rebreathing method during stepwise water immersion, water gymnastics and swimming.

Results Water immersion up to the chest increased cardiac index by 19% in controls, by 21% in patients with CAD and by 16% in patients with CHF. Although some patients with CHF showed a decrease of stroke volume during immersion, all subjects were able to increase cardiac index (by 87% in healthy subjects, by 77% in patients with CAD and by 53% in patients with CHF). O2 during swimming was 9.7 (3.3) ml/kg/min in patients with CHF, 12.4 (3.5) ml/kg/min in patients with CAD and 13.9 (4) ml/kg/min in controls.

Conclusions Patients with severely reduced left ventricular function but stable clinical conditions and a minimal peak O2 of at least 15 ml/kg/min during a symptom‐limited exercise stress test tolerate water immersion and swimming in thermoneutral water well. Although cardiac index and O2 are lower than in patients with CAD with preserved left ventricular function and

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controls, these patients are able to increase cardiac index adequately during water immersion and swimming.

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Exercise in thermoneutral water has a long tradition in rehabilitative training institutions and has been used for many years in patients with coronary artery disease (CAD). Exercises to improve mobility, strength and cardiovascular fitness can easily be performed in water.

Whole‐body head‐up immersion leads to a significant shift of blood into the intrathoracic circulation, followed by an increase in central venous pressure, heart volume and cardiac output.1,2,3 Because this hydrostatically induced volume shift might overstrain the cardiovascular adaptive mechanisms in patients with heart failure and lead to left ventricular decompensation, recent guidelines state that patients with diastolic and systolic dysfunction should refrain from swimming.4 On the other hand, exposure to thermoneutral water leads to a number of physiological responses, which may be beneficial in patients with heart failure. Both systemic and pulmonary vascular resistance have been shown to decrease during bathing in warm water in these patients,5 and an improvement in the ventilation/perfusion ratio of the lungs6 may increase oxygen consumption ( O2). Water immersion leads to a reduction of renin, angiotensin II and aldosterone activity whereas increased release of atrial natriuretic peptide elicits natriuresis.7,8 The aim of this study was to evaluate cardiovascular adaptations in patients with stable chronic heart failure (CHF) during stepwise water immersion, water gymnastics and swimming, and to compare the results with those in patients with coronary artery disease (CAD) with preserved left ventricular function and in healthy controls. We hypothesised that patients with stable CHF and a functional class A or B (peak O2 during a symptom‐limited cardiopulmonary exercise test >14 ml/kg/min), according to the Weber classification,9 are able to increase stroke volume and cardiac index during water immersion and to tolerate water gymnastics and swimming without symptoms of pulmonary congestion.

Go to: Methods

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Patients

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We examined 30 male subjects: 10 patients with stable CHF, 10 patients with CAD and preserved left ventricular function, and 10 healthy controls (table 11).). Patients with heart failure included eight patients with ischaemic heart disease and two patients with idiopathic dilated cardiomyopathy. All patients were taking β‐blockers, whereas the controls were taking no drugs. Patients had to be swimmers and in a stable clinical condition. They were informed about the study procedure and written informed consent was obtained from them. The study protocol was reviewed and accepted by the local ethical committee.

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Table 1 Characteristics of the study population Experimental setting The study was performed in the swimming pool of the physiotherapeutic facilities at the University Hospital of Bern, Bern, Switzerland. The water temperature was 32°C throughout the study.

Haemodynamic measurements were performed with an inert gas rebreathing method using an infrared photoacoustic gas analyser (Innocor, Innovision A/S, Odense, Denmark). The patient breathes a gas mixture containing two physiologically inert compounds in a closed rebreathing assembly, one being soluble in blood (N2O, 0.5%) and the other being insoluble in blood (SF6, 0.1%). When the blood‐soluble gas comes in contact with the blood in the lung capillaries, it is dissolved and washed out by the blood perfusing the lungs. In the absence of pulmonary shunts (defined as an arterial saturation >98%), the pulmonary blood flow is proportional to the rate of washout of the blood‐soluble compound, measured continuously by a gas analyser. The blood‐insoluble compound is used to determine the lung volume, which is also required in the equation used to calculate cardiac output from the measured washout curve of the blood‐soluble compound.10 Previous validations of the foreign gas

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rebreathing method showed that the method gives accurate measurements of cardiac output at both rest and exercise.10,11

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Rebreathing was performed over 15 s with a gas volume of 3 litres. Heart rate, blood pressure and oxygen saturation of haemoglobin were measured simultaneously, and stroke volume, cardiac index and systemic vascular resistance were calculated.

As β‐blocker treatment is recommended by current guidelines in patients with CHF and CAD, and to allow for an optimal comparability of the haemodynamic measures, we only included patients who were taking β‐ blocker treatment. The healthy subjects, however, were not treated.

Study protocol An initial measurement was taken at rest at the border of the pool with the patient standing outside the water. Thereafter, the patient walked into the water step by step on a staircase. Additional measurements were taken at immersion to pelvis and chest, followed by the ―jumping‐jack‖ exercise for 30 s and a 60 s swim along the edges of the pool. Haemodyamic measurements were taken three times at every stage and mean values were calculated.

Statistical analysis Data analysis was performed using SPSS V.12.0 for Windows software. All data are expressed as mean (SD). Mean comparisons were effectuated using non‐parametric (Wilcoxon and Mann–Whitney U) tests. For bivariate correlation analysis, Pearson's correlation coefficient was calculated. A value of p<0.05 was considered significant.

Go to: Results Heart rate During stepwise water immersion up to the pelvis and chest, heart rate decreased from 69 (11) to 64 (9) beats/min in patients with CHF, from 74 (10) to 66 (10) beats/min in patients with CAD with preserved ventricular function, and from 82 (10) to 74 (14) beats/min in controls (fig 11).). During

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swimming, heart rate increased to 93 (14) beats/min, 93 (16) beats/min and 97 (23) beats/min in patients with CHF, patients with CAD and controls, respectively. Compared with controls and patients with CAD, the decrease in heart rate during water immersion was proportionally lower in patients with CHF, whereas the rate response during water gymnastics and swimming paralleled the other two groups.

Figure 1 Haemodynamic adaptation to water immersion, water gymnastics and swimming in patients with stable chronic heart failure (CHF), patients with coronary artery disease (CAD) with preserved left ventricular systolic function and healthy controls (more ...)

Stroke volume Water immersion up to the chest led to an increase in stroke volume of 30% in normal subjects and of 41% in the patients with CAD (fig 11).). In patients with CHF, stroke volume increased by 17%. During swimming, stroke volume was increased further by 47% in controls, by 30% in patients with CAD and by 35% in patients with CHF. Changes in stroke volume showed a positive correlation with peak O2 achieved during a maximal cardiopulmonary exercise test (r = 0.57; p = 0.006; fig 22).

Figure 2 Relationship between peak oxygen uptake O2 during maximal cardiopulmonary exercise test and change ( ) in stroke volume between rest and swimming.

Blood pressure Systolic blood pressure decreased from 122 (11) to 110 (9) mm Hg during water immersion in controls, from 119 (17) to 117 (15) mm Hg in patients with CAD, and from 113 (15) to 110 (19) mm Hg in patients with CHF. Diastolic pressure decreased from 75 (7) to 60 (7) mm Hg, from 77 (8) to 64 (8) mm Hg, and from 72 (8) to 59 (8) mm Hg, respectively, in controls, in

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patients with CAD and in patients with CHF. During swimming, systolic blood pressure rose up to 130 (24), 143 (13) and 122 (10) mm Hg in patients with CHF, CAD and controls, respectively, whereas diastolic blood pressure revealed only minor changes (63 (11), 68 (4) and 56 (9) mm Hg, respectively (fig 11).

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Peripheral vascular resistance Peripheral resistance, which was highest in patients with CHF, decreased in all study groups during water immersion (by 21% in patients with CHF, by 30% in patients with CAD and by 28% in controls). During swimming, vascular resistance decreased further by 33%, 33% and 43%, respectively (fig 11).

Cardiac index Water immersion up to the chest increased cardiac index by 19% in controls, by 21% in patients with CAD and by 16% in patients with CHF (fig 33).). During exercise, cardiac index increased further by 87% in controls, by 77% in patients with CAD and by 53% in patients with CHF. Figure 44 shows the individual responses of the patients with heart failure. Although cardiac index decreased in two patients during water immersion up to the chest, all patients were able to increase cardiac output during swimming.

Figure 3 Adaptation of cardiac index and oxygen consumption to water immersion, water gymnastics and swimming in patients with stable chronic heart failure (CHF), in patients with coronary artery disease (CAD) with preserved left ventricular systolic (more ...)

Figure 4 Individual haemodynamic response to water immersion (A) and swimming (B) in patients with heart failure (n = 10). ***p<0.001.

Oxygen uptake

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O2 was unaffected by water immersion. Water gymnastics required a

O2 of 11.4 (2.5) ml/kg/min in controls. Patients with CAD and CHF achieved a O2 of 10.7 (3.1) and 9.2 (2.1) ml/kg/min, respectively. During swimming, O2 rose to 9.7 (3.3) ml/kg/min in patients with CHF, to 12.4 (3.5) ml/kg/min in patients with CAD, and to 13.9 (4) ml/kg/min in controls (fig 33).

Go to:

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Discussion During head‐out water immersion, intrathoracic blood volume increases.

The reason for this volume shift from the periphery to the central organs is an increase of venous return as a consequence of the effect of hydrostatic pressure on the capacitance vessels, supported by a diminution of gravity dependency of the lower body.

To compensate for decreased myocardial contractility and to maintain an adequate cardiac output in patients with heart failure, the left ventricular end‐diastolic volume increases according to the Frank–Starling mechanism. Furthermore, increased diastolic distensibility leads to increased end‐diastolic volume tolerance in order to avoid end‐diastolic pressure rise, which could lead to pulmonary oedema. Volume shifts, as they occur during water immersion, might potentially overstrain these compensatory mechanisms and as a consequence lead to a decrease in stroke volume, a further rise in the end‐diastolic pressure and the occurrence of pulmonary congestion.

In our study, the cardiac response to water immersion up to the chest was characterised by a decrease in heart rate, an increase in stroke volume, no change in systolic blood pressure but a slight decrease in diastolic blood pressure and a reduction in peripheral vascular resistance (fig 11).

The observed response is the result of the following reflex mechanisms, all interfering with each other: a raise in atrial pressure due to the increase in venous return would lead to an increase in heart rate to evacuate the higher circulating volume (Bainbridge reflex). On the other hand, the rise in right atrial pressure and the increase in the circulating volume also initiates the Frank–Starling mechanism, which increases stroke volume and systolic blood pressure. The rise in blood pressure on his part activates the arterial baroreceptor control system located in the wall of the internal carotid

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arteries, the carotid sinus and the aortic arch. This leads finally, through excitation of the vagal centre, to a decrease in heart rate and venous and arteriolar tone over‐ruling, therefore the Bainbridge reflex.

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The patients with heart failure were characterised by the lowest heart rate, stroke volume and blood pressure but the highest peripheral vascular resistance of the three groups. The picture of the haemodynamic response, nevertheless, was similar in all three groups, which means that also in the population with heart failure, the reflex mechanisms were still intact.

Despite their severely reduced left ventricular function with a peak O2 between 15.4 and 24.1 ml/kg/min, they tolerated water immersion, gymnastics and swimming clinically well. Although stroke volume decreased in 4/10 patients and cardiac index decreased in 2/10 patients during water immersion, all patients were able to increase cardiac index during exercise (fig 44).

After a 60 s swim in a pool at 32°C, we found a mean O2 of 9.7 ml/kg/min in patients with heart failure, 12.4 ml/kg/min in patients with CAD with preserved left ventricular function and 13.9 ml/kg/min in controls (fig 33).).

The differences in O2 between controls and patients with cardiac problems, for the same physical activity, might result from a slightly different swimming speed and technique or, more likely, from differences in the Δ O2/Δwatt relationship during exercise (CHF, 8.1 (1.5); CAD, 9.2 (0.4); healthy, 10.0 (0.6); table 11),), reflecting a reduced central haemodynamic response to exercise in patients with impaired left ventricular ejection fraction and/or condition after myocardial infarction.

Left ventricular function at rest is a poor predictor of exercise capacity. 12,13 When it comes to recommendations for water sports in patients with heart failure, parameters of exercise capacity rather than echocardiographic measures seem therefore to be of particular importance. Water aerobics, water callisthenics and swimming correspond to a metabolic equivalent (MET) intensity level of 4 or a O2 of 14 ml/kg/min (1 MET = 3.5 ml/kg/min).14 The oxygen uptake at the anaerobic threshold in our study was 13.5 (3.2), 19.6 (6.2) and 26.4 (6.7) ml/kg/min for the patients with CHF, CAD and controls, respectively. This shows that swimming in the tested conditions (with a mean O2 of 9.7 (3.3), 12.4 (3.5) and 13.9 (4.0) ml/kg/min in the patients with CHF, CAD and controls, respectively) corresponds to an intensity level below the anaerobic threshold, even in patients with heart failure.

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As O2 is proportional to stroke volume, peak O2 can be used to appreciate the behaviour of the stroke volume during water immersion and swimming (fig 44).). Thus, in a stable clinical condition, a minimal peak O2 of at least 15 ml/kg/min and an anaerobic threshold >10 ml/kg/min characterises patients who can participate in water sports in the described conditions without the risk of cardiac decompensation. In patients with a peak O2 of <15 ml/kg/min or a Δ O2/Δwatt relationship clearly <8, however, caution has to be raised.

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To what extent parameters of cardiopulmonary exercise obtained on land can be compared with exercise in water has been investigated in various studies.2,15,16 In controls, the central shift of blood volume with head‐out water immersion results in a higher stroke volume at rest and during graded intensities of exercise, compared with values on land in the same posture and at the same metabolic rate.15 Despite an increased stroke volume in water, there is no proportional decrease in heart rate, at least at submaximal exercise levels, and therefore cardiac output is higher in water.

Similarly, mean right atrial and pulmonary arterial pressures were found to remain increased, indicating that preload remains increased during graded exercise up to maximal effort in water.2 In patients with cardiac problems, Hanna et al16 compared the effect of increased preload during head‐out water immersion on exercise response in men with healed myocardial infarction without signs of congestive heart failure and with an exercise capacity of at least 5 MET. At rest, cardiac output and stroke volume increased during water immersion, whereas heart rate did not change. During exercise, contrary to the studies conducted on healthy individuals,3,15 these patients did not show a shift of the cardiac output– O2 curve to the left, which means that cardiac output was not increased in water compared with land‐based exercise. This difference has been explained by a lack of further increase of the stroke volume from rest to exercise in the patient group. This might have been the consequence of a more intense adaptation using the Frank–Starling mechanism to maintain cardiac output during land‐based exercise in patients after myocardial infarction and a rapid exhaustion of this compensatory mechanism in water.

Furthermore, controls and patients after myocardial infarction showed a different heart rate response to exercise. In healthy people, heart rate response to exercise on land and in water are similar up to a work load of 40% of peak O2, but becomes lower at higher work loads in water. By contrast, subjects with a healed myocardial infarction had the same

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average heart rate in water and at land at all work loads examined up to 75% of peak O2. It can be concluded that in controls, the haemodynamic response to exercise in water is mainly determined by mechanisms including preload and stroke volume, whereas in patients with a reduced ejection fraction, cardiac output is regulated predominantly by changes in heart rate.

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In practice, two important points can be deduced from this fact. (1) Chronotropic response during an exercise stress test is a key parameter in the evaluation of water immersion tolerance in patients with heart failure. In our cohort, mean heart rate increased by 24 beats/min. By generalising these data, one can state that an increase in heart rate during submaximal exercise (eg, up to the anaerobic threshold) of this dimension would be a prerequisite for safe water immersion. (2) The data from Sheldahl et al15 and Christie et al2 show that healthy subjects have a similar heart rate response to exercise on land and in water up to 60% of peak O2 but a somewhat lower heart rate in water at higher work loads with a difference of approximately 10 beats/min. In patients after a myocardial infarction no difference in heart rate response to exercise on land and at all work loads examined in water (up to 75% of peak O2) was found.16 Therefore, there is no need for adaptation of the training heart rate for exercise on land or in water at intensities <60% of peak O2, especially in patients with reduced left ventricular function.

Distention of the peripheral vessels by thermoneutral water results in several salutary effects, which may be particularly beneficial for patients with heart failure: systemic vascular resistance decreases, whereas arginine, vasopressin, renin and norepinephrine are suppressed.17 Activation of cardiac mechanoreceptors leads to reflex adjustments of water and electrolyte excretions from the kidney,18 a mechanism that is preserved in patients with heart failure. Gabrielsen et al8 also showed that intravascular and central blood volume expansion in compensated heart failure suppresses the activity of the renin–angiotensin–aldosterone system, increases the release of atrial natriuretic peptide and elicits a natriuresis, which is enhanced when angiotensin II and aldosterone concentrations are suppressed by ACE inhibitor treatment. It can be concluded that water immersion elicits a number of physiological reactions that are similar to those achieved by modern pharmacological treatment.

While the impact on the renin–angiotensin–aldosterone system is of rather short duration, patients with difficulties in regulating their fluid status could

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particularly profit from the enhancement of natriuresis and therefore be ideal candidates for regular treatment in water.

Recently, the effect of 8 weeks of hydrotherapy in 25 elderly (72 (6) years), stable patients with CHF has been reported.19 These patients with a New York Heart Association (NYHA) functional class II to III and with an exercise capacity that was markedly lower than in our patient group ( O2 14.3 (2.7) vs 18.8 ml/kg/min) were randomised either to 8 weeks of hydrotherapy with three weekly sessions of 45 min (n = 15) or to a control group (n = 10). Hydrotherapy yielded improvements in exercise capacity and was well tolerated without any adverse events, suggesting that such a treatment can be safely offered to patients with CHF. These results are now supported by our haemodynamic studies and should therefore stimulate a paradigm shift in the recommendations of water gymnastics or swimming in thermoneutral water in patients with stable CHF and an NYHA functional class I to II. Study limitations The study has been effectuated in a controlled indoor setting, and in thermoneutral water. Therefore the results cannot be translated into activities in different environmental conditions. For example, for swimming at lower temperatures, in rivers, lakes or the sea, a higher exercise capacity would be required. Such activity has been shown to correspond to an intensity level of 6 METs or a O2 of 21 ml/kg/min.14 We did not study patients with CHF with severely impaired exercise capacity and a O2 capacity <14 ml/kg/min, which is the reason why we cannot draw any conclusion about patients in NYHA class III or IV. In addition, the fact that two of our patients showed a decrease in cardiac output during water immersion (although during exercise, cardiac output increased) should remind us to advise such patients with appropriate caution.

The absolute values of cardiac index measured at rest in this study seem to be rather low. However, it has to be kept in mind that these measures have been effectuated in a standing position, which could account for some differences of cardiac index values known from the literature, in general measured in supine position. Whereas validation studies have proved reliable compared with invasive techniques to determine cardiac output,10,11

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some limitations have to be mentioned. Uneven distribution between ventilation, lung tissue volume, alveolar volume and pulmonary blood flow, as they are observed in more severe forms of lung disease, may cause errors.20 Thus the presence of pulmonary disease might present one obstacle to the use of the rebreathing method.

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Conclusion Stable clinical conditions and a minimal peak O2 of at least 15 ml/kg/min with an anaerobic threshold >10 ml/kg/min during a symptom‐limited exercise stress test characterise patients with severely reduced ejection fraction who can safely participate in water sports in thermoneutral water.

Although cardiac index and O2 are lower in these patients compared with patients with CAD and preserved left ventricular function and controls, such patients are able to adequately increase cardiac index during water gymnastics and swimming in thermoneutral water.

In general practice, the ability of a patient to exercise safely on a cycle ergometer with a workload of 70 W (corresponding to 4 METs) or 110 W (corresponding to 6 METs) is a good indicator that water gymnastics and swimming in thermoneutral water are safe even in the presence of stable CHF. However, an inadequate chronotropic response to exercise might denote patients with impaired tolerance to water sports, given the fact that in patients with a reduced ejection fraction, cardiac output during water immersion and swimming is regulated predominantly by the heart rate.

Go to: Abbreviations CAD - coronary artery disease CHF - chronic heart failure MET - metabolic equivalent NYHA - New York Heart Association O2 - oxygen consumption

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Go to: Footnotes Competing interests: None declared.

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References

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1. Arborelius M, Jr, Ballidin U I, Lilja B. et al Hemodynamic changes in man during immersion with the head above water. Aerosp Med 1972. 43592– 598.598. [PubMed] 2. Christie J L, Sheldahl L M, Tristani F E. et al Cardiovascular regulation during head‐out water immersion exercise. J Appl Physiol 1990. 69657– 664.664. [PubMed] 3. Risch W D, Koubenec H J, Beckmann U. et al The effect of graded immersion on heart volume, central venous pressure, pulmonary blood distribution, and heart rate in man. Pflugers Arch 1978. 374115–118.118.

[PubMed] 4. Giauzzi P, Tavazzi L, Meyer K. et al Recommendations for exercise training in chronic heart failure patients. Eur Heart J 2001. 22125–135.135.

[PubMed] 5. Tei C, Horikiri Y, Park J C. et al Acute hemodynamic improvement by thermal vasodilation in congestive heart failure. Circulation 1995. 912582– 2590.2590. [PubMed] 6. Arborelius M, Jr, Balldin U I, Lila B. et al Regional lung function in man during immersion with the head above water. Aerosp Med 1972. 43701– 707.707. [PubMed] 7. Gauer O H. Recent advances in the physiology of whole body immersion. Acta Astronaut 1975. 231–39.39. [PubMed] 8. Gabrielsen A, Bie P, Holstein‐Rathlou N H. et al Neuroendocrine and renal effects of intravascular volume expansion in compensated heart failure. Am J Physiol Regul Integr Comp Physiol 2001. 281R459– R467.R467. [PubMed] 9. Weber K T, Janicki J S. Cardiopulmonary exercise testing for evaluation of chronic cardiac failure. Am J Cardiol 1985. 5522A–31A.31A. 10. Gabrielsen A, Videbaek R, Schou M. et al Non‐invasive measurement of cardiac output in heart failure patients using a new foreign gas rebreathing technique. Clin Sci (Lond) 2002. 102247–252.252. [PubMed]

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11. Agostoni P, Cattadori G, Apostolo A. et al Noninvasive measurement of cardiac output during exercise by inert gas rebreathing technique: a new tool for heart failure evaluation. J Am Coll Cardiol 2005. 461779– 1781.1781. [PubMed] 12. Franciosa J A, Ziesche S, Wilen M. Functional capacity of patients with chronic left ventricular failure. Relationship of bicycle exercise performance to clinical and hemodynamic characterization. Am J Med 1979. 67460– 466.466. [PubMed] 13. Cohen‐Solal A, Logeart D, Guiti C. et al Cardiac and peripheral responses to exercise in patients with chronic heart failure. Eur Heart J 1999. 20931–945.945. [PubMed] 14. Ainsworth B E, Haskell W L, Whitt M C. et al Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 2000. 32(Suppl)S498–S504.S504. [PubMed] 15. Sheldahl L M, Tristani F E, Clifford P S. et al Effect of head‐out water immersion on cardiorespiratory response to dynamic exercise. J Am Coll Cardiol 1987. 101254–1258.1258. [PubMed] 16. Hanna R D, Sheldahl L M, Tristani F E. Effect of enhanced preload with head‐out water immersion on exercise response in men with healed myocardial infarction. Am J Cardiol 1993. 711041–1044.1044. [PubMed] 17. Gabrielsen A, Sorensen V B, Pump B. et al Cardiovascular and neuroendocrine responses to water immersion in compensated heart failure. Am J Physiol Heart Circ Physiol 2000. 279H1931–H1940.H1940.

[PubMed] 18. Epstein M. Renal effects of head‐out water immersion in humans: a 15‐ year update. Physiol Rev 1992. 72563–621.621. [PubMed] 19. Cider A, Schaufelberger M, Sunnerhagen K S. et al Hydrotherapy—a new approach to improve function in the older patient with chronic heart failure. Eur J Heart Fail 2003. 5527–535.535. [PubMed] 20. Petrini M F, Peterson B T, Hyde R W. Lung tissue volume and blood flow by rebreathing theory. J Appl Physiol 1978. 44795–802.802. [PubMed Bilateral Pulmonary Emboli in a Collegiate Gymnast: A Case Report Leamor Kahanov, EdD, ATC and Tarah Daly, MS Author information ► Copyright and License information ► Go to: Abstract

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Objective: To characterize the diagnosis of pulmonary embolism in collegiate student-athletes and to raise awareness among sports medicine providers of the possibility of this potentially fatal disease in the student-athlete population.

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Background: An 18-year-old, previously healthy National Collegiate Athletic Association Division I female gymnast complained of intense pain, bilaterally, deep in her chest. The athlete was referred to her team physician, who identified normal vital signs but referred her to the emergency room because of significant pain. The student-athlete was diagnosed with bilateral pulmonary emboli in the emergency room.

Differential Diagnosis: Pneumonia, renal calculi, upper urinary tract infection, intercostal muscle strain or rib fracture, pancreatitis, gall bladder disease, gastritis, ulceration, esophagitis, infection, tumor, pulmonary embolism.

Treatment: The student-athlete was immediately placed on anticoagulants for 6 months.

During that time, she was unable to participate in gymnastics and was limited to light conditioning.

Uniqueness: Documented cases of female student-athletes developing a pulmonary embolism are lacking in the literature. Two cases of pulmonary embolism in male high school student-athletes have been documented, in addition to many cases in elderly and sedentary populations.

Conclusions: All health care providers, including sports medicine professionals, should be aware that this condition may be present among student-athletes. During the initial evaluation, prescreening should include questions about any previous or family history of pulmonary embolism or other blood clots. Athletes who answer

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positively to these questions may have a higher likelihood of pulmonary embolism and should be referred for testing.

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Keywords: cardiovascular diseases, vascular diseases Pulmonary embolism (PE) is a leading cause of unexpected death in the United States.1 Pulmonary embolism is estimated to cause 50 000 to 200 000 deaths every year1; however, only 2 cases of PE in the young athletic population have been documented. We present this case of PE in a collegiate female gymnast to inform sports medicine health care providers about this uncommon and life-threatening condition. This case is unique in that it is the only published record of a female athlete who has presented with a PE. Go to: PERSONAL DATA AND CHIEF COMPLAINT An 18-year-old (freshman) previously healthy National Collegiate Athletic Association Division 1 gymnast with no previous history or family history of pulmonary or cardiac conditions presented with upper right and upper left abdominal quadrant pain in the middle of the fall season. The athlete was evaluated during practice and was, therefore, warm and sweaty because of activity. She was visibly distressed and crying, indicating her frustration with a sharp pain in her chest and upper abdomen that was inhibiting her participation. The pain did not radiate or decrease with cessation of activity or change in position (standing, sitting, or lying). Her breathing was shallow because of pain and increased while lying in a prone or supine position. The athlete's only reported medication was an oral contraceptive (Yaz; Bayer HealthCare Pharmaceuticals, Wayne, NJ). The athlete had taken Yaz for irregular menstruation for the 3 months before her symptoms began. Questioning about her sexual activity revealed that pregnancy was not likely. Her pain began the night before her evaluation and was located in the upper right quadrant. At the time of the athletic trainer's evaluation, the team physician's on-campus office hours were ending. Because of the athlete's distress and pain symptoms, the athletic trainer did not want to wait until the next morning for a physician consult. The athlete was, therefore, immediately referred to the team physician.

Go to: PHYSICAL EXAMINATION AND MEDICAL HISTORY

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The team physician evaluated the athlete promptly (within 10 minutes). Her blood pressure was on the low end of normal limits at 110/64, similar to the measurement on her preparticipation physical examination. Additional vital signs were also similar to those on the preparticipation physical examination, including a heart rate of 80 beats/min, respiratory rate of 28 breaths/min, and oral temperature of 36.6°C (97.88°F). Oxygen saturation by pulse oximetry was 99%, slightly lower than normal.

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Upon physical examination, tenderness of the upper right and left abdominal quadrants was noted, in addition to rib cage tenderness with oblique and anterior compression. No organomegaly was identified. A cardiac examination indicated no irregular heart sounds and normal heart rate and rhythm. In addition, auscultation of the lungs was normal. The athlete's legs were palpated and a calf squeeze produced no findings of pain or knots. Based on the athlete's significant pain level and inconclusive evaluation, she was referred to the emergency room by the physician for additional evaluation. The team physician called ahead to apprise the emergency room staff of the referral and evaluation findings and to order blood laboratory tests and chest radiographs. Abdominal radiographs and urinalysis were not requested at that time.

Go to: EMERGENCY ROOM EVALUATION AND LABORATORY STUDIES The athlete was immediately transported to the emergency room by the athletic trainer in a golf cart, arriving within minutes. Emergency room vital signs evaluated during triage were unchanged from the physician's evaluation. No additional physical examination was conducted. An electrocardiogram indicated Twave inversion in leads V1 and V2, which characterizes right ventricular outflow obstruction or volume or pressure overload and can reflect pulmonary emboli.

Repeat electrocardiogram indicated normal rhythm, which may have accounted for the normal sinus rhythm upon auscultation. A chest radiograph suggested no abnormalities. A computed tomography angiogram (CTA) indicated bilateral basilar, segmental, and subsegmental filling defects consistent with PE (Figures 1 and and2).2). Wedge-shaped infarcts in the right lower lobe and left lower lobe were also identified, demonstrating that the clots were, in fact, obstructing blood flow (Figures 3 and and44).

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Figure 1

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Computed tomography angiogram demonstrating segmental and subsegmental filling defects.

Figure 2 Computed tomography angiogram demonstrating filling defect.

Figure 3 Computed tomography angiogram demonstrating left lower lobe infarction.

Figure 4 Computed tomography angiogram demonstrating left lower lobe blood clot.

Blood tests were conducted at this time, indicating an extremely elevated D-dimer concentration of 2566 ng/mL (normal is less than 451 ng/mL). An elevated Ddimer concentration is present when blood clot dissolution occurs. The athlete had a normal international normalized ratio (INR) prothrombin time and partial prothromboplastin time, and the hypercoagulability evaluation, including homocysteine, antithrombin III, anticardiolipin antibody, prothrombin 20210A, factor V Leiden, and lupus anticoagulant levels, was within normal limits. The D-

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dimer test was the key to determining that a blood clot was present because all other tests were noted as normal. A complete blood count, urinalysis, and chemistry panel were unremarkable.

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DIFFERENTIAL DIAGNOSIS

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Possible alternative diagnoses based on symptoms included pneumonia, renal calculi (kidney stones), upper urinary tract infection, intercostal muscle strain or rib fracture, and numerous abdominal conditions, such as pancreatitis, gall bladder disease, gastritis, ulceration, esophagitis, infection, and tumor. After examination, the physician thought that the athlete's cardiac and pulmonary symptoms could be the result of pneumonia; however, because of the amount of pain the athlete was experiencing and her inability to attain a comfortable position, as well as her upper abdominal pain and pain upon palpation, the physician suggested kidney stones might be responsible.

The case history, physical examination, and laboratory results failed to substantiate a diagnosis of either pneumonia or kidney stones. Cardiovascular signs that can occur with PE include tachycardia, hypotension, palpitations, cyanosis, calculated shock index (pulse divided by systolic blood pressure) greater than 0.8, new onset of atrial fibrillation, cardiac murmur, and chest pain.1–,6 This athlete presented with very mild cardiac symptoms except that 1 of 2 electrocardiograms indicated right ventricular flow problems. Pulmonary symptoms of PE can include dyspnea, tachypnea, cough (may be nonproductive), hemoptysis, coarse breath sounds (rhonchi, wheezing, rales), and pleural rub.1–,6 Neurologic symptoms can include syncope; decreased level of consciousness or confusion, with or without seizures; confusion (decrease in orientation); and seizures.1–,6 Psychological symptoms associated with PE are apprehension and anxiety.1–,6 Integumentary symptoms that can occur with PE are diaphoresis and cyanosis,1–,6 and musculoskeletal symptoms consist of leg cramps and edema. Gastrointestinal symptoms include nausea and vomiting, which were absent in the athlete.1–,6 Other possible symptoms, such as fever and chills, were absent in the athlete1–,6 (Table 1). Other than pain, pain upon palpation, and anxiety, the athlete's symptoms were unremarkable. Her blood tests did not indicate any significant inherited markers (ie, factor V Leiden, antithrombin mutations, prothrombin mutations). The key to diagnosis in this athlete was an elevated D-dimer concentration in conjunction with an abnormal CTA scan demonstrating the presence of blood clots, which disrupted blood flow and caused pain.

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Table 1 Prodromal Signs and Symptoms of Pulmonary Emboli by Body System1–,6 Go to: TREATMENT COURSE To quickly reabsorb the clots that had formed, the athlete was administered Lovenox (Sanofi-Aventis, Bridgewater, NJ) 60 mg, a low–molecular-weight heparin, subcutaneously every 12 hours, until her INR increased to 2 to 3 times normal. She was also prescribed warfarin, 2.5 mg orally on a daily basis for 6 months, to maintain her elevated INR. Increasing the athlete's INR was intended to drastically reduce the likelihood of developing further clots. While she was on blood thinners, she was unable to participate in any activity that might subject her to injury. Thus, she was limited to basic gymnastic skills and cardiovascular exercise. After the course of blood thinners ended, she was required to wait for 2 weeks, until the medicine was completely eliminated from her system, and then was allowed to return to full sport activity.

Go to: DISCUSSION Only 2 other cases of PE have been documented in young athletes, and both were in high school-aged, male student-athletes.2,7 This case study may present the only female athlete with PE described in the literature. Our athlete did not have any genetic predispositions based on history and blood tests. Environmentally, an oral contraceptive may have played a role in predisposing the athlete to PE; however, she did not display other risk factors associated with deep vein thrombosis or PE (Table 2).3

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Table 2

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Pulmonary Emboli Risk Factors3 Environmental factors such as smoking, obesity, and hospitalization or bed rest typically are not factors in the athletic population, yet they must be reviewed during the history and initial evaluation. Oral contraceptives, travel above 3000 ft (914 m) or for longer than 4 hours, and pregnancy are factors that health care providers for a younger athletic population must investigate during a diagnostic evaluation. Pregnancy may induce PE, in part because of the associated hypercoagulability and obstructed venous return by the enlarged uterus; therefore, it must be eliminated as a potential cause of PE. Oral contraceptives have also been identified as a risk factor, particularly within the first year of treatment. 3,8 In this case the athlete had just started contraceptive medication within 3 months, which may have played a role in development of the PE. Estrogen-containing contraceptives carry a small increased risk of PE that can be exacerbated in the presence of a genetic procoagulant mutation, such as factor V Leiden.3,8,9 The use of estrogen-containing contraceptives is contraindicated in females with a history of thrombophilic states or inherited thrombophilias. Thus, females with a thrombophilic history should be tested for several inherited conditions, including factor V Leiden, prothrombin gene mutation, protein S deficiency, protein C deficiency, antithrombin deficiency, and dysfibrinogenemia (fibrin disorders) before estrogen-containing contraceptives are prescribed.3,9 Factor V Leiden mutation accounts for 50% to 60% of thrombophilic cases.3 Based on her history, the athlete did not have any inherited predisposition to thrombophilic events that would have signaled the need for testing, nor did she have a history suggesting pregnancy. Nonetheless, health care providers should understand and screen for inherited conditions, which, when coupled with oral contraceptive use, can create a high-risk scenario for PE or thromboembolism.3,8 We present the case of an athlete who developed 2 acute, submassive PEs. Pulmonary embolisms are categorized as either acute or chronic. Acute PE

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develops in a short period of time and either is treated and dissolves or results in mortality.1 Chronic PE occurs when an initially acute PE seems to dissolve, but incompletely, resulting in smaller emboli that travel to the lungs.1 Acute PE can be further categorized by the amount of pulmonary artery involvement, the presence or absence of a major predisposing factor, embolus mobility, or the interaction of PE size and underlying cardiovascular status.1 Massive and submassive are the 2 subsets for PE based on pulmonary artery involvement. A massive PE arises when a pulmonary vasculature obstruction of more than 50% occurs or in more than 1 lobar artery1 and is defined as shock or hypotension (systolic blood pressure of less than 90 mm Hg) or a blood pressure decrease of more than 40 mm Hg for longer than 15 minutes.1 Unlike massive PE, submassive PE is characterized by right ventricular dysfunction without hemodynamic instability, which can be identified through electrocardiography.1 Several undiagnosed submassive PEs can lead to a massive PE.1 The specific type of PE may not be particularly important for initial evaluation and referral, but the underlying risk factors and primary evaluation provide evidence for the final diagnosis and, therefore, should be understood by the health care practitioner. The knowledge gained from proper differentiation will aid the health care provider in monitoring symptoms should the athlete develop a second PE. The first published study on a high school wrestler with this condition involved a massive PE.7 The second study was of a high school soccer player with many acute PEs of unknown origin.2 We report on submassive acute PEs in both lower lobes of the athlete's lungs. Thus, despite the paucity of information in the literature, clinicians should be aware of the range of forms PE can take in the young studentathlete population.

Preventing PE is difficult for health care providers dealing with athletes, who tend to be young and healthy. A family history questionnaire during the preparticipation physical examination might allow the clinician to screen for predisposing genetic risk factors. Further testing to assess inherent conditions should be performed based on the initial screening, particularly for female athletes seeking oral contraceptives. Questions that may indicate predisposing factors include a personal or familial history of PE or deep vein thrombosis or a history of stroke or heart attack, all of which could be triggered by a blood clot. Athletes who have predisposing factors for PE should be aware of their risk and informed as to the signs and symptoms that may develop in the presence of a PE. Three techniques for evaluating PEs have been described in the literature.4,5 The first is based on the clinical examination and the likelihood of PE: the Wells

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―Prediction Rule for Deep Vein Thrombosis‖ (Table 3). Each factor for which the answer is yes adds 1 point; factors include active cancer, paralysis or immobilization, being recently bedridden for more than 3 days, swelling of the entire leg, and calf swelling.4 A score of 3 or greater indicates a high chance of deep venous thrombosis. A second test for PE is the Geneva and Wells ―Prediction Rules for Pulmonary Embolism‖ (Table 4). This test examines other factors, including age and previous history of PE or deep vein thrombosis.4 Both prediction tests are performed by a physician whenever an athlete or patient has a suspected PE. Based on the prediction rules, the likelihood of PE for our athlete was not high.

Table 3 Wells Prediction Rule for Deep Vein Thrombosis: Clinical Evaluation Table for Predicting Pretest Probability of Deep Vein Thrombosisa

Table 4 Geneva and Wells Prediction Rules for Pulmonary Embolisma The second method used to evaluate PE is diagnostic imaging: for example, ultrasonography. Ultrasonography has high specificity and sensitivity of diagnosing deep vein thrombosis of the lower extremity. In asymptomatic patients with a high probability of having the condition, such as postoperative patients, specificity is maintained but sensitivity may be decreased.4 Helical computed tomography scanning is another example of diagnostic imaging used for PE and deep vein thrombosis. A computed tomography scan combined with an elevated Ddimer level (despite the low likelihood of PE on the prediction scales) was used to correctly diagnose the athlete in the presence of unremarkable symptoms.

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As a last diagnostic resort, pulmonary angiography can be performed. Pulmonary angiography is usually reserved as a measure of last resort because of high cost, invasiveness, and potential complications in patients with acute respiratory failure. 5 Pulmonary angiography was not conducted on our athlete because a conclusive image was obtained with computed tomography angiography. Side effects are most likely in patients who have had surgical complications (eg, difficulty with anesthesia).

The standard treatment of PE consists of a short regimen of heparin, followed by warfarin. However, the exact length of time patients must remain on an anticoagulant is unclear. Physicians typically make decisions on a case-by-case basis with appropriate monitoring. Some investigators have suggested 3 months; the risk of PE recurrence is higher within the first 3 months of treatment than after that time, regardless of treatment. Six months of drug treatment has also been suggested, but the risk of hemorrhaging during the anticoagulation treatment persists, and careful monitoring is required.6 Longer regimens of anticoagulants are usually reserved for patients with many risk factors, especially recurring PE. The physician treating our athlete selected a 6-month course of anticoagulants as the best option for decreasing the likelihood of recurrent PE in this young, highly active person. To obtain the best outcome for the athlete, health care providers should communicate with the treating physician to monitor or deter activity as warranted.

Athletes prescribed anticoagulation medicines are at much greater risk for secondary damage resulting from injuries because normal blood clotting is compromised. Thus, a simple abrasion could cause excessive bleeding or hemorrhaging, bruising, and concussion. Athletes taking anticoagulation medication should not participate in any contact sport or activity in which they might collide with another person or forcefully hit the ground. In addition, the athlete should avoid any heavy lifting or training in which strains or sprains might occur. Low-level cardiovascular training, with little to no risk of falling, is permissible, as is low-level strength training. Treatment for PE can be effective but may end an athlete's season or athletic career.

Go to: CONCLUSIONS Early diagnosis of PE is the key to appropriate treatment, decreased morbidity, and the likelihood of continued athletic participation. Health care providers should

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ensure proper screening and follow-up treatment if necessary and should monitor athletes diagnosed with PE to facilitate compliance. Physician involvement in diagnosis and continued treatment is essential and should align with sports medicine health care providers' policies and procedures regarding continuity of care and disqualification from participation. Future authors should investigate both the occurrence of PE in the athletic population and optimal treatment to ensure continued participation.

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Footnotes

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Leamor Kahanov, EdD, ATC, and Tarah Daly, MS, contributed to conception and design, analysis and interpretation of the data, and drafting, critical revision, and final approval of the article.

Go to: REFERENCES 1. English J. B. Prodromal signs and symptoms of a venous pulmonary embolism.

Medsurg Nurs. 2006;15(6):352–356.[PubMed] 2. Moffatt K., Silberberg P. J., Gnarra D. J. Pulmonary embolism in an adolescent soccer player: a case report. Med Sci Sports Exerc. 2007;39(6):899–902.[PubMed] 3. Bauer K. A. Overview of the causes of venous thrombosis. UpToDate. www.uptodate.com. Accessed August 24, 2008.

4. Segal J. B., Eng J., Tamariz L. J., Bass E. B. Review of the evidence on diagnosis of deep venous thrombosis and pulmonary embolism. Ann Fam Med. 2007;5(1):63–73. [PMC free article][PubMed] 5. Hartmann I. J., Hagen P. J., Melissant C. F., Postmus P. E., Prins M. H. Diagnosing acute pulmonary embolism: effect of chronic obstructive pulmonary disease on the performance of D-dimer testing, ventilation/perfusion scintigraphy, spiral computed tomographic angiography, and conventional angiography: ANTELOPE Study Group. Advances in New Technologies Evaluating the Localization of Pulmonary Embolism. Am J Resp Crit Care Med. 2007;162(6):2232–2237.[PubMed] 6. Campbell I. A., Bentley D. P., Prescott R. J., Routledge P. A., Shetty H. G. M., Williamson I. J. Anticoagulation for three versus six months in patients with deep vein thrombosis or pulmonary embolism, or both: randomised trial. BMJ. 2007;334(7595):674. [PMC free article][PubMed]

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7. Croyle P. H., Place R. A., Hilgenberg A. D. Massive pulmonary embolism in a high school wrestler. JAMA. 1979;241(8):827–828.[PubMed] 8. Dietrich J. E., Hertweck S. P. Thrombophilias in adolescents: the past, present and future. Curr Opin Obstet Gynecol. 2008;20(5):470–474.[PubMed] 9. Ornstein D. L., Cushman M. Cardiology patient page: factor V Leiden.

Circulation. 2003;107(15):e94–e97.[PubMed] Published online 2012 January 13. doi: 10.1186/1758-2555-4-4 PMCID: PMC3398328

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Biomechanical approaches to understanding the potentially injurious demands of gymnastic-style impact landings

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Marianne JR Gittoes 1 and Gareth Irwin1 Author information ► Article notes ► Copyright and License information ► Go to: Abstract Gymnasts are exposed to a high incidence of impact landings due to the execution of repeated dismount performances. Biomechanical research can help inform recent discussions surrounding a proposed rule change in potentially injurious gymnastic dismounting. The review examines existing understanding of the mechanisms influencing the impact loads incurred in gymnastic-style landings achieved using biomechanical approaches. Laboratory-based and theoretical modelling research of inherent and regulatory mechanisms is appraised. The integration of the existing insights into injury prevention interventions studies is further considered in the appraisals. While laboratory-based studies have traditionally been favoured, the difficulty in controlling and isolating mechanisms of interest has partially restricted the understanding gained. An increase in the use of theoretical approaches has been evident over the past two decades, which has successfully enhanced insight into less readily modified mechanisms. For example, the important contribution of mass compositions and 'tuned' mass coupling responses to impact loading has been evidenced. While theoretical studies have advanced knowledge in impact landing mechanics, restrictions in the availability of laboratory-based input data have suppressed the benefits gained. The advantages of integrating laboratory-based and theoretical approaches in furthering scientific understanding of loading mechanisms have been recognised in the literature. Since a multi-mechanism contribution to impact loading has been evident, a deviation away from studies examining isolated mechanisms may be supported for the future. A further scientific understanding of the use of regulatory mechanisms in

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alleviating a performer's inherent injury predisposition may subsequently be gained and used to inform potential rule changes in gymnastics. While the use of controlled studies for providing scientific evidence for the effectiveness of gymnastics injury counter measures has been advocated over the past decade, a lack of information based on randomised controlled studies or actual evaluation of counter measures in the field setting has been highlighted. The subsequent integration of insight into biomechanical risk factors of landing with clinical practice interventions has been recently advocated.

Keywords: Impact loading, Laboratory-Based Research, Theoretical Research, Inherent Mechanisms, Regulatory Mechanisms Go to: Review Introduction Gymnastic-style landings involving high-velocity impacts and controlled rotation during ground contact are performed regularly in sport e.g. during landing from a vertical jump or in dismounting from a gymnastics apparatus. Gymnasts are naturally exposed to a high frequency of impact landings and may be required to perform dismounts in excess of 200 times a week [1]. Unlike many other sports involving impact landings, gymnastic routines uniquely require a simultaneous address of performance and injury objectives. In dismounting, gymnasts are challenged by the need to modulate a prescribed rotation of the body orientation in flight to ensure the feet contact the ground. For example, when dismounting from the beam apparatus, gymnasts are frequently required to prepare for landing following a backward or forward somersault (rotation about the transverse axis) performed with high degrees of hip flexion (piked position). The subsequent ground contact or impact landing phase must be achieved using a safe, aesthetic and well-executed, double-foot landing. Although performed less frequently, single-foot impact landings such as performed in a floor routine, require similar performance and injury objectives to be addressed but typically require a succeeding skill to be performed.

Constraints in the ability of a gymnast to satisfy the multiple requirements of competitive landing tasks have subsequently been linked to errors in performance and high injury incidence rates [2]. Performance deductions may, for example be incurred for the execution of an uneven landing involving the use of multiple, single-foot placements during the impact landing phase. A serious problem faced

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by modern-day gymnasts is however the subsequent injury risks associated with competitive landing tasks. In 1983, Hunter and Torgan [3] questioned the need to re-evaluate gymnastic scoring of dismounts following the high incidence of associated major acute knee injuries e.g. tears to the anterior cruciate ligament.

Caine and colleagues [4] highlighted that 36% of all injuries sustained by young competitive females occurred during dismounting. Singh and colleagues [5] more recently confirmed that gymnastics had one of the highest injury rates for all girls' sports between 1999 and 2005 and reported a high proportion of acute strain/sprain (44.5%) and fracture/dislocation (30.4%) diagnoses within the respective cohort.

While contemporary epidemiological studies of gymnastic-related injuries have remained sparse, discussions for rule changes to de-emphasise 'sticking' landing routines in the scoring of dismounts have remained evident in the biomechanics literatures [e.g. [6]].

The ability of a performer to resist the collapse of the lower extremities has been suggested to influence the success with which reaction forces are attenuated [2].

Performers are exposed to rapidly occurring and high magnitudes of ground reactions forces during impact landings typically performed in gymnastic. Peak vertical ground reaction forces exceeding nine bodyweights and occurring in less than 0.05 s have been reported by McNitt-Gray and colleagues [2] for drop landings (height: 1.82 m) performed by gymnasts. Biomechanical analyses of the loading mechanisms used in double- and single-foot impact landings provide scientific support for the physical demands incurred on the gymnastic performer.

Quantification of the physical demands imposed in landing may subsequently help to inform the respective discussions surrounding a potential rule change in gymnastic dismounting. The aim of this review was to appraise the development of current understanding of the loading mechanisms influencing the potentially injurious demands of gymnastic-style impact landings using biomechanical approaches. The review typically appraised existing insights into double-foot impact landings in order to assist the discussions regarding regulatory changes in commonly performed gymnastics dismounts.

Loading mechanisms As evidenced in Table Table1,1, biomechanical investigations of commonlyperformed gymnastic-style impact landings have endeavoured to enhance insight into the inherent and regulatory mechanisms that can influence loading and the physical demands incurred. Multiple innate mechanisms including a performer's lower leg alignment [7], neuromuscular control [8], knee joint musculature [9-11] and joint laxity [12] have been linked to injury predisposition and have further

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been accounted for by gender differences. Gender disparities in the incidence of impact landing injuries have additionally been attributed to athletic posture and movement patterns [13], which may be modified or regulated by the performer. As a partial consequence of the voluntary or sub-conscious adaptations that can be achieved and integrated into safe and effective landing protocols, insights into regulatory loading mechanisms have typically been widespread in the literature.

Studies of regulatory mechanisms have examined landing experience [14], impact velocity or height [2,14,15], technique [16-18] and the nature of the impacting interface [2]. While some mechanisms have been consistently recognised as contributors to injury predisposition in impact landings, less well documented mechanisms such as a performer's inherent mass composition [19,20] and lower extremity stiffness response, which was defined as the relationship between the deformation of a body and a given force [21], have recently emerged in the literature. The most prominent mechanisms contributing to impact loading have however been difficult to ascertain due to the frequent examination of isolated mechanisms and the use of diverse research approaches and analyses.

Table 1 Summary of biomechanical studies of loading mechanisms in impact landings Laboratory-based studies of loading mechanisms The majority of biomechanical investigations of impact landings have utilised laboratory-based approaches that have provided descriptive insights into regulatory loading mechanisms. While the laboratory-based approaches have included, practical hypothesis-driven experimental studies, the majority of studies have been observational in nature. As highlighted by Yeow and colleagues [15], many previous studies had specifically used motion analyses to examine various landing conditions e.g. diverse heights [14,15,22-24], lower extremity landing technique [15,16,25-27], experience [14,22,24] and the nature of the impacting interface [2,23]. Laboratory-based studies examining regulatory changes to landing technique have been the most evident in the literature. Decker and colleagues [28]

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reported that it has generally been accepted that the internal and external loads experienced in landing may be manipulated by the lower extremity kinematics (technique). While investigations of self-selected techniques have established a common phasic joint-by-joint reduction in whole body momentum [14,16,19,29], studies identifying individual and marginal ankle, knee and hip joint kinematic adjustments have suggested contradictory effects on the resulting impact loads [2,15,30,31]. Other studies [15,16,23,25-27] examined the effects of diverse degrees of knee joint flexion during ground contact using controlled comparisons of 'stiff' and 'soft' landing techniques, which were typically differentiated by the maximum knee flexion permitted on initial ground contact. As illustrated in Table Table1,1, an inverse relationship between the degree of initial or maximum knee flexion and the resulting peak ground reaction force experienced has been commonly reported in the respective studies. As a consequence of the need to execute prescribed landing techniques to achieve high dismount scores in gymnastics, biomechanical studies implementing a restricted rather than selfselected knee joint motion may better examine the demands of a gymnastic performer.

Further research has examined the associative effects of multiple regulatory loading mechanisms. Studies investigating the interaction of landing height with experience [14,22,24] or the nature of the impacting interface [22,23] have been prominent but a continuing lack of laboratory-based data regarding high landing heights has been reported [15]. As evidenced in Table Table1,1, laboratory-studies involving controlled drop landings have been common and have typically examined landing performed from heights of less than 1.50m without prior flight phase rotation. Studies examining 'real' gymnastic-style landings e.g. Gittoes and colleagues [32], have however highlighted that realistic landing heights for gymnastic dismounts typically exceed 2.00m. While some insight into more complex gymnastic-style landings involving flight phase rotation has been achieved in the literature [32,33] limited understanding of the regulation of loading in more challenging dismounts continues to exist. Since, gymnastic dismounts are typically characterised by: 1. a requirement to gain height in flight; 2. a need to control whole body orientation in landing and 3. an exacerbated lower limb injury risk, extended insight into challenging 'realistic' height conditions and more complex gymnastic landing manoeuvres is warranted.

Within gymnastics routines, females typically have a shorter time in the air and subsequently gain less height than males. In order to achieve higher scores, females continue to attempt similar transverse (somersaulting) and longitudinal (twisting) rotations to their male counterparts, which potentially accentuates the

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physical demands experienced by females. The heightened injury predisposition of females performing impact landings has primarily been addressed by an extensive body of research examining gender-related mechanical responses [18,28,31,34,35].

Contradictory findings regarding gender-based techniques have however limited understanding of the primary loading mechanisms underpinning impact landings.

Gender comparisons of the techniques employed in double-foot drop jump landings have suggested a tendency for the use of a greater range of motion in the knee (20%) [28] and ankle (up to 39%) [28,35] by females compared to males.

Cortes and colleagues [18] contrastingly suggested a lack of gender differences in lower extremity joint flexion angles during the ground contact phase of double-foot drop landings performed utilising diverse foot placement strategies.

In contrast to studies examining landing technique, investigations of gender-based loading responses in single- [31] and double-foot [35] have frequently confirmed heightened lower extremity loading in females compared to males. Females have been suggested to be predisposed to larger peak vertical ground reaction forces of between 9% [31] and 34% [35] when compared to their male counterparts. The current lack of consensus regarding the gender-based landing technique and loading responses predisposing females to injury in impact landings inhibits the extent to which gender-based prevention strategies may be developed and implemented. The preference for kinematic analyses alone and diversity in the protocols investigated in gender-based studies may partially contribute to the incomplete insight gained in the literature. Further insight into the gender-disparity may subsequently be achieved by the wider application of more comprehensive biomechanical analyses. As evidenced by Decker and colleagues [28], examinations of internal joint kinetics have been important in quantifying loads for establishing gender-based control strategies during drop landings. Future studies that further examine the interaction of gender-based technique modifications and the resulting internal and external loads may therefore be warranted in the literature.

Quantification of the joint moments of force produced at the ankle, knee and hip have provided a valuable understanding of the internal loads, joint-specific stresses and controlling mechanisms used to decelerate the body in landing [36]. Inverse dynamics, which integrates kinematic, external force and inertia data collected in a laboratory based setting with a linked-segment assumption, has been the preferred tool for the estimation of internal joint loading. While employing inverse dynamic analyses, DeVita and Skelly [16] established a 19% greater absorption of the body's kinetic energy in a soft landing (less than 90° knee flexion) compared to a stiff landing (greater than 90° of knee flexion). While also using inverse dynamic

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analyses, Kovacs and colleagues [17] reported greater relative knee joint contributions to the total lower extremity torque produced using a heel-toe (45%) compared to a forefoot (37%) landing technique. However, Kovacs and colleagues [17] further recognised the need to examine individual muscle contributions, which are precluded in inverse dynamic analyses, through the use of electromyography.

More recent laboratory-based studies continue to advocate the use of inverse dynamics [e.g. [15]] and electromyography [e.g. [11]] for the estimation of internal loading in dynamic movements. Although potentially limited by their descriptive nature, laboratory-based studies continue to remain popular in biomechanical investigations of landing and are becoming more evident in a growing body of research examining the influence of applied injury prevention strategies.

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Application of laboratory-based studies to injury prevention strategies As suggested by Daly and colleagues [6] in 2001, controlled trials may provide the best scientific evidence for the effectiveness of gymnastics injury counter measures, but a lack of information based on randomised controlled studies or actual evaluations of counter measures in the field setting existed. While the use of a 'correct technique' had been considered essential to prevent gymnastics injuries in landing [6], an explicit link between adapted landing techniques and an alleviation of the high incidence of gymnastic-style landing injuries had been difficult to ascertain in the literature. As further evidenced by the contradictory outcomes of gender-based studies, establishing common responses to loading mechanisms, that may inform injury prevention programs, has proven difficult. In 2000, Boden and colleagues [13] had however suggested that improved jumping, stopping and turning techniques had shown promising results in injury prevention programs.

A number of recent studies have attempted to identify biomechanical predictors of landing injuries for prevention interventions [37-39]. 'Clinician friendly' approaches for predicting anterior cruciate ligament injuries in impacts using biomechanical measures such as knee flexion range of motion have been identified [37,39]. However, relatively less attention has been given to establishing the shortand long-term effectiveness of injury prevention interventions. As suggested by Daly and colleagues [6] over a decade ago, continuing biomechanical research into the mechanism(s) of gymnastics injury and the influence of different landing techniques on injury prevention should be considered in counter measure research.

More recently, the continued need to 'bridge the gap' between laboratory identification of biomechanical risk factors in landing and clinical practice has been recognised by Myer and colleagues [39].

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Theoretical studies of loading mechanisms

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Despite intense laboratory-based study, the associated descriptive analyses, and control and ethical constraints has precluded a thorough causal insight into the effects of prevalent loading mechanisms in challenging impact landings. As indicated in Table Table1,1, biomechanics studies using a less conventional theoretical approach have emerged in the landing literature. A theoretical approach uses a theory or model to make predictions about the behaviour of a system [40] and permits a non-invasive, systematic manipulation of independent variables or mechanisms of interest through simulation. While a theoretical approach alone offers a solution to the limited control associated with more traditional scientific approaches, caution in using the approach must be taken due to a potential lack of realism to the living human performer. Laboratory-derived data from experimental or observational studies are however frequently used to ensure realistic inputs for a theoretical model, and to check the accuracy and validity of the predicted outcomes.

Until recently, theoretical approaches using rigid body simulation models, which assume the human performer may be represented by a series of single segment rigid components, have been customary for gaining insight into loading mechanisms [41,42]. The frequent presence of uncharacteristic oscillations in the internal joint load estimations derived in numerous kinetic analyses conducted using rigid body and inverse dynamic assumptions [16,22] had however questioned the assumption of whole body rigidity, particularly for dynamic impacts. In 1998, Gruber, and colleagues [43] conducted an innovative theoretical study to specifically examine the potential limitations of inverse dynamic analyses and rigid body assumptions on load estimations during a gymnastic-style drop landing.

Gruber and colleagues [43] reported that rigid body assumptions yielded completely incorrect predictions of internal joint loads during the impact phase such that hip joint torques may be three to four times too large. More realistic skeleto-mechanical models of impact landings that incorporate soft tissue properties have subsequently become more evident in the literature over the past decade. The models, which have been termed 'wobbling mass' models, have increasingly been used to investigate the influence of soft and rigid tissue mass compositions on impact loading during simulated running [44,45] and more dynamic gymnastic-style landings [20,46-49]. Simulation studies employing 'wobbling mass' models have reported soft tissue contributions to an external peak impact load reduction of as much as 8.6 [49] and 24.3 [19] bodyweights in double foot drop landings performed with a forefoot- and heel-first ground contact, respectively.

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'Wobbling mass' studies have partially attributed soft tissue loading contributions to regulation of the coupling between soft and rigid masses, which has been associated with modified muscle activity levels or muscle tuning [45]. Mass coupling represents the elasticity and damping characteristics of soft tissue (e.g. muscle, skin, subcutaneous fat) motion relative to the underlying rigid mass (e.g. bone) within a human segment e.g. thigh or shank. Liu and Nigg [44] had further supported the notion that through muscle tuning, mass coupling properties may interact with inherent mass distributions to control the forces incurred in simulated running impacts. Reductions in the damping between soft and rigid masses were later found to positively interact with localised rigid mass compositions by providing a 0.13 bodyweight additional external load attenuation during potentially injurious gymnastic-style landings [20]. If the concept of muscle tuning is correct, a subject-specific response to impact loading may be expected [45] and has been supported by the reporting of idiosyncratic responses to peak load attenuation with adapted soft tissue compositions [20]. Insight into prevalent loading mechanisms and injury predisposition in gymnastic-style landings may subsequently warrant more individual performer analyses in the future.

The theoretical support for a link between impact loading and mass compositions advocates the need for extended 'wobbling mass' modelling research into regulatory mechanisms that may alleviate a performer's innate injury predisposition. While high-speed filming of impact situations has provided insight into the complex damped manner of soft tissue motion [43], the general lack of soft and rigid mass information from living subjects currently inhibits the widespread use of 'wobbling mass' models [50]. While evidently beneficial, the increase in model complexity associated with wobbling mass compared to rigid body models is further associated with heightened development and processing demands.

Despite the potential increase in simulation run time, Mills and colleagues [47] advocated a continued need to prioritise the selection of a simulation model that determines realistic internal forces when assessing injury risk in gymnastics landing. The continued merger of laboratory information with advances in theoretical modelling may subsequently offer a successful approach to ensuring a sustained enhancement of knowledge in impact biomechanics and injury prevention strategies.

Application of theoretical studies to injury prevention strategies While recent efforts to integrate laboratory-based findings into injury prevention studies are being made [37-39], the explicit integration of theoretical study insights remains sparse. Unlike laboratory-based studies, theoretical investigations can

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provide explicit information on the magnitude of impact loading change that may be incurred by systematic changes to a regulatory loading mechanism. The permitted address of 'cause and effect' based research questions can subsequently provide advance knowledge for injury prevention interventions.

Recent theoretical studies [19,49] have explicitly supported the load attenuation benefits of soft tissue properties and marginally adapted mass coupling regulatory mechanisms, which have traditionally been difficult to ascertain in laboratorybased studies. Further studies have acknowledged that while a performer's innate mass compositions may be difficult to alter, tuning of the self-selected landing technique [51] and mass coupling [19,49] responses may alleviate a natural predisposition to high impact loading. As further suggested in the study of Gittoes and colleagues [51], marginal changes (up to 5 ms) to the timing of the ankle and knee joint action could influence external impact loading by as much as 3.9 and 1.5 bodyweights, respectively in gymnastic-style landing protocols.

Due the potential counter effect of internal and external loading [48,51], and idiosyncratic responses [51], caution in considering the explicit influence of regulatory changes on impact loading has been highlighted by the theoretical literature. As recently evidenced by Mills and colleagues [48], using a reduction in external loading (ground reaction force), due to a change in landing technique, as a basis for a reduction in injury potential in gymnastic movements may not be appropriate since internal loading can be heightened. Injury prevention programmes that are customised to specific performers, and assessed following internal and external loading analyses may therefore be warranted when informing prevention strategies developed to alleviate the physical demands incurred in gymnastic-style landings.

Future directions While the existing body of biomechanical research into gymnastic-style impact landings has traditionally been laboratory-based, theoretical studies, which have offered distinct advancements in knowledge, remain relatively sparse in the literature. In order to benefit from the ecological validity of laboratory studies, and the systematic control and non-invasive testing environment of theoretical investigations, a more widespread use of an approach that integrates data obtained from the field or laboratory with theoretical models may be advocated in future investigations. In particular, the growing number of theoretical studies using 'wobbling mass' models [20,46,47], may be more effectively employed to develop insight into loading in gymnastic-style landings with the availability of increased

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empirical support regarding soft tissue properties. While the mechanisms predisposing a performer to gymnastic-style impact injuries may be multi-factorial in nature, the majority of existing research continues to favour examination of isolated loading mechanisms. The extent to which regulatory mechanisms can be used to alleviate an innate predisposition remains relatively under-documented.

Evidence of performer-specific responses to impact loading [20,31] supports a need to further consider, through the simultaneous examination of multiple mechanisms, the interaction of innate profiles and regulatory mechanisms in understanding injury predisposition. A deviation from the tendency to consider internal and external loading in isolation may be further advocated in future research due to evidential support from theoretical studies [48,51] for a potential antagonistic response in the respective measures.

Considering the likely maintenance of a scoring system for gymnastic dismounting, which requires the achievement of constrained landing techniques, regulatory strategies such as mass coupling tuning, may alleviate a performer's innate predisposition to high physical demands without substantial alterations to technique. Accommodating self-selected landing techniques, which are tailored to the movement conditions and a performer's unique physical composition in the scoring system, may conversely offer substantially greater protection benefits for performers repeatedly executing demanding landings. The success of injury referral schemes and clinical practice is partially reliant on the comprehensive evaluation of injury prevention programmes used in training and competition.

While the suggested need for a growing body of scientific evidence remains justified [6], further attempts to fully integrate existing insight in the development and evaluation of tailored injury prevention interventions is also warranted.

Go to: Conclusion The review has appraised the development of current understanding of the loading mechanisms contributing to the physical demands of gymnastic-style impact landings using biomechanical approaches. While current insights have typically been derived from laboratory-based studies, investigations employing theoretical approaches are becoming more widely employed in the literature. As a partial consequence of the tendency to examine isolated mechanisms within the respective laboratory and theoretical studies, the primary loading mechanisms influencing the physical demands of gymnastic-style landings remain difficult to ascertain. While enhanced scientific understanding of the interaction of inherent and regulatory

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mechanisms is warranted to inform potential scoring changes in gymnastics, increased attempts to inform the development and evaluation of tailored injury prevention interventions using existing insights should also be made.

Go to: Competing interests The authors declare that they have no competing interests.

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Authors' contributions MJRG prepared and compiled the manuscript. MJRG and GI both contributed to the appraisal of the literature and the approval of the final manuscript.

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Journal of Biomechanics. 2006;39:119–124. doi: 10.1016/j.jbiomech.2004.10.036.[PubMed] [Cross Ref] 20.Gittoes MJR, Kerwin DG. Interactive effects of mass proportions and coupling properties on external loading in simulated forefoot impact landings. Journal of Applied Biomechanics. 2009;25:238–246.[PubMed] 21.Butler RJ, Crowell HP III, McClay-Davis I. Lower extremity stiffness: implications for performance and injury. Clinical Biomechanics.

2003;18:511–517. doi: 10.1016/S0268-0033(03)00071-8.[PubMed] [Cross Ref] 22.McNitt-Gray JL. Kinetics of the lower-extremities during drop landings from 3 heights. Journal of Biomechanics. 1993;26:1037–1046. doi: 10.1016/S0021-9290(05)80003-X.[PubMed] [Cross Ref] 23.Arampatzis A, Brüggemann GP, Klapsing GM. A three-dimensional shankfoot model to determine the foot motion during landings. Medicine and Science in Sports and Exercise. 2002;34:130–138.[PubMed] 24.Seegmiller JG, McCaw ST. Ground reaction forces among gymnasts and recreational athletes in drop landings. Journal of Athletic Training.

2003;38:311–314. [PMC free article][PubMed] 25.Zhang S, Bates BT, Dufek JS. Contributions of lower extremity joints to energy dissipation during landings. Medicine and Science in Sport and Exercise. 2000;32:812–819. doi: 10.1097/00005768-200004000-00014.

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Journal of Applied Biomechanics. 2007;23:203–212.[PubMed] 28.Decker MJ, Torry MR, Wyland DJ, Sterett WI, Steadman JR. Gender differences in lower extremity kinematics, kinetics and energy absorption during landings. Clinical Biomechanics. 2003;18:662–669. doi: 10.1016/S0268-0033(03)00090-1.[PubMed] [Cross Ref]

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29.Lees A. Methods of impact absorption when landing from a jump.

Engineering in Medicine. 1981;10:207–211. doi: 10.1243/EMED_JOUR_1981_010_055_02. [Cross Ref] 30.Yu B, Lin C, Garrett WE. Lower extremity biomechanics during the landing of a stop-jump task. Clinical Biomechanics. 2006;21:297–305. doi: 10.1016/j.clinbiomech.2005.11.003.[PubMed] [Cross Ref] 31.Schmitz RJ, Kulas AS, Perrin DH, Riemann BL, Shultz SJ. Sex differences in lower extremity biomechanics during single leg landings. Clinical Biomechanics. 2007;22:681–688. doi: 10.1016/j.clinbiomech.2007.03.001.[PubMed] [Cross Ref] 32.Gittoes MJR, Irwin GI, Mullineaux DR, Kerwin DG. Whole-body and multi-joint kinematic control strategy variability during backward rotating dismounts from beam. Journal of Sport Sciences. 2011;29:1051–1058. doi: 10.1080/02640414.2011.576690. [Cross Ref] 33.McNitt-Gray JL, Hester DME, Mathiyakom W, Munkasy BA. Mechanical demand and multijoint control during landing depend on orientation of the body segments relative to the reaction force. Journal of Biomechanics.

2001;34:1471–1482. doi: 10.1016/S0021-9290(01)00110-5.[PubMed] [Cross Ref] 34.Chappell JD, Yu B, Kirkendall DT, Garrett WE. A comparison of knee kinetics between male and female recreational athletes in stop-jump tasks.

American Journal of Sports Medicine. 2002;30:261–267.[PubMed] 35.Kernozek TW, Torry MR, van Hoof H, Cowley H, Tanner S. Gender differences in frontal and sagittal plane biomechanics in drop landings.

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36.Dufek JS, Bates BT. Biomechanical factors associated with injury during landing in jump sports. Sports Medicine. 1991;12:326–337. doi: 10.2165/00007256-199112050-00005.[PubMed] [Cross Ref] 37.Myer GD, Ford KR, Khoury J, Succop P, Hewett TE. Clinical correlates to laboratory measures for use in non-contact anterior cruciate ligament injury risk prediction algorithm. Clinical Biomechanics. 2010;25:693–699. doi: 10.1016/j.clinbiomech.2010.04.016. [PMC free article][PubMed] [Cross Ref] 38.Padua DA, Boling MC, DiStefano LJ, Onate JA, Beutler AI, Marshall SW. Reliability of landing error scoring system real-time, a clinical assessment tool of jump-landing biomechanics. Journal of Sport Rehabilitation.

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analysis. British Journal of Sports Medicine. 2011;45:238–244. doi: 10.1136/bjsm.2010.072843.[PubMed] [Cross Ref] 40.Yeadon MR, Challis JH. Review of sports biomechanics research. Journal of Sports Sciences. 1994;12:3–32. doi: 10.1080/02640419408732156.[PubMed] [Cross Ref] 41.Hatze H. A comprehensive model for human motion simulation and its application to the take-off phase of the long-jump. Journal of Biomechanics.

1981;14:135–142. doi: 10.1016/0021-9290(81)90019-1.[PubMed] [Cross Ref] 42.Gerritsen KGM, van den Bogert AJ, Nigg BM. Direct dynamics simulation of the impact phase in heel-toe running. Journal of Biomechanics.

1995;28:661–668. doi: 10.1016/0021-9290(94)00127-P.[PubMed] [Cross Ref] 43.Gruber K, Ruder H, Denoth J, Schneider K. A comparative study of impact dynamics: Wobbling mass model versus rigid body models. Journal of Biomechanics. 1998;31:439–444. doi: 10.1016/S0021-9290(98)000335.[PubMed] [Cross Ref] 44.Liu W, Nigg BM. A mechanical model to determine the influence of masses and mass distribution on the impact force during running. Journal of Biomechanics. 2000;33:219–224. doi: 10.1016/S0021-9290(99)001517.[PubMed] [Cross Ref] 45.Nigg BM, Liu W. The effect of muscle stiffness and damping on simulated impact force peaks during running. Journal of Biomechanics. 1999;32:849– 856. doi: 10.1016/S0021-9290(99)00048-2.[PubMed] [Cross Ref] 46.Pain MTG, Challis JH. Wobbling mass influence on impact ground reaction forces: A simulation model sensitivity analysis. Journal of Applied Biomechanics. 2004;20:309–316.

47.Mills C, Pain MTG, Yeadon MR. The influence of simulation model complexity on the estimation of joint loading in gymnastics landings.

Journal of Biomechanics. 2008;41:620–628. doi: 10.1016/j.jbiomech.2007.10.001.[PubMed] [Cross Ref] 48.Mills C, Pain MTG, Yeadon MR. Reducing ground reaction forces in gymnastics' landings may increase internal loading. Journal of Biomechanics. 2009;42:671–678. doi: 10.1016/j.jbiomech.2009.01.019.[PubMed] [Cross Ref] 49.Gittoes MJR, Brewin MA, Kerwin DG. Soft tissue contributions to impact forces using a four-segment wobbling mass model of forefoot-heel landings.

Human Movement Science. 2006;25:775–787. doi: 10.1016/j.humov.2006.04.003.[PubMed] [Cross Ref]

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50.Arthurs KL, Andrews DM. Upper extremity soft and rigid tissue mass prediction using segment anthropometric measures and DXA. Journal of Biomechanics. 2009;42:389–394. doi: 10.1016/j.jbiomech.2008.11.021.[PubMed] [Cross Ref] 51.Gittoes MJR, Kerwin DG, Brewin MA. Sensitivity of loading to the timing of joint kinematic strategies in simulated forefoot impact landings. Journal of Applied Biomechanics. 2009;25:229–237.[PubMed] 52.Sustained skeletal benefit from childhood mechanical loading 53.T. A. Scerpella, J. N. Dowthwaite, and P. F. Rosenbaum 57.Author information ► Copyright and License information ► 59.The publisher's final edited version of this article is available at Osteoporos Int 60.Go to: 61.Abstract 62.Summary 63.Preliminary prospective, longitudinal results suggest that pre-menarcheal exposure to artistic gymnastics is associated with greater radius BMC, aBMD, and projected area throughout growth and into early adulthood, more than 4 years after activity cessation. Any loss of benefit associated with detraining appears to be temporary.

64.Introduction 65.Mechanical loading may enhance bone accrual during growth, but prospective evidence of benefit retention is limited. This prospective, longitudinal cohort study tests whether gymnastics is linked to distal radius advantages during growth and four or more years post-training cessation.

66.Methods 67.Semi-annually, female ex/gymnasts and non-gymnasts underwent height and weight measurements; questionnaires assessed calcium intake, physical activity, and maturation. Annual dual energy X-ray absorptiometry scans (Hologic QDR 4500W) measured total body fat-free mass, skull areal density (aBMD), and bone mineral content (BMC); forearm scans measured ultradistal and 1/3 radius area, BMC, and aBMD. Analysis inclusion criteria were: (1) achievement of gynecological age >4 years and (2) for gymnasts, >2 years of pre-menarcheal training (>6 h/week), ceasing between 0.5 year pre-menarche and 1 year post-menarche. Hierarchical linear modeling (HLM v6.0) evaluated outcomes for ex/gymnasts versus non-gymnasts; a slope/intercept discontinuity evaluated de-training effects.

68.Results 69.Data from 14 non-gymnasts and six ex/gymnasts represented outcomes from 4 years pre-menarche to 9 years post-menarche. All adjusted distal radius

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parameters were higher in ex/gymnasts than non-gymnasts (p<0.02).

Ultradistal BMC, ultradistal aBMD, and 1/3 aBMD temporarily decreased with gymnastic cessation (p<0.04); ultradistal area, 1/3 area, and 1/3 BMC did not change significantly. Skull outcomes did not differ between groups or change with activity cessation.

70.Conclusion 71.Gymnastic exposure during childhood and early puberty is associated with greater radius bone mass, size, and aBMD. Despite brief de-training losses in density and mass, significant skeletal benefits are manifested throughout growth and at least 4 years beyond activity cessation into early adulthood.

72.Keywords: Adolescence, Bone, DXA, Female, Mechanical loading, Radius 73.Go to: 74.Introduction 75.Adult bone quality is likely improved by optimization of skeletal growth through childhood and adolescence. Mechanical loading during growth appears to enhance bone accrual. However, most evidence of residual benefits in adulthood is retrospective and cross-sectional in nature, based upon a single adult measurement only. There are few prospective, longitudinal studies that evaluate long-term benefits of pediatric loading in a series of observations as growth progresses. In a unique longitudinal study, Gunter et al. noted retention of skeletal improvements in a group of young women for 7 years after a childhood jumping program [1]. Benefits were small but significant (+1.4%) and had diminished since intervention completion.

76.Gymnastics has been studied extensively as a model of mechanical loading.

Numerous pediatric studies have reported advantages in skeletal measures for gymnasts versus non-gymnasts, and several have reported increased bone accrual over a 1–3-year period. Several dual energy X-ray absorptiometry (DXA) studies report residual advantages in bone mineral measures among ex-gymnasts compared to non-gymnasts [2–5]. Complementing existing DXA evidence, Eser et al. used three-dimensional peripheral quantitative computed tomography (pQCT) to evaluate retention of skeletal advantages in ex-gymnasts (aged 18–36 years), 3–18 years after gymnastics cessation, reporting significant residual advantages in upper extremity bone geometry [6].

77.To date, there are no prospectively measured, longitudinal analyses documenting subject-specific acquisition of skeletal benefits during the course of childhood mechanical loading and demonstrating retention of these benefits in adulthood. Furthermore, most existing studies do not account for disparate rates of physical maturation among gymnasts and non-gymnasts,

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which may confound studies of skeletal development. Therefore, the purpose of this paper is to report preliminary results from a prospective, longitudinal study, accounting for variability in growth and maturation, and testing the hypothesis that skeletal benefits attributed to childhood gymnastic exposure persist into young adulthood.

78.Go to: 79.Methods 80.Protocol for this longitudinal bone accrual study (1997–present) was approved by the SUNY Upstate Medical University Institutional Review Board and has been performed in accordance with the ethical standards of the 1964 Declaration of Helsinki. Girls and/or their parents provided informed assent/consent, as dictated by subject age. Pre-menarcheal girls aged 8 to 12 were recruited in two phases (1997: 55 gymnasts, 20 nongymnasts; 2002: 15 gymnasts, 25 non-gymnasts); a small subset of postmenarcheal gymnasts was recruited to compensate for peri-menarcheal subject attrition. As subjects were originally recruited for only 18–36-month studies, many withdrew after providing data for these periods. Of those who continued participation, few were included in this analysis due to stringent inclusion criteria: (1) achievement of gynecological age (years postmenarche) greater than 4 years; (2) for gymnasts, at least 2 years of premenarcheal gymnastic training (defined as greater than 6 h/week), continuing to 0.5 year pre-menarche and ceasing by 1 year post-menarche.

Thus, ―ex/gymnasts‖ were gymnasts prior to menarche and ex-gymnasts for at least 4 years post-menarche. Gymnasts who continued training beyond 1 year post-menarche were excluded. ―Non-gymnasts‖ were a heterogeneous group of athletes and non-athletes (e.g., lacrosse, basketball, track, dance).

81.Semi-annually, girls underwent anthropometric measurements and completed questionnaires on calcium intake, physical activity, and maturation [7]. Non-dominant forearm and total body DXA scans were performed annually. Total body scans measured total fat-free mass (FFM) and skull outcomes (areal bone mineral density (aBMD), bone mineral content (BMC)). Forearm scans were evaluated at ultradistal (metaphyseal) and 1/3 (diaphyseal) radius sites, yielding bone projected area, BMC, and aBMD (Hologic QDR 4500W). The coefficient of variation for this machine is 1% for both total body and forearm scans. The majority of scans were performed by the same technician (C. Riley, 2000 onward). All scans were re-analyzed by a single researcher (J. Dowthwaite) using Discovery A software (v12.7) to ensure optimal consistency. In contrast to standard Hologic protocols, forearm analysis boxes were placed to yield consistent distal radius regions of interest throughout development (ulnar position was

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disregarded due to discrepant ulna versus radius positions). The analysis box included the distal articular edge of the ulnar side of the radius and excluded carpal bones. The rationale for evaluation of non-dominant distal radius scans was: (1) total body mass impact loading of the non-dominant arm distinguishes gymnastic loading from most other activities, theoretically yielding the most sensitive indicator of adaptation to gymnastic exposure; (2) the radius is the primary weight-bearing bone in the distal forearm; and (3) influence of fan beam magnification error is minimal at this site. For comparison, the skull was evaluated as a non-loaded, control site.

82.Hierarchical linear modeling (HLM, also known as multilevel modeling) is a more complex outgrowth of traditional regression modeling used to link each subject‘s repeated measures for appropriate treatment of longitudinal data with time-varying covariates (HLM v6.0, alpha=0.05). Menarcheal age and linear/quadratic functions of gynecological age (years pre- and postmenarche) were included in the model, centering analyses at menarche to account for the potential confounding influence of variability in rate of physical maturation upon bone outcomes. Height, FFM, and calcium intake served as time-varying covariates. Gymnastic status was evaluated dichotomously as the focus of this simple preliminary analysis; other weight-bearing physical activity was not evaluated. Intercept and slope discontinuities were evaluated as indicators of short- and long- term detriments associated with training cessation. Age at menarche was evaluated as a non-time-varying predictor. A priori power analyses used cross-sectional ANCOVA to compare forearm aBMD in ex-gymnasts versus non-gymnasts at 18 months post-menarche and >2 years post-cessation [5], yielding projected required cell sizes of n=7 (80% power). For this preliminary analysis, ex/gymnasts (n=6) are just short of estimated cell size for cross-sectional analyses, but post hoc power analyses for longitudinal HLM of all radius variables indicate >85% power to detect significant differences [8]. In contrast, for skull outcome differences, power was <10% due to smaller effect sizes.

83.Go to: 84.Results 85.Distal radius parameters were evaluated for 20 subjects (14 non-gymnasts, 6 ex/gymnasts), representing growth from 4.0 years pre-menarche to 9.3 years post-menarche, totaling 146 observations (104 non-gymnast, 42 ex/gymnast). The number of annual DXA scans per subject varied from 4 to 11 (non-gymnasts 4–11 scans, mean=7.4; ex/gymnasts 6–8 scans, mean=7.0). There were no significant differences between groups for any independent variable at initial or final measurement points (Table 1,

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ANOVA, p>0.05); initial and final Tanner breast stage distributions were similar. Subsequent to menarche (non-gymnasts) or cessation of gymnastics (ex/gymnasts), ex-gymnast versus non-gymnast differences were not detected for physical activity participation (ANOVA, p>0.64).

86.

87.Table 1 88.Subject characteristics by gymnast status 89.Accounting for gynecological age, height, FFM, age at menarche, and calcium intake, all distal radius parameters were higher in ex/gymnasts than non-gymnasts (p<0.02, Fig. 1a, b), as indicated by distinct ex/gymnast versus non-gymnast growth curves, in which points seldom overlap. In contrast, skull aBMD was not associated with gymnastic status (p>0.83, Fig. 1c); ex/gymnast and non-gymnast curves are continuously intermingled and cannot be distinguished from each other. Similarly, skull BMC differences were not detected (p>0.98, Fig. 1c), although there was a trend toward decreasing ex/gymnast BMC after gymnastic cessation (p<0.06). Gymnastic cessation was not associated with a significant slope decrease for any radius outcome. However, gymnastic cessation was associated with an abrupt, temporary decrease in 1/3 aBMD, ultradistal BMC, and ultradistal aBMD (significant intercept discontinuity, p<0.04). No significant gymnastic cessation effects were observed for 1/3 BMC, 1/3 area, ultradistal area, or skull aBMD. Age at menarche was not a significant predictor for any bone outcome (p>0.35). Similarly, calcium intake was not a significant predictor, except for 1/3 aBMD (negative, p<0.04).

90.

91.Fig. 1 92.Ex/gymnast and non-gymnast data are depicted over a 12-year period of longitudinal growth/accrual, aligned by physical maturity. Data points are aligned by years since menarche (gynecological age) and adjusted for age at menarche, as well as time-varying (more ...)

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93.Go to: 94.Discussion 95.This longitudinal analysis provides the first preliminary evidence of prolonged, post-menarcheal retention of skeletal benefits attributed to mechanical loading during childhood and early adolescence. Ex-gymnasts demonstrated advantages in diaphyseal and metaphyseal distal radius aBMD, BMC, and projected area throughout growth and early adulthood, despite cessation of sub-elite gymnastics training around menarche. As such, ex-gymnast advantages were demonstrated prospectively into early adulthood, from 4 to 9 years post-menarche.

96.One other group has provided prospective, longitudinal evidence of skeletal benefit retention following childhood activity [1, 9, 10]. Fuchs et al. reported retention of benefits in a group of pre-pubertal children who had participated in a 7-month randomized, controlled high-impact loading intervention [9].

Advantages in total hip BMC for the intervention group were 5.4% at the completion of the intervention and 3.5% 7 months later. In a 7-year followup, jumpers maintained a significant 1.4% advantage in total hip BMC [1].

An identical intervention in a separate cohort yielded significantly greater BMC at the total body (2.9%), lumbar spine (2.3%), femoral neck (4.4%), and total hip (3.2%), 3 years following the intervention [10]. The authors attributed the gradual dissipation of benefits in the 7-year cohort to interactions between growth, physical activity, diet, and genetic predisposition over the subsequent period of extensive growth, thereby overwhelming effects of the brief intervention [1].

97.Long-term retention of childhood skeletal advantages has been suggested by several retrospective studies evaluating adult ex-gymnasts. In a crosssectional evaluation, Bass et al. identified 6–26% advantages in aBMD at the arm, proximal femur, and lumbar spine for adult ex-gymnasts at 8 years post-cessation, compared to non-gymnasts; advantages were not diminished with increased cessation interval. Zanker et al. reported 10–17% aBMD advantages at the proximal femur, lumbar spine, and total body for adult exgymnasts 17 years post-cessation [11]. Similarly, at 15 years post-cessation, Kirchner et al. identified significant advantages in lumbar spine, proximal femur, and total body aBMD for former collegiate gymnasts compared to non-gymnasts [3]. At a follow-up evaluation 9 years later, these ex-gymnasts maintained 8–14% advantages over non-gymnasts, at multiple sites (lumbar spine, proximal femur, femoral neck, leg, and arm) and the total body, at a mean of 24 years post-cessation [12]. Ex-gymnasts in these adult studies had participated in gymnastics throughout childhood and adolescence; thus, results indicate maintenance of benefits when gymnastics is continued after

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completion of skeletal growth. Our maturity-specific results suggest maintenance of skeletal benefits in early adulthood following loading exposure during child-hood and early adolescence alone.

98.Eser et al. used three-dimensional pQCT to evaluate retention of skeletal advantages in a broad age range of ex-gymnasts who had ceased gymnastic participation 3–18 years (mean 6.1 years) prior [6]. These investigators identified ex-gymnast advantages in bone geometry of 20–32% in the upper extremity (humerus, radius). Of note, 20 subjects had been retired for 3–6 years, and ten subjects had been retired for 6–18 years. Ex-gymnasts were 18–36 years old (mean age 23±0.9 years) at the time of pQCT study, had participated in gymnastics from a mean age of 6.1 years (range 3.0–9.6 years) and had trained for an average of 10.5 years (range 6–16 years). With a mean menarcheal age of 14.7 years, it appears that most, if not all, exgymnasts trained into their early post-menarcheal years. This contrasts with our population of ex/gymnasts; only one girl participated in gymnastics for more than 1 month post-menarche, retiring at 1 year post-menarche. In addition, the ex-gymnasts in the study by Eser et al. participated at a higher intensity than the ex/gymnasts in our study, with a highest level of 40 h/week and average peak at 23 h/week [6]. The highest annual mean for our cohort was 18.8 h/week, with an average peak annual mean of 14.3 h/week (the average annual mean for the year prior to cessation was 14.2 h/week).

Thus, compared to ex-gymnasts in the study by Eser et al., our results reflect relatively conservative gymnastic exposure. Furthermore, our ex/gymnasts and non-gymnasts did not differ significantly for anthropometric measures at either the initial or the final measurement point, indicating that our ex/gymnasts were effectively ―normal girls‖ exposed to gymnastic loading during growth.

99.Geometric adaptations appear to contribute to observed aBMD advantages in our ex-gymnast cohort, as indicated by significant advantages in radius projected area. Previously, in larger, related samples, we have associated enlarged bone geometry with gymnastic loading using DXA [13] and pQCT [14]. Further evidence of geometric adaptation is provided by childhood gymnast pQCT studies [15, 16] and ex-gymnast results by Eser et al. [6].

Corroborating Eser et al., our results suggest that geometric adaptation to childhood and early adolescent loading persists into adulthood, 4 to 9 years after activity cessation.

100.

In a cross-sectional study of pre-pubertal girls, Courteix et al. reported a deficit in skull BMC for gymnasts relative to swimmers and non-gymnasts [17]. These authors suggested that the skull may be drained of BMC to supplement mineralization at loaded sites [2]. In our longitudinal data, such

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a phenomenon would be expected to appear as low gymnast BMC/aBMD during pre-menarcheal loading, with a rebound increase in skull aBMD or BMC after training cessation. We detected no significant skull BMC/aBMD activity group difference, with a contradictory trend toward decreasing gymnast skull BMC after gymnastic cessation (p<0.06), possibly reflecting a systemic bone metabolic shift. Our results corroborate those of Bass et al., who detected no difference in skull aBMD between pre-pubertal gymnasts and non-gymnasts, despite significant gymnast advantages at loaded sites [2]. We interpret all of the above as evidence for the role of mechanical loading in observed ex/gymnast advantages, weakening the argument that gymnast advantages are attributable to self-selection for robust bone.

101.

Go to: 102.

Limitations 103.

Although skull outcomes are subject to positional variation in pediatric subjects, this problem was likely alleviated by large numbers of repeated observations per subject. Because this study is not a randomized, controlled intervention, ex-gymnast skeletal benefits are correlational in nature. Further-more, ex-gymnast pre-exposure skeletal parameters are unknown, as subjects had been training for 2 to 8 years prior to the initial DXA scan. Although statistical power is bolstered by large numbers of repeated observations, subject numbers are small. In particular, due to the stringent inclusion criteria for maturation-specific timing of gymnastic exposure, few ex-gymnasts are represented. Our capacity to evaluate retention of benefits beyond 4 years post-menarche is limited by our relatively young cohort. Continued observation of our entire cohort will enhance power (more subjects) and provide a longer period to assess benefit retention (more data points beyond 4 years post-menarche), enabling future analyses of skeletal sites with lower theoretical loading contrasts and higher required sample sizes (e.g., hip, lumbar spine).

104.

Go to: 105.

Conclusion 106.

Gymnastic exposure during childhood and early puberty is associated with enhanced radius bone mass, size, and areal density. Despite evidence of brief de-training losses in density and mass, significant benefits appear to persist for at least 4 years beyond activity cessation and into early adulthood, corroborating results from previous retrospective studies.

107.

Go to: 108.

Acknowledgments 109.

This work was supported by funding from the Orthopedic Research and Education Foundation and from the National Institutes of Health

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(National Institute of Arthritis, Musculoskeletal and Skin Diseases: R03 AR047613, R01 AR054145). We would also like to acknowledge Cathy Riley, Christina Morganti, Moira Davenport, Nicole Gero, and Jill Kanaley, whose assistance in data collection, analysis, and other aspects of this research were instrumental in the success of this longitudinal project.

110.

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Footnotes 112.

Conflicts of interest None.

113.

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Contributor Information 115.

T. A. Scerpella, Department of Orthopedics and Rehabilitation, University of Wisconsin, 1685 Highland Avenue, 6th Floor, Madison, WI 53705-2281, USA. 116.

J. N. Dowthwaite, Department of Orthopedic Surgery, SUNY Upstate Medical University, Institute for Human Performance, 505 Irving Avenue, Syracuse, NY 13210, USA. 117.

P. F. Rosenbaum, Department of Public Health and Preventative Medicine, SUNY Upstate Medical University, Institute for Human Performance, 505 Irving Avenue, Syracuse, NY 13210, USA. 118.

Go to: 119.

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2. Bass S, Pearce G, Bradney M, Hendrich E, Delmas PD, Harding A, Seeman E. Exercise before puberty may confer residual benefits in bone density in adulthood: studies in active prepubertal and retired female gymnasts. J Bone Miner Res. 1998;13:500–507.[PubMed] 122.

3. Kirchner EM, Lewis RD, O‘Connor PJ. Effect of past gymnastics participation on adult bone mass. J Appl Physiol. 1996;80:226– 232.[PubMed] 123.

4. Kudlac J, Nichols DL, Sanborn CF, DiMarco NM. Impact of detraining on bone loss in former collegiate female gymnasts. Calcif Tissue Int. 2004;75:482–487.[PubMed] 124.

5. Scerpella TA, Dowthwaite JN, Gero NM, Kanaley JA, PloutzSnyder RJ. Skeletal benefits of pre-menarcheal gymnastics are retained after activity cessation. Pediatr Exerc Sci. 2010;22:21–33.[PubMed]

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125.

6. Eser P, Hill B, Ducher G, Bass S. Skeletal benefits after long-term retirement in former elite female gymnasts. J Bone Miner Res. 2009;24:1981–1988.[PubMed] 126.

7. Scerpella TA, Davenport M, Morganti CM, Kanaley JA, Johnson LM. Dose related association of impact activity and bone mineral density in pre-pubertal girls. Calcif Tissue Int. 2003;72:24–31.[PubMed] 127.

8. Liu X, Spybrook J, Congdon R, Martinez A, Raudenbush SW. [Accessed 31 August 2010];Optimal Design for Multi-level and Longitudinal Research. HLM Software. (Version 2.0). 2009 http://www.wtgrantfoundation.org/resources/overview/research_tools.

128.

9. Fuchs RK, Snow CM. Gains in hip bone mass from high-impact training are maintained: a randomized controlled trial in children. J Pediatr.

2002;141:357–362.[PubMed] 129.

10. Gunter K, Baxter-Jones AD, Mirwald RL, Almstedt H, Fuller A, Durski S, Snow C. Jump starting skeletal health: a 4-year longitudinal study assessing the effects of jumping on skeletal development in pre and circum pubertal children. Bone. 2008;42:710–718.[PubMed] 130.

11. Zanker CL, Gannon L, Cooke CB, Gee KL, Oldroyd B, Truscott JG. Differences in bone density, body composition, physical activity, and diet between child gymnasts and untrained children 7–8 years of age. J Bone Miner Res. 2003;18:1043–1050.[PubMed] 131.

12. Pollock NK, Laing EM, Modlesky CM, O‘Connor PJ, Lewis RD. Former college artistic gymnasts maintain higher BMD: a nine-year followup. Osteoporos Int. 2006;17:1691–1697.[PubMed] 132.

13. Dowthwaite JN, Flowers PP, Spadaro JA, Scerpella TA. Bone geometry, density, and strength indices of the distal radius reflect loading via childhood gymnastic activity. J Clin Densitom. 2007;10:65–75. [PMC free article][PubMed] 133.

14. Dowthwaite JN, Scerpella TA. Distal radius geometry and skeletal strength indices after peri-pubertal artistic gymnastics. Osteoporos Int. 2010 (in press) 134.

15. Dyson K, Blimkie CJ, Davison KS, Webber CE, Adachi JD. Gymnastic training and bone density in pre-adolescent females. Med Sci Sports Exerc. 1997;29:443–450.[PubMed] 135.

16. Ward KA, Roberts SA, Adams JE, Mughal MZ. Bone geometry and density in the skeleton of pre-pubertal gymnasts and school children.

Bone. 2005;36:1012–1018.[PubMed] 136.

17. Courteix D, Lespessailles E, Obert P, Benhamou CL. Skull bone mass deficit in prepubertal highly-trained gymnast girls. Int J Sports Med. 1999;20:328–333.[PubMed]

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Differential effects of strength versus power training on bone mineral density in postmenopausal women: a 2‐year longitudinal study

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Simon von Stengel, Wolfgang Kemmler, Dirk Lauber, Willi A Kalender, and Klaus Engelke Author information ► Article notes ► Copyright and License information ► This article has been corrected. See Br J Sports Med. 2007 December; 41(12): 926.

This article has been cited by other articles in PMC. Go to: Abstract Objectives To investigate the effect of two different schemes of loading in resistance training on bone mineral density (BMD) and pain in pretrained postmenopausal women.

Methods 53 pretrained women (mean (SD) age 58.2 (3.7) years) who carried out a mixed resistance and gymnastics programme were randomly assigned to a strength training (ST) or power training (PT) group. The difference between the two groups was the movement velocity during the resistance training (ST, 4 s (concentric)/4 s (eccentric); PT, explosive/4 s). Otherwise both groups carried out periodised progressive resistance training (10–12 exercises, 2–4 sets, 4–12 repetitions at 70– 92.5% of the one‐repetition maximum (2/week) for 2 years. Mechanical loading was determined with a force measuring plate during the leg press exercise. At baseline and after 2 years, BMD was measured at different sites with dual x‐ray absorptiometry. Pain was assessed by questionnaire.

Results Loading magnitude, loading/unloading rate, loading amplitude and loading frequency differed significantly (p<0.001) between the two groups. After 2 years, significant between‐group differences were detected for BMD (PT, −0.3%; ST, −2.4%; p<0.05) and bone area (PT, 0.4%; ST, −0.9%; p<0.05) at the lumbar spine.

At the hip, there was a non‐significant trend in favour of the PT group. Also the incidence of pain indicators at the lumbar spine was more favourable in the PT group.

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Conclusion The results show that PT may be superior for maintaining BMD in postmenopausal women. Furthermore, PT was safe as it did not lead to increased injury or pain.

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Keywords: postmenopausal women, exercise, strength training, power training, bone mineral density Low bone mineral density (BMD) is a major risk factor for osteoporotic fracture.

Therefore prevention of age‐related bone loss is important, in particular, during the critical phase of the menopause. Recent meta‐analyses of exercise studies have confirmed the positive effect of physical exercise on BMD in postmenopausal women.1,2,3,4 It is doubtful, however, whether the most effective strategy to maintain or regain BMD has yet been found.

Results from cross‐sectional studies with athletes of different sports disciplines show that high‐impact load‐bearing activities such as sports competitions and gymnastics5,6,7,8 and activities associated with high muscular tension such as weightlifting7,9,10,11 are related to high BMD. For optimisation of exercise regimens, two main components have to be considered: the differential impact of the various mechanical stimuli on bone, and the differential generation of these stimuli by specific physical activities or exercises.

Strength is the capacity of muscle to generate force, and power is defined as the product of force and velocity. Thus power training (PT) is characterised by a high velocity of muscle shortening. The focus of this study is quantification of the mechanical loading characteristics of strength training (ST) versus PT, and investigation of the effect of these two training types on BMD in postmenopausal women. We hypothesise that a high movement velocity (PT) results in more pronounced stimulation than a low movement velocity (ST) by producing higher strain rates. On the basis of this hypothesis, we further assume that PT is more effective in maintaining BMD in postmenopausal women. As PT is characterised by explosive muscle contractions which produce higher stress on tendons and joints, it may have a higher risk of discomfort, pain and injury. Thus, we also determined the exercise‐related incidence of pain by analysing pain intensity and frequency at different skeletal sites. We here report the 2‐year results of a study in pretrained postmenopausal women. The first‐year results have been published elsewhere.12 Go to:

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Methods This study was approved by the ethics committee of the University of Erlangen (Ethik Antrag S21‐22112‐81‐00) and the German and Bavarian radiation safety agencies (Bundesamt für Strahlenschutz: Z2.1.2‐22462/2‐2002‐016).

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Subjects Fifty three osteopenic postmenopausal woman (mean (SD) age 58.2 (3.7) years; 4– 11 years post menopause) who had participated in the training arm of the EFOPS study for 3 years13 were group‐wise randomly assigned to an ST (n = 28) or PT (n = 25) programme. Before the beginning of the study, none of the subjects had any diseases or took any medication that affected bone metabolism.

Intervention programme Both groups carried out two supervised sessions of resistance training (60 min/week), one supervised session of gymnastics (60 min/week) and one non‐ supervised home training session (20 min/week). On the basis of calcium and vitamin D results from an individual nutritional analysis, participants received supplemental calcium and vitamin D to ensure a total daily intake of 1500 mg and 500 IE, respectively.

Weightlifting session Each resistance training session consisted of three sequences: 20 min warm‐up programme (low/high‐impact aerobic at 70–85% of maximum heart rate), short jumping sequence (4×15 multidirectional jumps), resistance sequence (40 min).14 In the high‐intensity, periodised weightlifting programme, all main muscle groups were trained on machines (Technogym, Gambettola, Italy). The following dynamic exercises were used: horizontal leg press, leg curls, bench press, rowing, leg adduction and abduction, abdominal flexion, back extension, lat pulley, hyperextension, leg extension, shoulder raises and hip flexion. A progressive, periodised design was used, which was characterised by 12‐week periods of high‐ intensity training (70–92.5% of the one‐repetition maximum (1RM)) interspersed with 4–5 weeks of lower training intensity (50% of 1RM) ensuring enough time for adaptation and regeneration.

The only difference between the ST and PT study arms was the velocity with which the exercises were carried out. In the ST mode, movements were performed in a 4 s (concentric)/4 s (eccentric) scheme. The subjects in the PT group were

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instructed to perform the concentric part ―as fast as possible‖, whereas the eccentric period was to be carried out slowly (4 s). In the home training and gymnastics sessions described next, there were no differences between ST and PT.

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Gymnastic session The purpose of the weekly gymnastic programme was to improve fall‐related abilities, in particular balance and coordination, strength, endurance and flexibility.

The session started with aerobics or games, followed by balance exercises. Further isometric and dynamic strength exercises for the trunk, shoulders and arms were performed, partly using elastic bands. At the end of the session, stretching exercises were carried out.

Home training session All participants were requested to carry out a 20 min home training session once a week. In this session, subjects received written instructions to perform selected strength and stretching exercises also carried out in the gymnastic session.

Measurements Characterisation of differential mechanical loading At 6 months into the study, when the subjects had become accustomed to the new training modality, reaction forces were evaluated in 16 members of the PT group and 18 members of the ST group with a force plate (mtd‐Systems, Neuburg v Wald, Germany) during the leg press procedure. Force–time curves were recorded over six repetitions carried out with loads corresponding to ~75% of 1RM. From these curves, loading magnitude, amplitude, frequency and maximum loading and unloading rates were extracted and compared between PT and ST groups.

The loading magnitude was defined as the mean of the six force maxima normalised by the lifted weight (fig 11).). Analogously the loading amplitude was calculated as the mean of the differences between the six maxima and minima normalised by lifted weight (fig 11).). The maximum loading and unloading rates (N/ms) were determined from the derivatives and calculated as mean rates of the six maxima or the six minima, respectively. Spectral loading characteristics were assessed by decomposing the force–time curves into sinusoidal components using fast Fourier transforms. The decomposition gave the dependence of force on frequency, the so‐called frequency spectrum of the force. For the statistical analysis, the frequency spectrum between 0 and 3 Hz, which is the range of

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relevant amplitudes, was divided into six intervals of 0.5 Hz each. Finally, a Fourier synthesis was performed to analyse the contribution of each 0.5 Hz interval to the original signal.

Figure 1 Characteristic force–time curves for strength training (A) and power training (B). The maxima and minima of each repetition are marked by small circles. Maximal loading and unloading rates are marked for each repetition by small (more ...)

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Bone densitometry BMD at the lumbar spine (L1–L4), the proximal femur (total hip and sub regions) and the forearm (distal forearm and ultradistal radius) were measured at baseline and after 1 year and 2 years by dual x‐ray absorptiometry (QDR 4500A; Hologic, Bedford, MA, USA) using standard protocols.

Pain Pain frequency and intensity at various skeletal sites (spine segments, big joints, small joints) were assessed at baseline and after 1 year and 2 years by a questionnaire described by Jensen et al15 and the Osteoporosis Quality of Life Study Group.16 Anthropometric data Weight and body composition was assessed using impedance scales (Tanita BF 305; Tanita, Tokyo, Japan).

Maximum strength Maximum isometric strength of the trunk extensors and flexors was determined using a Schnell M‐3 dynamometer (Schnell, Peutenhausen, Germany). Maximal dynamic muscle strength of the legs (leg press) and the chest (seated bench press) was determined at the training machines using 1RM tests.

Nutritional data Individual dietary intakes were assessed from a 5‐day diary analysed using Prodi‐ 4,5/03 Expert software (Wissenschaftlicher Verlag, Freiburg, Germany).

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Statistical analysis

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The Kolgomorov–Smirnov test was used to check for normal distribution.

Homogeneity of variance was determined using the Levine F‐test. Student t tests were used to compare the baseline characteristics of the two groups. Changes between baseline and follow‐up within the groups were analysed by paired t tests.

Within‐group changes were calculated as percentage changes; unpaired t tests were used to compare these differences in the two groups. For variables that were not normally distributed, Wilcoxon or Whitney‐Mann U tests were applied instead of t tests. Because of the multiple test problem, we also performed a two‐way analysis of variance with repeated measures. The type of resistance training (PT versus ST) was used as between‐group factor, and the time between baseline and follow‐up visit was used as within‐group factor. The results of the two statistical methods were identical. All tests were two‐tailed, and a 5% probability level was considered significant. We used SPSS V.12.0 (SPSS Inc, Chicago, Illinois, USA) for statistical analysis. The fast Fourier transformation and spectral analysis of the force–time curves were carried out in Excel 2003 (Microsoft Corp).

Go to: Results At baseline, 53 women were included in the study. Five subjects dropped out during the 2 years of intervention for personal reasons. Another two subjects were excluded from the data analysis because they had developed a disease that affected bone metabolism. Thus 24 women from the ST group and 22 women from the PT group were included in the analysis.

The attendance rate was similar in the two groups: 2.2 (0.4) sessions per week in the ST group and 2.3 (0.5) sessions in the PT group. Table 11 shows anthropometric and nutritional baseline data for both groups, and table 22 compares osteodensitometric and muscle‐strength variables at baseline. Except for leg press values (p<0.05), no significant group differences were detected.

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Table 1 Anthropometric and nutritional data at baseline for subjects in the strength training (ST) and power training (PT) groups

Table 2 Osteodensitometric and maximum muscle‐strength variables at baseline for subjects in the strength training (ST) and power training (PT) groups Mechanical loading of power and strength training Figure 11 shows two characteristic force–time curves, one for a subject in the ST group (A) and one in the PT group (B). As a consequence of the explosive muscle contraction, the curves are quite different, with higher maxima and minima and higher frequencies in the PT group. Compared with the ST group, the PT group showed a 16% higher relative loading magnitude, a 82% higher relative loading amplitude, and 262% (612%) higher loading (unloading) rate. All differences were highly significant (p<0.001).

Figure 22 shows the results of the frequency analysis. It can be seen that in the ST group the 0–0.5 frequency range accounts for most of the original signal (74%), whereas in the PT group there are high amplitudes from 0 to 2.5 Hz. In the PT group, frequencies greater than 1 Hz account for 77% of the signal compared with 14% in the ST group. The differences between the groups were highly significant for all variables (p<0.001).

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Figure 2 Contribution of the six 0.5 Hz frequency intervals to the total signal in the strength training (ST) and power training (PT) group. Values are mean (SD).

Significant between‐group differences are marked with asterisks. (more ...)

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Osteodensitometry Figure 33 illustrates the results of the osteodensitometric measurements as percentage changes between baseline and year 2 for BMD and area. Figure 3A3A shows the results for the lumbar spine (L1–L4). Whereas the ST group lost BMD and area significantly, there were no differences in the PT group. Between‐group differences were significant for both variables. Figure 3B3B shows the corresponding results for the total hip, femoral neck and trochanter. The ST group significantly lost BMD at the total hip and femoral neck. However, between‐group differences were not significant. At the forearm (fig 3C3C)) no changes were observed at all.

Figure 3 Percentage changes in bone mineral density (BMD), measured by dual x‐ray absorptiometry, between baseline and year 2 at (A) the lumbar spine (L1– L4), (B) the proximal femur and (C) the forearm in the strength training (more ...)

Pain and injuries Figure 44 gives results for pain frequency and intensity in the lower back and big joints (hip, knee, shoulder). These regions in particular were loaded during our resistance training regimen. In the ST group, a significant increase in pain intensity at the lumbar spine was observed, whereas a slight non‐significant decrease was found in the PT group. This resulted in a significant between‐group difference for pain intensity in the lumbar spine. At the spine, similar but insignificant results were found for pain frequency. For the big joints, a significant decrease in pain frequency was even observed in the PT group. No significant within‐group or

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between‐group differences could be detected for pain in the small joints or the thoracic or cervical spine.

Figure 4 Pain frequency (A) and pain intensity (B) at baseline and year 2 at the lumbar spine and big joints in the strength training (ST) and power training (PT) group. Values are mean (SD). Significant within‐group changes are marked (more ...)

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Discussion In our 2‐year exercise study in postmenopausal woman, we determined the differential effects of PT versus ST. The first aim was of a technical nature: to show that a difference in training velocities translated into differential effects of the mechanical loading stimuli. The main hypothesis was based on the assumption that different mechanical stimuli result in differences in BMD in our groups of postmenopausal women.

We found a significant impact of the training scheme on the loading stimuli varying from 16% to 611% between the PT and ST group. The effect on loading magnitude was lowest; the effect on loading and unloading rate was highest.

However, these results do not answer the question whether loading parameters determined by measuring external reaction forces can be used to estimate internal loading and strain of bones. There is not much literature on this topic. Bassey et al17 simultaneously determined ground reaction and internal forces at the proximal femur via an instrumented hip implant during different activities (walking, jumping, jogging). They found that the ground reaction forces were significantly related to the internal peak force and the internal force rate. As the bone strain is directly proportional to the applied force,18 we conclude that the external reaction forces can be used to estimate the internal forces and the resulting bone strains of loaded bones.

There are very few human studies that have quantified the effect of specific mechanical stimuli on bone. The studies that do exist almost exclusively focus on loading magnitude and investigate the effect of low versus high intensity resistance training.19,20,21,22,23,24 One study showed that high‐impact (jumping) exercises were significantly more efficient in positively affecting BMD than low‐impact exercises but did not quantify the loading rate.19 To our knowledge, the present study is the

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first longitudinal human study that quantifies the mechanical loading of different training strategies in combination with analysis of the BMD.

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In contrast with human studies, numerous published animal studies have investigated the influence of mechanical stimuli on bone. Their results are very useful in the discussion of the outcome of our study. The isolated effect of strain magnitude was analysed in two studies using the isolated avian ulna model.25,26 In accordance with the mechanostat theory,27 at a threshold of about 1000 με, bone formation was enhanced and the newly formed bone increased approximately linearly with strain magnitude.

The isolated influence of the strain rate is addressed in several publications. All show that a higher strain rate is associated with a higher adaptive bone response.28,29,30 Two studies compared the mechanical loading characteristics of walking, running (low‐impact exercises) and drop jumps (high‐impact exercises) at the tarsometatarsus of roosters.31,32 Compared with walking and running, drop jumps produce only moderately higher strain magnitudes (+30% and +11%, respectively) but much higher strain rates (+740% and +256%, respectively). In contrast with treadmill running, drop jumps increased bone formation significantly.

These results emphasise the importance of strain rate. Another study using the rat ulna loading model shows that loading and unloading rates are of equal importance for stimulating bone formation.33 What is already known on this topic   

Physical activity and sport positively influence bone mineral density (BMD).

High‐impact load‐bearing exercises and high‐intensity strength training are more effective than endurance and low‐impact/intensity training.

Bone is sensitive to several mechanical loading variables such as loading magnitude, rate and frequency. However, in vivo, their differential effects on bone are not fully understood.

What this study adds 



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This study investigates the effect of the movement velocity during weightlifting training on mechanical loading variables and compares the effects of strength and power training on BMD. Higher movement velocity, in particular, results in higher loading rates and is more effective at the lumbar spine but not at the hip.

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The isolated assessment of mechanical stimuli is not easy, and studies must be interpreted carefully. For example, in the study of Turner et al30 mentioned above, the loading rate was increased by raising the loading amplitude (0, 18, 36, 54 N) of a sinusoidal loading at constant loading magnitude (54 N). In other words, there was not complete unloading. The enhanced bone formation may be attributed to a combination of higher strain rates and higher strain amplitudes. There is some speculation that there may be an important role for strain amplitude in increasing fluid flow, which some researchers suggest is a key stimulus of mechanotransduction.34 The fourth stimulus investigated in our study was loading frequency. Most animal studies have shown an increase in bone formation rate with increasing frequency.35,36,37 However, most used much higher frequencies (10–50 Hz) than those that result from exercise, which are predominantly in a range up to 3–4 Hz (fig 22).). Thus the results of these animal studies are more relevant for the construction of vibration platforms.38,39,40,41 However, one animal study used loading frequencies between 0.2 and 2.0 Hz.37 It showed that higher frequencies were associated with higher osteogenic response.

In summary, all these studies indicate that PT should be more effective than ST in stimulating the mechanosensitive bone cells and in inducing bone adaptation, be it through the pathways of higher loading magnitude or amplitude, higher loading and unloading rate, higher frequency, or a combination of these factors. Overall, our study results confirm this conclusion. After 2 years, there was a significant BMD loss at the spine in the ST group versus no loss in the PT group, and in the proximal femur there was a trend of a greater BMD loss in the ST group compared with the PT group. Between‐group differences reached significance at the lumbar spine.

Unfortunately, we did not use more sophisticated techniques to investigate BMD or bone structure changes such as quantitative CT or high‐resolution MRI. Thus, for example, differential effects on cortical and trabecular bone could not be investigated. Interestingly, the 2‐year results were slightly different from the 1‐year data12 in significant between‐group differences at the lumbar spine and total hip.

After 1 year, total hip BMD in the PT group was constant (0.0 (1.7)%, NS); after 2 years, we found a small decrease of −0.8 (1.3)% that was still not significant. In contrast, the decrease in the ST group was similar in both years (year 1, −1.2 (1.5)%, p<0.01; year 2, −1.3 (2.5)%). A cautious, although not statistically proven, interpretation of our results might conclude that the superior effect of the PT in the first year was eroded in the second year. This is suggested by the fact that, in the

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spine area in the PT group, a slight BMD increase (+0.7 (2.1)%, NS) after year 1 turned into a small decrease (−0.4 (2.2)%) in the second year. Again the use of more advanced techniques such as quantitative CT may be preferable to dual x‐ray absorptiometry to clarify this questions.

This may indicate habituation effects, also observed by other authors,22,42,43,44 and support the model of Schriefer et al45, according to which bone adapts mainly to changes in its mechanical environment based on the principle of cellular accommodation. All women that participated in our study had previously exercised in the EFOPS programme. Compared with ST, PT was an unaccustomed stimulus and therefore initially was more effective at maintaining BMD. In the second year, the women had become accustomed to the new training stimulus and PT lost its superiority. However, as this possible interpretation of our results is not backed by hard statistical evidence, we will not discuss it further.

There are very few intervention studies using PT in older people,46,47,48,49,50,51,52,53,54,55 and this may be one reason why the overall benefits of PT in this age group are controversial. Obviously, PT results in greater stress on muscles, tendons and joints and may thus imply a higher risk of injuries. Thus older people are generally advised to perform weightlifting exercises with low movement velocity.56 In our study, there was no increased incidence of injury or pain associated with the high movement velocity. We attribute this to the fact that our subjects were pretrained and well adapted to high‐intensity resistance at the study start. In the preceding EFOPS training, the subjects performed a progressive weightlifting programme over a period of 3 years. We further attribute these results to the periodised design, characterised by 12‐week periods of high‐intensity training (70– 92.5% of 1RM) interspersed by 4–5 weeks of lower training intensity (50% of 1RM) ensuring enough time for adaptation and regeneration. However, we admit that, to date, little is known about the long‐term effects of PT in older subjects, and consequently it is too early to generalise PT recommendations for this group.

In summary, this study shows that, at least at the spine, PT was superior to ST with respect to increasing BMD, and therefore may have greater potential for preventing osteoporosis. It can be assumed that, for healthy older people who can tolerate high‐intensity training, a resistance programme with PT may not only benefit bone but also be beneficial in improving physical function and enhancing everyday functional abilities.49,51,57,58,59,60 Our results suggest that there should be no increase in pain and injury if sufficient slow adaptation to this strenuous training is allowed.

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Go to: Acknowledgements

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This work was supported by the state of Bavaria (Gesetz zur Förderung des wissenschaftlichen und künstlerischen Nachwuchses vom 18.12.1984). We further gratefully acknowledge support from Sanofi Synthelabo (Paris, France), who supplied calcium and vitamin D supplements, and mtd‐Systems (Neuburg v. Wald, Germany), who supplied the force plates. We thank Manfred von Stengel for helpful discussions on the analysis of the force–time curves.

Go to: Abbreviations 1RM - one‐repetition maximum BMD - bone mineral density PT - power training ST - strength training Go to: Footnotes Competing interests: None.

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567–77.77.

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3. Wallace B A, Cumming R G. Systematic review of randomized trials of the effect of exercise on bone mass in pre‐ and postmenopausal women. Calcif Tissue Int 2000. 6710–18.18. [PubMed] 4. Wolff I, van Croonenborg J J, Kemper H C. et al The effect of exercise training programs on bone mass: a meta‐analysis of published controlled trials in pre‐ and postmenopausal women. Osteoporos Int 1999. 91–12.12. [PubMed] 5. Fehling P C, Alekel L, Clasey J. et al A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone 1995.

17205–210.210. [PubMed] 6. Lee E J, Long K A, Risser W L. et al Variations in bone status of contralateral and regional sites in young athletic women. Med Sci Sports Exerc 1995. 271354– 1361.1361. [PubMed] 7. Morel J, Combe B, Francisco J. et al Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int 2001. 12152– 157.157. [PubMed] 8. Risser W L, Lee E J, LeBlanc A. et al Bone density in eumenorrheic female college athletes. Med Sci Sports Exerc 1990. 22570–574.574. [PubMed] 9. Heinonen A, Oja P, Kannus P. et al Bone mineral density of female athletes in different sports. Bone Miner 1993. 231–14.14. [PubMed] 10. Heinrich C H, Going S B, Pamenter R W. et al Bone mineral content of cyclically menstruating female resistance and endurance trained athletes. Med Sci Sports Exerc 1990. 22558–563.563. [PubMed] 11. Nilsson B E, Westlin N E. Bone density in athletes. Clin Orthop 1971. 77179– 182.182. [PubMed] 12. von Stengel S, Kemmler W, Engelke K. et al Power training is more effective for maintaining bone mineral density in postenopausal women. J Appl Physiol 2005. 99181–188.188. [PubMed] 13. Engelke K, Kemmler W, Lauber D. et al Exercise maintains bone density at spine and hip EFOPS: a 3‐year longitudinal study in early post‐menopausal women. Osteoporos Int 2006. 17133–142.142. [PubMed] 14. Kemmler W, Engelke K, Lauber D. et al Exercise effects on fitness and BMD in early postmenopausal women: 1 year EFOPS results. Med Sci Sports Exerc 2002. 342115–2123.2123. [PubMed] 15. Jensen M P, Karoly P, Braver S. The measurement of clinical intensity: a comparison of six methods. Pain 1986. 27117–126.126. [PubMed] 16. Investigators Measuring quality of life in women with osteoporosis. The Osteoporosis Quality of Life Study Group. Osteoporos Int 1997. 7478–487.487.

[PubMed] 17. Bassey E J, Littlewood J J, Taylor S J. Relations between compressive axial forces in an instrumented massive femoral implant, ground reaction forces, and

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integrated electromyog‐raphs from vastus lateralis during various ‗osteogenic' exercises. J Biomech 1997. 30213–223.223. [PubMed] 18. Jiang Y, Zhao J, Rosen C. et al Perspectives on bone mechanical properties and adaptive response to mechanical challenge. J Clin Densitom 1999. 2423–433.433.

[PubMed] 19. Bassey E J, Ramsdale S J. Increase in femoral bone density in young women following high‐impact exercise. Osteoporos Int 1994. 472–75.75. [PubMed] 20. Bemben D A, Fetters N L, Bemben M G. et al Musculoskeletal responses to high‐ and low‐intensity resistance training in early postmenopausal women. Med Sci Sports Exerc 2000. 321949–1957.1957. [PubMed] 21. Kerr D, Morton A, Dick I. et al Exercise effects on bone mass in postmenopausal women are site‐specific and load‐dependent. J Bone Miner Res 1996. 11218–225.225. [PubMed] 22. Kerr D, Ackland T, Maslen B. et al Resistance training over 2 years increases bone mass in calcium‐replete postmenopausal women. J Bone Miner Res 2001.

16175–181.181. [PubMed] 23. Maddalozzo G F, Snow C M. High intensity resistance training: effects on bone in older men and women. Calcif Tissue Int 2000. 66399–404.404. [PubMed] 24. Vincent K R, Braith R W. Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc 2002. 3417–23.23. [PubMed] 25. Rubin C T, Lanyon L E. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int 1985. 37411–417.417. [PubMed] 26. Turner C H, Forwood M R, Rho J Y. et al Mechanical loading thresholds for lamellar and woven bone formation. J Bone Miner Res 1994. 987–97.97.

[PubMed] 27. Frost H M. Bone mass and the mechanostat. A proposal. Anat Rec 1987. 2191– 19.19. [PubMed] 28. Mosley J R, Lanyon L E. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone 1998. 23313–318.318. [PubMed] 29. O'Connor J A, Lanyon L E, MacFie H. The influence of strain rate on adaptive bone remodelling. J Biomech 1982. 15767–781.781. [PubMed] 30. Turner C H, Owan I, Takano Y. Mechanotransduction in bone: role of strain rate. Am J Physiol Endocrinol Metab 1995. 269E438–E442.E442.

31. Judex S, Zernicke R F. High‐impact exercise and growing bone: relation between high strain rates and enhanced bone formation. J Appl Physiol 2000.

882183–2191.2191. [PubMed] 32. Judex S, Zernicke R F. Does the mechanical milieu associated with high‐speed running lead to adaptive changes in diaphyseal growing bone? Bone 2000. 26153– 159.159. [PubMed]

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33. Skerry T M., Peet Nm ―Unloading‖ exercises increases bone formation in rats.

J Bone Miner Res 1997. 121520.

34. Weinbaum S, Cowin S C, Zeng Y. A model for the excitation of osteocytes by me‐chanical loading‐induced bone fluid shear stresses. J Biomech 1994. 27339– 360.360. [PubMed] 35. Hsieh Y F, Turner C H. Effects of loading frequency on mechanically induced bone formation. J Bone Miner Res 2001. 16918–924.924. [PubMed] 36. Rubin C T, McLeod K J. Promotion of bony ingrowth by frequency specific, low‐amplitude mechanical strain. Clin Orthop 1994. 298165–174.174. [PubMed] 37. Turner C H, Forwood M R, Otter M W. Mechanotransduction in bone: do bone cells act as sensors of fluid flow? FASEB J 1994. 8875–878.878. [PubMed] 38. LaMothe J M, Zernicke R F. Rest insertion combined with high‐frequency loading enhances osteogenesis. J Appl Physiol 2004. 961788–1793.1793.

[PubMed] 39. Rubin C, Turner A S, Mallinckrodt C. et al Mechanical strain, induced noninvasively in the high‐frequency domain, is anabolic to cancellous bone, but not cortical bone. Bone 2002. 30445–452.452. [PubMed] 40. Rubin C, Xu G, Judex S. The anabolic activity of bone tissue, suppressed by disuse, is normalized by brief exposure to extremely low‐magnitude mechanical stimuli. FASEB J 2001. 152225–2229.2229. [PubMed] 41. Warden S J, Turner C H. Mechanotransduction in the cortical bone is most efficient at loading frequencies of 5–10 Hz. Bone 2004. 34261–270.270. [PubMed] 42. Heikkinen J, Kyllonen E, Kurttila‐Matero E. et al HRT and exercise: effects on bone density, muscle strength and lipid metabolism. A placebo controlled 2‐year prospective trial on two estrogen‐progestin regimens in healthy postmenopausal women. Maturitas 1997. 26139–149.149. [PubMed] 43. Iwamoto J, Takeda T, Ichimura S. Effects of exercise training and detraining on bone mineral density in postmenopausal women with osteoporosis. J Orthop Sci 2001. 6128–132.132. [PubMed] 44. Prince R L, Devine A, Dick I. et al The effect of calcium supplementation (milk powder or tablets) and exercise on bone density in postmenopausal women. J Bone Miner Res 1995. 101068–1075.1075. [PubMed] 45. Schriefer J L, Warden S J, Saxon L K. et al Cellular accommodation and the response of bone to mechanical loading. J Biomech 2005. 381838–1845.1845.

[PubMed] 46. Bean J F, Herman S, Kiely D K. et al Increased Velocity Exercise Specific to Task (InVEST) training: a pilot study exploring effects on leg power, balance, and mobility in community‐dwelling older women. J Am Geriatr Soc 2004. 52799– 804.804. [PubMed]

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47. Earles D R, Judge J O, Gunnarsson O T. Velocity training induces power‐ specific adap‐tations in highly functioning older adults. Arch Phys Med Rehabil 2001. 82872–878.878. [PubMed] 48. Fielding R A, LeBrasseur N K, Cuoco A. et al High‐velocity resistance training increases skeletal muscle peak power in older women. J Am Geriatr Soc 2002.

50655–662.662. [PubMed] 49. Foldvari M, Clark M, Laviolette L C. et al Association of muscle power with functional status in community‐dwelling elderly women. J Gerontol A Biol Sci Med Sci 2000. 55M192–M199.M199. [PubMed] 50. Hakkinen K, Kraemer W J, Newton R U. et al Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle‐aged and older men and women. Acta Physiol Scand 2001. 17151–62.62. [PubMed] 51. Henwood T R, Taaffe D R. Improved physical performance in older adults undertaking a short‐term programme of high‐velocity resistance training.

Gerontology 2005. 51108–115.115. [PubMed] 52. Miszko T A, Cress M E, Slade J M. et al Effect of strength and power training on physical function in community‐dwelling older adults. J Gerontol A Biol Sci Med Sci 2003. 58171–175.175. [PubMed] 53. Orr R, de Vos N J, Singh N A. et al Power training improves balance in healthy older adults. J Gerontol A Biol Sci Med Sci 2006. 6178–85.85. [PubMed] 54. Sayers S P, Bean J, Cuoco A. et al Changes in function and disability after resistance training: does velocity matter? A pilot study. Am J Phys Med Rehabil 2003. 82605–613.613. [PubMed] 55. de Vos N J, Singh N A, Ross D A. et al Optimal load for increasing muscle power during explosive resistance training in older adults. J Gerontol A Biol Sci Med Sci 2005. 60638–647.647. [PubMed] 56. Evans W J. Exercise training guidelines for the elderly. Med Sci Sports Exerc 1999. 3112–17.17. [PubMed] 57. Bassey E J, Fiatarone M A, O'Neill E F. et al Leg extensor power and functional performance in very old men and women. Clin Sci (Lond) 1992. 82321– 327.327. [PubMed] 58. Skelton D A, Greig C A, Davies J M. et al Strength, power and related functional ability of healthy people aged 65–89 years. Age Ageing 1994. 23371– 377.377. [PubMed] 59. Suzuki T, Bean J F, Fielding R A. Muscle power of the ankle flexors predicts functional performance in community‐dwelling older women. J Am Geriatr Soc 2001. 491161–1167.1167. [PubMed]

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60. Rantanen T, Avela J. Leg extension power and walking speed in very old people living independently. J Gerontol A Biol Sci Med Sci 1997. 52M225– M231.M231. [PubMed] Isokinetic Scapular Muscle Performance in Young Elite Gymnasts

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Ann M Cools, PhD, PT, Ellen Geerooms, PT, Dorien F. M Van den Berghe, PT, Dirk C Cambier, PhD, PT, and Erik E Witvrouw, PhD, PT Author information ► Copyright and License information ► This article has been cited by other articles in PMC. Go to: Abstract Context: During gymnastic exercises, considerable force output is required in the shoulder girdle muscles. Isokinetic performance of the scapular muscles in young, elite gymnasts has not been examined.

Objective: To compare the isokinetic muscle performance of the scapular muscles between elite adolescent gymnasts and nonathletic adolescents to identify differences in strength, endurance, and muscle balance based on high-level sport participation.

Design: Single-session, repeated-measures design.

Setting: University human research laboratory.

Patients or Other Participants: Sixteen young, elite gymnasts and 26 age-matched nonathletic subjects participated in the study.

Intervention(s): Linear protraction-retraction movement in the scapular plane at 2 velocities (12.2 cm/s and 36.6 cm/s).

Main Outcome Measure(s): Isokinetic strength and endurance values, peak force/body mass, work/body mass, fatigue index (difference between the work performed in the first third and the last third of the test), and protraction to retraction strength ratios.

Results: Elite gymnasts demonstrated higher values for the protraction peak force/body mass than the control group demonstrated (P < .05), and they demonstrated higher protraction to retraction ratios on the nondominant side than

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on the dominant side (P < .05 at low velocity, P < .001 at high velocity).

Work/body mass and fatigue index values were not statistically different between the groups. Side differences (P = .003) for retraction strength with lower protraction to retraction ratios (P < .001) were apparent in the gymnast group on the dominant side.

Conclusions: Scapular muscle performance in elite, young gymnasts is characterized by increased protraction strength and altered muscular balance around the scapula compared with nonathletic adolescents.

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Keywords: scapulothoracic joint, scapular muscle balance Key Points 



Compared with nonathletic adolescents, elite adolescent gymnasts demonstrated increased protraction strength and altered muscle balance around the scapula.

Adaptations in the scapular muscles may influence the quality of gymnastic performance and the risk for overuse injuries in other body parts.

The scapula plays a vital role in upper extremity function. The quality of movement depends upon the interaction between scapular and glenohumeral kinematics, especially in overhead sports where the demands on the shoulder are extremely high.1 Recently, researchers1,2 have described the function of the scapulothoracic joint in overhead movements as an important link in the sportspecific kinetic chain in which the scapula functions. The kinetic chain principle describes how the human body can be considered as a series of interrelated links or segments. Movement of 1 segment affects segments proximally and distally.2 With respect to the kinetic chain, power, velocity, and accuracy of the throwing or smashing movement depend upon the quality of movement and stabilization of each link. For instance, during the throwing movement, the final outcome is the result of forces generated from the ground-reaction forces that come from the contralateral lower limb and are transferred in a diagonal pattern through the trunk into the throwing arm. Optimal positioning of every segment within the chain and functional muscle activation patterns from proximal to distal are the key premises in this transfer of energy.2 Gymnasts are a group of athletes who use their arms extensively during their sport activity.3,4 However, the starting and ending points of the kinetic chain in these athletes substantially differ from those of throwers. Hence, the relative role of the links in the chain, including muscle activation patterns, is likely different. Indeed, a

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unique aspect of gymnastics is the regular use of the upper extremities to support body mass.5 Contrary to overhead throwing athletes who use their arms in an open kinetic chain, gymnasts use their upper extremities very often in closed kinetic chain activities with the hand supported on a floor, balance beam, or pommel horse. The additional task of weight bearing requires supplementary strength of the arm muscles and stability of all contributing joints.3–5 Strong scapular muscles are among the major prerequisites for optimal stability and functional movement of the scapulothoracic joint.1,6,7 Several investigators have studied scapular muscle adaptations in healthy overhead athletes who are involved in overhead sports, such as baseball8 or volleyball,9,10 that involve the primary use of their dominant arm. However, few investigators have examined scapular muscle performance in overhead athletes with bilateral use of their arms during their sports. Muscle strength of the scapular muscles and scapular position have been investigated only in swimming athletes.11–13 Recently, Cools et al14 developed an isokinetic protocol for the measurement of scapulothoracic protraction and retraction muscle strength. Normal nonathletic subjects and overhead athletes have been evaluated with this procedure.9,14,15 Scapular muscle adaptations in young gymnasts, however, have not been examined. Therefore, the purpose of our study was to compare the isokinetic muscle performance of the scapular muscles between elite adolescent gymnasts and nonathletic adolescents to identify differences in strength, endurance, and muscle balance based on high-level sport participation.

Go to: METHODS Subjects Sixteen young, elite gymnasts (3 males, 13 females) were recruited to participate in our study. They had a mean age of 12.8 ± 1.8 years (range, 11–17 years), mean height of 146.7 ± 12.7 cm (range, 135–176 cm), and mean mass of 37.1 ± 1.2 kg (range, 26–64 kg). Subjects were all members of the Sports School at the time of the investigation and had a mean training intensity of 30.25 ± 1.2 h/wk (range = 28–34 h/wk). Seven athletes participated in sport acrobatics, and 9 athletes were artistic gymnasts. Subjects were excluded from the study if they were unable to attend the normal training regimen because of upper extremity pain or injury.

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Twenty-six age-matched nonathletic adolescents (3 males, 23 females) served as a control group. This group had a mean age of 13.5 ± 1.6 years (range, 11–17), mean height of 161.6 ± 8.2 cm (range, 148–175 cm), and mean mass of 48.3 ± 8.8 kg (range, 32–60 kg). Exclusion criteria for the control group were upper limb or cervical spine injuries within the year before the study and participation in overhead sports for more than 2 h/wk.

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All subjects completed questionnaires regarding their training and athletic activities and their injury history. All subjects and their legal guardians gave their written informed consent to participate in this study. The study was approved by the ethical committee of Ghent University.

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Testing Procedures We followed the testing procedures used in a previous study.9 All isokinetic tests were performed using an isokinetic dynamometer (Biodex System 3; Biodex Medical Systems, Inc, Shirley, NY). The testing session started with a warm-up procedure consisting of shoulder movements in all directions, push-up exercises against the wall, and stretching exercises for the rotator cuff and scapular muscles.

The dominant side was tested first in both groups. We determined arm dominance by identifying the arm that the subject used to throw a ball.16 For the testing procedure, the closed chain attachment was fixed to the isokinetic dynamometer in a horizontal position. The handgrip was inserted into the attachment-receiving tube with the neutral handle facing up to keep the glenohumeral joint in a neutral rotational position. The chair was rotated to 15°, and the dynamometer was rotated to 45° in the opposite direction (Figure). Each subject was assessed in the seated position with the arm horizontal in the scapular plane (30° anterior to the frontal plane). We stabilized the trunk by placing a strap diagonally from the contralateral shoulder across the chest and securing it with a buckle. Each participant was subjected to 3 isokinetic tests: low velocity, high velocity, and endurance. The first test involved a linear speed of 12.2 cm/s (5 repetitions at an angular velocity of 60°/s); the second, 36.6 cm/s (5 repetitions at an angular velocity of 180°/s); and the third, 36.6 cm/s (40 repetitions at an angular velocity of 180°/s). The resting period between tests was 10 seconds. Experimental procedures were modified from a previously published protocol14 consisting of the first 2 tests that we used. In the protocol,14 the test-retest reproducibility of this procedure was found to be good to excellent for the peak force values (intraclass correlation coefficient = 0.88–0.96). In our investigation, we added a third test comprising 40 repetitions at a linear speed of 36.6 cm/s to evaluate endurance and

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fatigue variables. The number of repetitions and the selected velocity were based on research regarding isokinetic endurance and fatigue analysis.17–20

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Experimental setup for the isokinetic protraction-retraction movement in the scapular plane using a Biodex isokinetic dynamometer.9.

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To assess range of motion, we asked the subjects to perform a maximal protraction and a maximal retraction movement. Gravity correction was not performed because the movement occurred in a horizontal plane. The test started in a maximal retracted position, and the subjects were instructed to perform maximal protraction and retraction movements over the total range of motion. They also were instructed to keep their elbows extended during the test. All movements were performed in the concentric-concentric mode, which means that protraction and retraction movements were performed with concentric muscle activity. Subjects performed 5 familiarization trials before data collection, and verbal encouragement was given during testing. Visual feedback from the computer screen was not allowed.

Statistical Analysis After data collection, we used Biodex software (Biodex Medical Systems) to determine peak force (N), work (J), and work fatigue (%). To select dependent variables for further analysis, we used independent t tests with the α set at .05 to analyze group differences with respect to anthropometric characteristics. Results showed no significant age differences between groups (t40 = 1.377, P = .176); however, significant height (t40 = 4.633, P < .001) and mass (t40 = 3.758, P < .001) differences existed between the gymnasts and the controls. Therefore, absolute strength data were normalized as a percentage of body mass. Peak force/body mass (N/kg × 100) and work/body mass (J/kg × 100) during protraction and retraction measured at 2 velocities (12.2 and 36.6 cm/s) were selected as dependent variables for statistical analysis. In addition, protraction to retraction ratios were calculated for both velocities based on the peak-force data. Finally, from the last test (40 repetitions), fatigue index was taken into account for further interpretation. This is a ratio of the difference between the work performed during the first third and the last third of the test bout. Positive values (%) represent a decline in work, and

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negative values mean that the work in the last third is increased compared with the first third.

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Because all data were distributed normally with equal variances, we used parametric tests for statistical analysis. A general linear model 2-way analysis of variance (ANOVA) with repeated-measures design was used for statistical analysis in which the within-subjects factor was side (2 levels) and the between-subjects factor was group (2 levels). Interaction effects of group and side, as well as main group effects, were of interest. In the presence of an interaction effect, group differences and side differences were tested post hoc at each level of the interacting variable using a Bonferroni adjustment. In the absence of interactions, main effects of group were analyzed. The α was set at .05. For each of the multiple pairwise comparisons, the Bonferroni adjustment was used with the α set at .025. All statistical analyses were performed with SPSS (version 12.0; SPSS Inc, Chicago, IL). Power analysis of the strength values was calculated at more than 80%.

Computations regarding effect size were based on the results from a previous study on healthy adult subjects.14 Go to: RESULTS Peak Force/Body Mass Table 1 summarizes the descriptive data and the results from the post hoc Bonferroni adjustments for peak force/body mass for both groups, both sides, both testing velocities, and both movement directions. The general linear model 2-way ANOVA with repeated-measures design revealed significant main group effects for protraction at low velocity (F1 = 10.469, P = .002) and at high velocity (F1 = 9.061, P = .005). For the retraction movement, no significant interaction or main effects were found at low velocity; however, results indicated a significant group × side interaction effect at high velocity (F1 = 4.19, P = .006). Results from the pairwise comparisons indicated that, for protraction, gymnasts were stronger than the controls on their dominant side at both velocities. For retraction, no significant group differences were found. Regarding side differences within each group, gymnasts demonstrated significantly more retraction strength on their dominant side than on their nondominant side (P = .003).

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Table 1 Peak Force/Body Mass (N/kg × 100) of Scapular Protraction and Retraction (Mean ± SD).

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Work/Body Mass The descriptive data and the results from the post hoc Bonferroni adjustments for work/body mass for both groups, both sides, both testing velocities, and both movement directions are presented in Table 2. For the protraction movement, a significant group × side interaction effect at low velocity (F1 = 4.646, P = .037) was noted. However, the post hoc Bonferroni tests did not confirm any significant group or side difference. For protraction at high velocity and retraction at both velocities, the general linear model 2-way, repeated-measures ANOVA showed no significant interaction or main effects.

Table 2 Work/Body Mass of Scapular Protraction and Retraction (Mean ± SD)*.

Protraction to Retraction Ratio Results from the descriptive analysis and results from the post hoc Bonferroni adjustments for both groups, both sides, and both testing velocities are presented in Table 3. For the agonist to antagonist ratio, the general linear model 2-way, repeated-measures ANOVA revealed significant main group effects (F1 = 4.316, P = .044) at low velocity and a significant group × side interaction effect at high velocity (F1 = 11.628, P = .001). Results from the post hoc tests showed that the gymnasts had a lower protraction to retraction ratio on their dominant sides than on their nondominant sides at high velocity (P < .001) and a higher protraction to

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retraction ratio on their nondominant sides at both velocities than the control group had (P = .021 at low velocity, P < .001 at high velocity).

Table 3. Agonist to Antagonist (Protractor to Retractor) Ratio as Mean ± SD for Both Groups, Both Sides, and Both Testing Velocities.

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Fatigue Index The results of the descriptive analysis for this variable for both groups and both sides are presented in Table 4. The general linear model 2-way, repeated-measures ANOVA showed no significant interaction or main effects for either movement direction. This means that, although fatigue index data were slightly lower in the gymnast group than in the control group (with the exception of retraction on the nondominant side), these results did not reach statistical significance.

Table 4 Fatigue Index of Scapula Protraction and Retractor (Mean ± SD).

Go to: DISCUSSION Our purpose was to determine whether, based on the high-level sport participation of the gymnasts, strength and endurance differences existed between young, elite gymnasts and nonathletic adolescents. Our study provides important information related to adaptations of scapular muscle training that occur in adolescent gymnasts participating at an elite level. This information will assist athletic trainers and physical therapists from both an injury-prevention and a rehabilitation perspective.

Peak Force/Body Mass Our results show that the gymnast group was significantly stronger into protraction on the nondominant side at low velocity and on both sides at high velocity than the

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controls were. This increased protraction strength may be the result of the specific characteristics of the sport, in which an athlete frequently has to push off from weight bearing. Powerful protraction is a necessary condition for this movement.

Showing higher values for protraction peak force/body mass, our results demonstrate that this muscle was stronger in the gymnasts than in the nonathletic adolescents.

No differences related to retraction peak force/body mass were apparent between groups, but side differences were evident based on arm dominance. Specifically at 36.6 cm/s, the gymnasts were significantly stronger on their dominant sides than on their nondominant sides. In view of the bilateral use of the arms in gymnastics, we did not expect side differences based on arm dominance in the gymnasts.

However, we should take into account that, despite the characteristic of bilateral arm use, gymnasts exhibit more unilateral arm use than, for instance, swimmers or rowers. In addition to bilateral exercises, numerous gymnastic movements are performed on 1 hand. Natural dominance probably determines the arm that the gymnast prefers to use. In addition, some categories of gymnastics, in particular acrobatic gymnastics, require considerable strength in the dominant arm for activities, such as elevating the partner. Seven of the 16 gymnasts practiced acrobatic gymnastics, possibly explaining side differences in this population.

Not all researchers agree that differences in muscle strength are based on arm dominance in overhead athletes. Cools et al9 found no significant side differences in isokinetic scapular muscle strength in a healthy population of volleyball players.

In contrast, other investigators have demonstrated increased muscle strength of the scapular depressors8 and in the middle and lower trapezius21 on the dominant side in professional baseball players. However, in these studies, isometric muscle strength was evaluated with a hand-held dynamometer, so comparison with our results should be performed with caution.

Work/Body Mass Our results revealed no significant group or side differences for the variable work/body mass. In spite of strength differences, work performed during the repetition of maximal peak force, which was normalized to body mass, seemed to be equal for both groups and both sides. We have no data with which to compare our results because this variable is rarely examined in isokinetic testing. However, work in relation to body mass provides the researcher or clinician with relevant information about muscle performance. Possibly, a difference in shape of the force-length curve may offer an explanation for this finding. A curve with a short,

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steep slope to a high peak-force value may result in similar work values as a curve with a long, flat slope to a smaller peak-force value.22 However, we did not examine the shape of the force-length curves, so our explanation remains hypothetical.

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Protraction to Retraction Ratio Agonist to antagonist ratios provide important information about the relative strength of 1 muscle group to another and, thus, about muscle balance around a joint or segment. During arm motion, the scapula performs rotatory and translatory movements, but these movements do not occur independent of one another. 1,6,23 The general scapular movement pattern consists of progressive external and upward rotation of the scapula and movement from an anteriorly to a posteriorly tilted position as the humeral elevation angle increases.23,24 Simultaneous actions of the serratus anterior and the trapezius muscle as a force couple perform and control these movements.1 In the scapulothoracic joint, the protraction to retraction ratio is approximately 1 in a nonathletic adult population, meaning the protractors and the retractors are equal in strength.14 Our gymnasts exhibited overall higher protraction to retraction ratios than the control group exhibited. These differences reached statistical significance on the nondominant side at both velocities. These higher values are the result of the higher protraction peak force/body mass in the gymnast group. Interestingly, in the control group, we also found that the agonist to antagonist ratios were slightly higher than the standard of 1,14 particularly at low velocity. Compared with adults, adolescents seem to have relatively stronger protractors than retractors. The question arises whether the higher values in the gymnast group should be interpreted as a result of sport-specific adaptation or as a reflection of adolescent muscle characteristics. Further investigation of agespecific characteristics of scapulothoracic muscle performance in athletic and nonathletic subjects is imperative to answer this question.

Fatigue Index In addition to evaluating muscle strength, we investigated muscle endurance. The fatigue index was selected as the dependent variable measuring the degree of muscle fatigue after 40 repetitions, and it indicated the endurance capacity of the muscles. Researchers11,17,25 have found that scapulothoracic muscles are susceptible to muscle fatigue and that muscle fatigue alters the scapular kinematics. Authors12,13,24 have shown that altered scapular kinematics are correlated with shoulder impingement. Therefore, analysis of scapular muscle endurance is clinically relevant. No standardized protocol for evaluating fatigue is

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available. The number of repetitions in a fatigue test varies from 20 to 100 repetitions.17–20 We chose a test bout of 40 repetitions to fatigue the scapular muscles. Because 180°/s is a frequently used testing velocity for endurance measurement, we chose the corresponding linear speed of 36.6 cm/s. In our investigation, the work fatigue index values were all positive. This means that, in both groups on both sides, the endurance test resulted in a decrease in work between the first third and the last third of the 40 repetitions. However, no significant group or side differences became apparent. The gymnast group seemed to have no more or no less endurance than the control group. Nevertheless, with the exception of retraction on the nondominant side, all values for work fatigue were slightly smaller in the gymnast group, reflecting less fatigue and more endurance capacity. The lack of significance may have resulted from the large SDs of this variable, suggesting much intersubject variability in endurance capacity.

Some questions arise from our results. What is the clinical relevance of the scapular muscle performance results? Are differences in strength and agonist to antagonist ratios the outcome of sport-specific adaptations, increasing the risk for injury? If they are, should the clinician try to alter them, or are these adaptations necessary for optimal sports performance and normal in view of the age of the population? Investigators1,4,8,9,26 do not have a unanimous opinion about this dilemma. According to some authors,1,8,26 adaptations should be corrected as early as possible in the athlete's career to prevent overuse injuries. In that case, the young gymnasts should thoroughly train the retractors to restore the muscle balance around the scapula. Others27 believe that structural and functional adaptations are necessary to protect the musculoskeletal system against injury imposed by the high-velocity movements, such as throwing or weight bearing in gymnastics. In view of that hypothesis, correcting the adaptations may increase the risk of overuse injuries.

Because of the relevance of the kinetic chain principles during daily movements and particularly during complex sport movements, local adaptations at the scapulothoracic joint may influence the quality of movement in other links of the kinetic chain and the quality of the final outcome. Stronger protractors possibly increase the energy transfer from the trunk into the upper extremities or vice versa, and they improve athletic performance.1 However, imbalances in the scapular muscles, with relative decrease in muscle strength of the trapezius muscle in relation to protractor strength, may jeopardize not only scapular stability but also trunk stability.28 Movement patterns that do not sequentially activate all portions of the kinetic chain or that leave out a portion or link, such as trunk extensions or rotation, can lead to injury and nonoptimal performance.2 Prospective studies of

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larger groups of gymnasts are needed to identify the possible influence of adaptations in the scapular muscles on the quality of gymnastic performance and on the risk for overuse injury in other body parts.

The major limitation of our study can be found in the composition of both groups.

Dividing the gymnasts into subgroups of sex, age, and gymnastic discipline was not possible because the number of participants was rather low. As a result of this limitation, extrapolation of our results into a general gymnastic population should be performed with caution. Investigating possible strength differences based on adolescence, specific biological development, and the specific demands of their discipline would be interesting. Moreover, we chose to investigate a control group matched by age because this grouping variable was objective and safe to standardize. However, we should take into account that the high level of sport participation probably resulted in large morphologic and physiologic differences between the groups. Normalizing our strength results to the subject's body mass possibly only partially addressed this limitation. Future investigators should emphasize the effort to categorize young gymnasts with respect to nonathletic individuals based on biologic age differences rather than on pure anthropometric data.

Go to: CONCLUSIONS In summary, scapular muscle performance in young, elite gymnasts is characterized by increased protraction strength and by altered muscular balance around the scapula compared with scapular muscle performance in nonathletic adolescents. Further research is necessary to determine whether these adaptations increase injury risk or are necessary in view of their high-level of sport performance.

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