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Muscle Hypertrophy in Prepubescent Tennis Players: a Segmentation MRI Study

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Muscle Hypertrophy in Prepubescent Tennis Players: a Segmentation MRI Study Muscle Hypertrophy in Prepubescent Tennis Players: A Segmentation MRI Study Joaquin Sanchis-Moysi1*, Fernando Idoate2, Jose A. Serrano-Sanchez1, Cecilia Dorado1, Jose A. L. Calbet1 1 Department of Physical Education, University of Las Palmas de Gran Canaria, Las Palmas de Gran Canaria, Spain, 2 Department of Radiology, Clı´nica San Miguel, Pamplona, Spain Abstract Purpose: To asses if tennis at prepubertal age elicits the hypertrophy of dominant arm muscles. Methods: The volume of the muscles of both arms was determined using magnetic resonance imaging (MRI) in 7 male prepubertal tennis players (TP) and 7 non-active control subjects (CG) (mean age 11.060.8 years, Tanner 1–2). Results: TP had 13% greater total muscle volume in the dominant than in the contralateral arm. The magnitude of inter-arm asymmetry was greater in TP than in CG (13 vs 3%, P,0.001). The dominant arm of TP was 16% greater than the dominant arm of CG (P,0.01), whilst non-dominant arms had similar total muscle volumes in both groups (P = 0.25), after accounting for height as covariate. In TP, dominant deltoid (11%), forearm supinator (55%) and forearm flexors (21%) and extensors (25%) were hypertrophied compared to the contralateral arm (P,0.05). In CG, the dominant supinator muscle was bigger than its contralateral homonimous (63%, P,0.05). Conclusions: Tennis at prepubertal age is associated with marked hypertrophy of the dominant arm, leading to a marked level of asymmetry (+13%), much greater than observed in non-active controls (+3%). Therefore, tennis particpation at prepubertal age is associated with increased muscle volumes in dominant compared to the non-dominant arm, likely due to selectively hypertrophy of the loaded muscles. Citation: Sanchis-Moysi J, Idoate F, Serrano-Sanchez JA, Dorado C, Calbet JAL (2012) Muscle Hypertrophy in Prepubescent Tennis Players: A Segmentation MRI Study. PLoS ONE 7(3): e33622. doi:10.1371/journal.pone.0033622 Editor: Hani A. Awad, University of Rochester, United States of America Received October 2, 2011; Accepted February 13, 2012; Published March 13, 2012 Copyright: ß 2012 Sanchis-Moysi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was granted by Real Madrid – Universidad Europea de Madrid Research Chair (2009/04RM) and Ministerio de Ciencia e Innovacio´n (DEP2010- 21866). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction individual muscles have never been assesed with state-of-the-art technology (MRI) in prepubertal athletes. It remains to be There is discrepancy about training-induced muscle hypertrophy determined whether tennis at prepubertal age elicits the in preadolescents [1,2,3]. It has been suggested that inadequate levels hypertrophy of specific muscles of the dominant compared to of circulating androgens [3] or training stimulus [4] may limit muscle the non-dominant arm using MRI. hypertrophy before puberty. Tennis is a good experimental approach Common injuries in tennis players have been associated to the to analyze whether exercise before puberty may elicit muscle asymmetric hypertrophy of the upper extremity, i.e., epicondilitis hypertrophy [5,6,7,8]. Both extremities have similar genetic endow- [9,10] or shoulder impingement syndrome [11,12,13]. A better ment, are submitted to similar hormonal and nutritional influences, knowledge of the adaptability of the upper extremity muscles in and therefore, side-to-side differences in arm muscle volumes reflect prepubertal tennis players could advance in the undersatanding of the maginitude of the exercise-induced muscle hypertrophy [8]. the mechanisms leading to overload injuries in adulthood. Using dual-energy X-ray absorptiometry (DXA), Calbet et al. The main purpose of this study was to asses if participation in [5] showed that male professional tennis players who started tennis regular tennis training during prepuberty is associated with the practice before puberty had 20% more lean mass in the dominant hypertrophy of dominant arm muscles, and to determine which than in the contralateral upper extremity. Recently, using the individual muscles of the dominant arm are specifically hypertro- same method, it has been estimated that 50–75% of this phied in response to tennis loading. asymmetry is attained at prepubertal ages [6]. A more detailed analysis using magnetic resonance imaging (MRI) found that in Methods male professional tennis players dominant deltoid, triceps, arm flexors and forearm superficial flexors are hypertrophied 11–15% Subjects compared to the contralateral arm, whilst no significant differences Fourteen boys (age 11.060.8 y, Tanner 1–2) enrolled in the were observed in the other muscle groups [8]. But the volumes of study. The participants were consecutively recruited from tennis PLoS ONE | www.plosone.org 1 March 2012 | Volume 7 | Issue 3 | e33622 Muscle Hypertrophy in Prepubescent Boys clubs of Gran Canaria, as well as from one primary school through volumes of: mobile wad (brachioradialis, extensor carpi radialis longus, local announcements. To be included participants had to be below extensor carpi radialis brevis), flexors (pronator teres, flexor carpi radialis, 12 years old, healthy, without any chronic disease and free of flexor carpi ulnaris, palmaris longus, flexor digitorum superficialis, pronator musculo-skeletal conditions or bone fractures. Seven of these boys quadratus, flexor digitorum profundus, flexor pollicis longus), extensors were tennis players (TP) who had been participating in competitive (extensor carpi ulnaris, extensor digitorum communis, extensor digiti tennis for a minimum of 2 years, with a frequency of at least 5 days minimi, anconeus, extensor indicis propius, extensor pollicis longus, per week. Control children (n = 7) were recruited from a primary extensor pollicis brevis, abductor pollicis longus) and supinator [16,17]. school among children who did not participate in any regular form To determine the distribution of muscle volume among muscles of of exercise, apart from the compulsory physical education a given tennis player, we calculated the volume fraction, expressed curriculum (2 weekly sessions of 45 min each), and were assigned as a percentage of total muscle volume for each muscle, as to the control group (CG). Table 1 summarizes the main described elswere [8,18]. The mean volume fraction for each characteristics of each group. muscle across participants and volume fractions for the upper arm Each participant and their parents were informed about the and forearm independently were also calculated. aims and procedures of the study and gave their informed signed consent to participate in the study. The study was approved by the Statistical analysis ethical committee of the University of Las Palmas de Gran Mean and standard desviation of the mean are given as Canaria. descriptive statistics in the text, standard error of the mean in the figures. Differences between groups were analyzed using a two Pubertal status assessment factor mixed ANCOVA with side (dominant or non- dominant) as Tanner pubertal status was self-assessed with parental guidance a within-subjects factor and group (TP or CG) as a between using the standard five scale Tanner stages [14]. subjects factor, with height as covariate and post hoc differences tested with the Bonferroni test. Prior to the ANCOVA tests, Magnetic resonance imaging variables were checked for normality using the Shapiro-Wilks test and for homogeneity with the Levene Test. Side-to-side differences MRI was used to determine the muscle cross sectional area into each group were assessed using Student’s paired t-tests, (CSA) and muscle volume of the arm and forearm muscles. A 1.5- adjusted for multiple comparisons with the Bonferroni-Holm T MRI scanner (Philips Achieva 1.5 Tesla system, Philips method. The degree of asymmetry was calculated as the mean of Healthcare, Best, The Netherlands) was used to acquire 10-mm the individual asymmetry values. Relationships between variables axial contiguous slices from each arm independently, i.e., without were assessed using the Pearson’s correlation test. SPSS package interslice separation. Participants were positioned as described (SPSS Inc., Chicago, IL, USA) for personal computers was used elsewhere [8]. Axial spin-echo T1-weighted MR images were for the statistical analysis. Significant differences were assumed acquired using a repetition time of 820 ms and echo time of when P,0.05. 20 ms, with a 35-cm2 field of view and a matrix of 5126512 pixels (in plane spatial resolution 0.6860.68 mm). Results The acquired MRI images were transferred to a PC computer for digital reconstruction to determine the CSA. All calculations Physical characteristics were carried out by the same investigator blinded to arm The physical characteristics of the boys are summarized in dominance using a specially designed image analysis software Table 1. The groups were comparable in height, age and total (SliceOmatic 4.3, Tomovision Inc, Montreal) for quantitative body mass (P = 0.86, P = 0.79 and P = 0.06, respectively). analysis of the images, as described elsewhere [15]. In the arms the volumes of the following muscles were assessed: Inter-arm asymmetry the flexor compartment (biceps brachii, brachialis and coracobrachialis), Table 2 summarizes total volume and muscle volume of each triceps and deltoid. In the forearms we determined the muscle muscle group of the dominant and the non-dominant arms, in TP and control participants. Tennis players had greater total muscle Table 1. Physical characteristics and training history of tennis volume in the dominant than in the contralateral arm (P,0.001), players and control group (mean 6 SD). whilst no significant differences were observed in the CG (P = 0.07). The magnitude of inter-arm asymmetry was greater in TP than in controls (13 vs 3%, respectively, P,0.001) (Fig.
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