The Hypertrophy of the Lateral Abdominal Wall and Quadratus Lumborum Is Sport-Specific: an MRI Segmental Study in Professional T

This article was downloaded by: [Univ Degli Studi di Verona] On: 23 May 2013, At: 11:49 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Sports Biomechanics Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rspb20 The hypertrophy of the lateral abdominal wall and quadratus lumborum is sport-specific: an MRI segmental study in professional tennis and soccer players Joaquin Sanchis-Moysi a , Fernando Idoate b , Mikel Izquierdo c , Jose A. Calbet a & Cecilia Dorado a a Physical Education Department, Las Palmas de Gran Canaria University, Canary Islands, Spain b Radiology Department, Clínica San Miguel, Pamplona, Navarra, Spain c Department of Health Sciences, Public University of Navarra, Navarra, Spain Published online: 18 Oct 2012.

To cite this article: Joaquin Sanchis-Moysi , Fernando Idoate , Mikel Izquierdo , Jose A. Calbet & Cecilia Dorado (2013): The hypertrophy of the lateral abdominal wall and quadratus lumborum is sport-specific: an MRI segmental study in professional tennis and soccer players, Sports Biomechanics, 12:1, 54-67 To link to this article: http://dx.doi.org/10.1080/14763141.2012.725087

PLEASE SCROLL DOWN FOR ARTICLE

Full terms and conditions of use: http://www.tandfonline.com/page/terms-and-conditions This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae, and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand, or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 Sports Biomechanics, 2013 Vol. 12, No. 1, 54–67, http://dx.doi.org/10.1080/14763141.2012.725087

The hypertrophy of the lateral abdominal wall and quadratus lumborum is sport-speciﬁc: an MRI segmental study in professional tennis and soccer players

JOAQUIN SANCHIS-MOYSI1,FERNANDOIDOATE2, MIKEL IZQUIERDO3, JOSE A. CALBET1, & CECILIA DORADO1

1Physical Education Department, Las Palmas de Gran Canaria University, Canary Islands, Spain, 2Radiology Department, Clı´nica San Miguel, Pamplona, Navarra, Spain, and 3Department of Health Sciences, Public University of Navarra, Navarra, Spain

(Received 25 August 2011; accepted 18 June 2012)

Abstract The aim was to determine the volume and degree of asymmetry of quadratus lumborum (QL), obliques, and transversus abdominis; the last two considered conjointly (OT), in tennis and soccer players. The volume of QL and OT was determined using magnetic resonance imaging in professional tennis and soccer players, and in non-active controls (n ¼ 8, 14, and 6, respectively). In tennis players the hypertrophy of OTwas limited to proximal segments (cephalic segments), while in soccer players it was similar along longitudinal axis. In tennis players the hypertrophy was asymmetric (18% greater volume in the non-dominant than in the dominant OT, p ¼ 0.001), while in soccer players and controls both sides had similar volumes ( p . 0.05). In controls, the non-dominant QL was 15% greater than that of the dominant ( p ¼ 0.049). Tennis and soccer players had similar volumes in both sides of QL. Tennis alters the dominant-to-non-dominant balance in the muscle volume of the lateral abdominal wall. In tennis the hypertrophy is limited to proximal segments and is greater in the non-dominant side. Soccer, however, is associated to a symmetric hypertrophy of the lateral abdominal wall. Tennis and soccer elicit an asymmetric hypertrophy of QL.

Keywords: Asymmetry, muscle volume, obliques abdominis, transversus abdominis Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013

Introduction Tennis and soccer induce the asymmetric hypertrophy of several trunk and leg muscles (Masuda et al., 2003; Sanchis-Moysi et al., 2010, 2011; Idoate et al., 2011). The muscles of the lateral abdominal wall (OT: external oblique, internal oblique, and transversus abdominis) and quadratus lumborum (QL) play an important role during kicking and tennis strokes (Raty et al., 1999; Chow et al., 2009). The asymmetric hypertrophy of these muscles may increase the risk of low back pain (Hides et al., 2008; Clark et al., 2009). It remains to be determined whether tennis and soccer practice elicits the hypertrophy of QL and the muscles of the lateral abdominal wall.

Correspondence: Joaquıń Sanchis Moysi, Departamento de EducaciońFı´sica, Campus Universitario de Tafira, 35017 Las Palmas de Gran Canaria, Canary Island, Spain, E-mail: [email protected]

q 2013 Taylor & Francis Hypertrophy of the lateral abdominal wall and QL 55

In tennis players, oblique muscles of the dominant side (the side of the arm holding the racket) together with rectus abdominis act as prime movers for twisting the trunk during the acceleration phase of the tennis serve (Chow et al., 2009). Professional tennis players have 35% greater volume in the non-dominant rectus abdominis than in the dominant side, reflecting the greater strength and power demands sustained by the contralateral side (Sanchis-Moysi et al., 2010). A similar pattern of asymmetry, although of lower magnitude, was recently observed in soccer players, suggesting that the forces acting on this muscle are somehow similar to tennis (Idoate et al., 2011). In addition, in Australian Football League (AFL) players, kicking induces greater hypertrophy of QL muscle from the side contralateral to the kicking leg (Hides et al., 2010). In fast bowler cricketers, who execute a similar movement than service in tennis, QL is also hypertrophied asymmetrically (Hides et al., 2008). The risk of low back pain has been associated with the asymmetric hypertrophy of obliques and transversus abdominis, and/or QL in AFL and cricketers (Engstrom et al., 2007; Hides et al., 2008, 2010), and also in non-athletes (Clark et al., 2009). The pattern and degree of asymmetry of trunk muscles can vary significantly depending on the sport (Sanchis-Moysi et al., 2010, 2011; Idoate et al., 2011). It remains to be determined whether soccer and tennis players without low back pain display asymmetrically hypertrophied QL and OT muscles. This information may be useful in the future to ascertain which type of muscle asymmetries may be associated with low back pain. It is not clear whether competing athletes are at risk of a higher prevalence of low back pain than non-athletes (Jacob et al., 2004). The prevalence and severity of low back pain is higher in sports with significant low back demands (Bahr et al., 2004). Low back pain is a common problem in tennis (Kibler, 2002) and not so frequent in soccer players (Junge & Dvorak, 2004). The incidence of low back pain over a one-year period in professional tennis players has been estimated in 19% (Verspeelt, 1995) and in professional soccer players in 12% (Walden et al., 2005). The main aim of the present study was to determine the pattern and degree of hypertrophy of QL and the muscles of the lateral abdominal wall (transversus abdominis, external and internal obliques, considered conjointly) in professional tennis and soccer players, using non- active controls as a reference. A secondary aim was to determine whether tennis and soccer induce an asymmetric hypertrophy of these muscles.

Methods

Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 Participants Eight male professional tennis players from the International Tennis Federation tour (Futures and Challengers tournaments), 14 male professional soccer players from a ﬁrst division team of the Spanish Football League and six non-active men (control group) agreed to participate in the study (Table I). Participants of the control group had never been involved in regular physical exercise. All subjects were randomly selected and did not have clinical history of musculoskeletal conditions, bone fractures or chronic diseases. Participants were informed about the potential beneﬁts and risks of the study and gave a written consent to participate. The study was approved by the ethical committee of the University of Las Palmas de Gran Canaria. All tennis and soccer players started their sport practice before 12 years old. In the tennis players, the arm holding the racket during the service stroke was selected as the dominant arm whereas in the controls, and in the soccer players, it was the preferred arm used to perform an overhead throw. In all participants, the criterion used to determine leg dominance was the preferred leg to kick a ball (dominant leg). 56 J. Sanchis-Moysi et al.

Table I. Physical characteristics of the tennis players, soccer players and control group.

Variables Tennis Soccer Controls

Age (years) 21.9 ^ 3.8 26.7 ^ 5.0* 27.5 ^ 8.1 Height (cm) 182.5 ^ 3.9 182.4 ^ 5.8 177.7 ^ 2.6‡ Body mass (kg) 75.4 ^ 6.9 77.2 ^ 6.2 75.5 ^ 11.1 BMI 22.6 ^ 1.5 23.2 ^ 1.2 23.9 ^ 3.5 Current training volume (h/week) 25.0 ^ 6.7 9.0 ^ 0.0 – Dominant leg right/left 6/2 12/2 6/0 Dominant arm/backhand stroke Right/2 hands backhand 6/2 12/0 6/0 Left/2 hands backhand 2/0 2/0 – OT length (cm) 1st segment 2.7 ^ 0.5 2.9 ^ 0.3 2.5 ^ 0.6 2nd segment 3.1 ^ 0.4 3.2 ^ 0.4 3.0 ^ 0.0 3rd segment 3.1 ^ 0.4 3.0 ^ 0.0 2.8 ^ 0.4 4th segment 3.5 ^ 0.5 3.5 ^ 0.5 3.0 ^ 0.0‡ 5th segment 2.8 ^ 0.5 2.9 ^ 0.3 2.7 ^ 0.5 6th segment 3.4 ^ 0.5 3.4 ^ 0.5 3.0 ^ 0.0‡ 7th segment 3.1 ^ 0.4 3.1 ^ 0.3 2.8 ^ 0.4 8th segment 3.6 ^ 0.5 3.8 ^ 0.4 3.0 ^ 0.0‡ Total 25.4 ^ 2.7 25.8 ^ 1.9 22.8 ^ 1.6† QL length (cm) 1st segment 3.0 ^ 0.5 3.1 ^ 0.4 3.2 ^ 0.4 2nd segment 3.3 ^ 0.5 3.4 ^ 0.5 3.3 ^ 0.5 3rd segment 3.8 ^ 0.7 3.9 ^ 0.3 3.7 ^ 0.5 Total 10.0 ^ 1.5 10.5 ^ 0.9 10.2 ^ 1.2

Notes: Totaland regional length of OTand QL (M ^ SD). Signiﬁcant differences ( p , 0.05): *TP vs. SP, †CG vs. SP, ‡CG vs. TP and SP.

Leg and arm dominance was in the same side in all subjects except in two. In one right handed tennis player, the left leg was the dominant and in one left handed tennis player the right leg was the dominant. For comparative purposes, in this article the dominant side of OT and QL corresponded to the same side of the dominant arm.

Magnetic resonance imaging (MRI) MRI was used to determine the muscle cross-sectional area (CSA) and the muscle volume of Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 the left and right QL and OT. A 1.5 T MRI scanner (Philips Achieva 1.5 Tesla system, Philips Healthcare, Best, the Netherlands) was used to acquire 10-mm axial contiguous slices from trunk, abdomen, and pelvis, without interslice separation. Sagittal, coronal, and transverse localizers of the body were obtained to determine precisely the anatomic sites for image acquisition. Transverse MRI images at rest (a breath-hold at mid expiration) oriented to be perpendicular to the anterior abdominal wall were obtained. Axial gradient-echo T1-weighted MR images were used with a repetition time of 132 ms and an echo time of 4.2 ms, ﬂip-angle of 808 with a 42-cm2 ﬁeld of view, and a matrix of 256 £ 256 pixels (in-plane spatial resolution 1.64 £ 1.64 mm). The body coil was used for image acquisition. The total MRI data acquisition time was about 20 s, which was within the breath-hold tolerance of all subjects. The acquired MRI images were transferred to a computer for digital reconstruction to determine the CSA. The volume for obliques and transversus abdominis (considered together), and QL were calculated from L1 to L2 discal level to the pubic symphysis (Sanchis-Moysi Hypertrophy of the lateral abdominal wall and QL 57

et al., 2010, 2011; Idoate et al., 2011). All calculations were carried out by the same investigator, who was blinded to arm dominance, using a specially designed image analysis software (SliceOmatic 4.3, Tomovision, Inc., Montreal, Canada), as described elsewhere (Lee et al., 2000). A threshold was selected for adipose and lean tissues on the basis of the gray-level image pixel histograms to identify tissue area, and the tissue boundaries were manually traced (Lee et al., 2000). The total volume of OT and QL were assessed in each subject (Bancroft et al., 2007). Regional volumes of OT were calculated for comparative purposes, as described elsewhere (Sanchis-Moysi et al., 2010). Total volume of OT was divided into eight regions (S1 –S8, from proximal to distal). To determine the boundaries of each segment, the total number of slices was divided by 2. Then, each fraction was divided successively by 2 until eight segments were obtained. If the initial number of slices in any segment was odd, the extra slice was included in the most distal region. The volume of each segment was calculated using the same procedures described to calculate the total volume. To calculate the regional volumes of QL, total volume was divided into three regions. The boundaries of each segment were determined by dividing the total number of slices by 3. When the initial number of slices was not multiple of 3, the extra slices after the division by 3 were included into the most distal segment. Then, the volume of each segment was calculated using the same procedures described to calculate the total volume. The degree of asymmetry was assessed by calculating the dominant-to-non-dominant volume ratio:

non-dominant2dominant volume £ 100: ð1Þ dominant volume

The intra-observer coefﬁcients of variation for the assessment of OTand QL total volumes were 1.6% and 0.9%, respectively.

Statistical analysis Results are presented as M ^ SD, except for the bar ﬁgures, which are presented as M ^ SE of the mean. Side-to-side comparisons were carried out using the paired Student’s t-test adjusted for multiple comparisons using the Bonferroni–Holm method, when more than

Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 two segments were compared. Analyses of covariance were performed to compare means across groups, with age, body mass index (BMI), and total length of OT and QL as covariates. Between-groups segment-to-segment comparisons were adjusted for the length of the segment under scrutiny. The relationship between muscle lengths and volumes into each group was determined by linear regression analysis. The similarity of slopes and intercepts of these linear relationships was tested with a t-test by applying the model: Yij ¼ ai þ biXij þ 1ij for i ¼ 1, 2 (1 ¼ tennis or soccer, 2 ¼ controls) and j ¼ 1, ..., n1, being 1ij independent identically distributed random variables following a distribution N (0, s1). SPSS package (SPSS, Inc., Chicago, IL, USA, v15.0) for personal computers was used for the statistical analysis. Signiﬁcant differences were assumed when p , 0.05.

Results Physical characteristics and total and regional length of OT and QL are summarized in Table I. 58 J. Sanchis-Moysi et al.

Differences into each group Tables II and III summarize total and regional muscle volumes of OT and QL, respectively, in tennis players, soccer players, and controls. In the tennis players, total volume of the non- dominant OT was 18% greater than the dominant ( p ¼ 0.001), while in the soccer players and in controls both sides had similar volumes ( p . 0.05 in both groups). In the tennis players, the non-dominant segments 2–4 of OT were hypertrophied compared to the dominant side ( p ¼ 0.024, p ¼ 0.004, and p ¼ 0.001, respectively). Side-to-side differences were not statistically signiﬁcant at any segmental level in the soccer players and in the control group. In the tennis players, an inverse relationship was observed between the length of OT starting from the proximal segment (cephalic segment) and the degree of asymmetry in muscle volume expressed as the non-dominant/dominant ratio (r ¼ -0.82, p ¼ 0.038). In the control group, the non-dominant QL was 15% greater than the dominant side ( p ¼ 0.049). Tennis and soccer players had similar volumes in both sides of QL ( p . 0.05 in both groups). When side-to-side differences in the volume of QL were compared segment by segment, no signiﬁcant differences were observed in any group at any segmental level.

Differences between groups Lateral abdominal wall. Compared with controls, the tennis players had 32% ( p ¼ 0.001) and 41% ( p , 0.001) more total volume in the dominant and non-dominant OT, respectively. The soccer players had 38% greater total volume than the controls in both OT ( p , 0.001). After adjusting for age, the length of OT and BMI as covariates, the tennis players had 25% ( p ¼ 0.001) and 34% ( p , 0.001) more total muscle volume than controls in the dominant and non-dominant OT, respectively (Figure 1A). In the soccer players, both adjusted-OT volumes were 30% greater than in the control group ( p , 0.001). Tennis and soccer players had similar volumes in both OT, even after controlling for age, the length of OTand BMI as covariates. Compared segment by segment, the soccer players had greater volumes than controls in dominant segments 1–7 ( p ¼ 0.005, p ¼ 0.001, p , 0.001, p , 0.001, p ¼ 0.001, p ¼ 0.007, and p ¼ 0.025, respectively) and non-dominant 1–8 ( p ¼ 0.017, p ¼ 0.002, p , 0.001, p , 0.001, p ¼ 0.005, p ¼ 0.007, p ¼ 0.024, and p ¼ 0.014, respectively). In the tennis players, segments 1–4 of the dominant ( p ¼ 0.032, p , 0.001, p , 0.001, and p ¼ 0.016, respectively) and non-dominant OT ( p ¼ 0.038, p , 0.001, p , 0.001, and p ¼ 0.004, respectively) were greater than in controls. After adjusting for age, the length of each OT segment and BMI as covariates, the differences between soccer players and controls Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 remained in the dominant OT and in the non-dominant side were significant in segments 2–4 and 7 (Figure 2A). Whereas in the tennis players, dominant segments 2 and 3 and non- dominant segments 2–4 were bigger compared with the control group (Figure 4A). The degree of side-to-side asymmetry in the OT was greater in the tennis players (17.8 ^ 8.4%) than in the control group (3.7 ^ 7.5%, p ¼ 0.007), and in the soccer players (2.0 ^ 5.7%, p , 0.001) (Figure 3A). Compared segment by segment, the degree of asymmetry was significantly greater in the tennis players than in controls in segments 3–5 ( p ¼ 0.030, p ¼ 0.009, and p ¼ 0.024, respectively), and also in tennis than in soccer players in segments 2–5 ( p ¼ 0.009, p ¼ 0.001, p , 0.001, and p ¼ 0.010, respectively) (Figure 3B). No significant differences were observed between soccer players and controls in the total or segmental dominant-to-non-dominant volume ratio.

Quadratus lumborum. Compared with controls, the soccer players had 40% ( p , 0.001) and 29% ( p ¼ 0.019) greater QL total volume in the dominant and non-dominant sides, Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013

Table II. Volumes of obliques and transversus abdominis, considered conjointly (values expressed in cm3, M ^ SD).

Tennis players Soccer players Controls

Segment Dominant Non-dominant p Dominant Non-dominant p Dominant Non-dominant p QL and wall abdominal lateral the of Hypertrophy

S1 94.3 ^ 18.4 100.2 ^ 19.9 .0.05 97.1 ^ 17.1 104.1 ^ 25.2 .0.05 67.6 ^ 22.9 71.1 ^ 27.2 .0.05 S2 114.2 ^ 12.7 130.2 ^ 15.7 0.024 115.0 ^ 22.6 118.1 ^ 25.6 .0.05 76.5 ^ 12.1 79.5 ^ 10.9 .0.05 S3 119.2 ^ 20.7 144.3 ^ 16.6 0.004 118.8 ^ 14.9 120.1 ^ 12.4 .0.05 70.7 ^ 15.9 75.3 ^ 17.6 .0.05 S4 91.9 ^ 29.0 117.4 ^ 37.0 0.001 109.7 ^ 25.1 107.7 ^ 24.9 .0.05 57.8 ^ 6.6 61.8 ^ 5.6 .0.05 S5 33.9 ^ 16.4 42.3 ^ 21.6 .0.05 46.0 ^ 9.8 46.6 ^ 16.0 .0.05 26.6 ^ 10.7 24.9 ^ 6.3 .0.05 S6 16.5 ^ 7.1 19.1 ^ 9.2 .0.05 22.6 ^ 5.9 22.2 ^ 7.1 .0.05 14.1 ^ 4.6 12.7 ^ 4.0 .0.05 S7 5.9 ^ 1.8 5.9 ^ 1.5 .0.05 9.8 ^ 2.5 9.9 ^ 3.2 .0.05 7.0 ^ 1.8 6.3 ^ 2.5 .0.05 S8 3.7 ^ 1.1 3.6 ^ 1.3 .0.05 6.1 ^ 2.6 6.2 ^ 2.5 .0.05 4.1 ^ 1.9 3.4 ^ 0.9 .0.05 Total 479.5 ^ 73.3 563.0 ^ 84.1 0.001 525.0 ^ 62.3 534.9 ^ 68.2 .0.05 323.7 ^ 53.6 334.2 ^ 49.7 .0.05

Note: Comparisons are made between dominant and non-dominant sides into each group. 59 Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 60 .SnhsMyie al. et Sanchis-Moysi J.

Table III. Volumes of quadratus lumborum (values expressed in cm3, M ^ SD).

Tennis players Soccer players Controls

Segment Dominant Non-dominant p Dominant Non-dominant p Dominant Non-dominant p

S1 13.6 ^ 5.8 13.0 ^ 5.5 .0.05 16.2 ^ 3.3 16.2 ^ 3.3 .0.05 12.1 ^ 3.8 13.3 ^ 3.3 .0.05 S2 22.4 ^ 4.2 23.5 ^ 5.0 .0.05 29.6 ^ 5.5 29.6 ^ 8.0 .0.05 17.0 ^ 4.5 20.5 ^ 9.8 .0.05 S3 33.5 ^ 7.7 35.8 ^ 9.3 .0.05 41.2 ^ 9.6 39.2 ^ 10.1 .0.05 23.5 ^ 5.3 27.2 ^ 6.6 .0.05 Total 69.4 ^ 14.6 72.2 ^ 13.2 .0.05 86.9 ^ 14.5 85.5 ^ 19.6 .0.05 52.3 ^ 12.1 60.9 ^ 19.1 0.049

Note: Comparisons are made between dominant and non-dominant sides into each group. Hypertrophy of the lateral abdominal wall and QL 61

Figure 1. Comparison of the total muscle volume of the dominant and non-dominant obliques and transversus abdominis (A), and quadratus lumborum muscles (B), between tennis players, soccer players, and non-athletes, after adjustment for the length of the muscle, age, and BMI. *p , 0.05. Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013

Figure 2. Differences between professional soccer players and non-athletes in the regional muscle volumes of the dominant and non-dominant sides (expressed in percentage) of obliques and transversus abdominis (A) and quadratus lumborum muscles (B), after adjustment for the length of the muscle, age, and BMI. 62 J. Sanchis-Moysi et al.

Figure 3. Comparison between the percentage of asymmetry, in tennis players, soccer players, and non-athletes, of obliques and transversus abdominis, in total volume (A) and segment by segment (B), and of quadratus lumborum,in total volume (C) and segment by segment (D). *p , 0.05.

Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 respectively. The tennis players had 25% greater dominant QL volume compared with controls ( p ¼ 0.038), but no signiﬁcant between-groups differences were observed in non- dominant side ( p . 0.05). In the soccer players the volume of the dominant QL was greater than in the tennis players (20%, p ¼ 0.013) but the volume of the non-dominant QL was similar in both groups ( p . 0.05). After controlling for age, the length of QL and BMI as covariates, the soccer players had 42% ( p , 0.001) and 31% ( p ¼ 0.002) greater QL volumes than controls in the dominant and non-dominant sides, respectively (Figure 1B). Compared with controls, the tennis players had 30% ( p ¼ 0.004) greater volumes in the dominant QL and the non-dominant QL showed a trend for greater values (20%, p ¼ 0.098). When soccer and tennis players were compared, the dominant QL muscle volume was 18% greater ( p ¼ 0.009) in the soccer players, while no signiﬁcant differences in non-dominant QL was observed between both groups ( p . 0.05). Compared segment by segment, the soccer players had greater volumes than controls in the dominant segments 1–3 ( p ¼ 0.024, p , 0.001, and p , 0.001, respectively) and Hypertrophy of the lateral abdominal wall and QL 63

non-dominant 2 and 3 ( p ¼ 0.041 and p ¼ 0.016, respectively), whereas in the tennis players only dominant segments 2–3 were greater than in controls ( p ¼ 0.038 and p ¼ 0.017, respectively). After controlling for age, the length of each segment of QL and BMI as covariates, these differences remained (Figures 2B and 4B). The dominant-to-non-dominant volume ratio of the QL was greater in controls than in soccer players (14.9 ^ 13.4 vs. -1.6 ^ 17.6, respectively, p ¼ 0.048), and similar in controls and in tennis players (14.9 ^ 13.4 vs. 5.3 ^ 12.6, respectively, p . 0.05) (Figure 3C).

Discussion and implications The present study shows that tennis and soccer practice at professional levels is associated with a similar degree of hypertrophy of OT (mean increase 30%, both sides considered conjointly). However, in the tennis players the hypertrophy of OT was limited to proximal segments, while in soccer players the degree of hypertrophy was similar along longitudinal axis. In addition, in tennis players the hypertrophy of OTwas asymmetric, the non-dominant side was 18% greater than the dominant, while soccer players and controls had similar volumes in both sides. The present study also shows that the side-to-side asymmetry of QL observed in control subjects is altered in tennis and soccer players, which displays greater hypertrophy of the dominant side. An important function of obliques and transversus abdominis muscles is to stabilize the trunk to protect the spine from injury (Borghuis et al., 2011). Both sports continuously encounter situations in which the stabilization of the upper trunk is required, i.e., turns, stops and starts or sudden changes of direction. However, abdominal muscles are also involved asymmetrically in power generation during kicking (Dorge et al., 2002; Sanchis-Moysi et al., 2010; Idoate et al., 2011) and tennis strokes (Elliott, 2002; Chow et al., 2009; Sanchis- Moysi et al., 2010). The present study shows for the first time that in tennis players OT is hypertrophied asymmetrically, the non-dominant side was 18% greater than the dominant, whereas in soccer players, both OT have similar volumes. Moreover, we have shown that the non-dominant OTwas greater than the dominant in a very small region (segments 2–4). The greater hypertrophy of the non-dominant OT in the tennis players, and especially in proximal segments, may reflect the higher loads imposed to this side and region during tennis strokes, since any other genetic, nutritional or hormonal factors are acting on both sides. In the soccer players OT was symmetric at all segmental levels. Previously, Kubo et al. (2010) found that in Japanese soccer players CSA of internal and external oblique muscles was similar in both sides (average CSA measured at the midlevel of L2/L3, L3/L4, and L4/L5). Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 Interestingly, rectus abdominis of soccer players is symmetric and displays similar degree of hypertrophy (mean 26%, both sides considered conjointly) (Idoate et al., 2011) when compared with the OT (30%). Therefore, our results consistently indicate that kicking actions do not demand an asymmetric hypertrophy of the abdominal muscles. However, the OT might have an important role in force generation during kicking by means of a modification in the pattern of hypertrophy along the longitudinal axis. Bilateral differences in the pattern of hypertrophy along a muscle can modify peak torque capacity during unilateral exercises (Housh et al., 1992; Narici et al., 1996). The pattern of hypertrophy of OT for the soccer players was different between sides. In the non-dominant side the degree of hypertrophy increased progressively from proximal to distal regions, but in the dominant side increased similarly in all segmental levels (see Figure 4). A similar pattern of hypertrophy was recently reported in the rectus abdominis of these soccer players (Idoate et al., 2011). It remains to be determined whether these differences affect power generation during kicking. 64 J. Sanchis-Moysi et al.

Figure 4. Differences between professional tennis players and non-athletes in the regional muscle volumes of the dominant and non-dominant sides (expressed in percentage) of obliques and transversus abdominis (A) and quadratus lumborum muscles (B), after adjustment for the length of the muscle, age, and BMI.

The present study shows that tennis and soccer practice at a professional level elicits the asymmetric hypertrophy of QL. Both sports are associated to greater hypertrophy of the dominant compared with the non-dominant QL (42% vs. 31% in soccer and 30% vs. 20% in tennis players, respectively). This asymmetric hypertrophy compensated the side-to-side difference in muscle volume observed in the QL of non-active population (15% greater volume in the non-dominant than in the contralateral side). The magnitude and localization of the QL asymmetry observed in our non-active subjects agrees with previous studies (Marras et al., 2001; Clark et al., 2009), but this is the ﬁrst study that has analyzed the Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 hypertrophy of each QL independently in tennis and soccer players. In a pioneer research, Raty et al. (1999) showed that the CSA of QL analyzed at L3/L4 level (both sides considered together) was greater in soccer players than in long-distance runners, weight lifters, and shooters. Recently, Kubo et al. (2011) observed that this measure was associated to increased performance during 10–20 m running sprints. Hides et al. (2010) reported that in AFL players the CSA of non-dominant QL was 10% greater than the dominant at L3/L4 vertebral level. This degree of asymmetry is lower than the 15% observed in our control group in a similar segmental level and higher than the 2% observed in our soccer players. Therefore, soccer appears to impose greater loads than Australian football on the dominant QL. On the other hand, the greater hypertrophy of the dominant than the contralateral QL in the tennis players agrees with studies conducted in fast bowler cricketers (Engstrom et al., 2007; Hides et al., 2008). Engstrom et al. (2007) showed that the QL muscle volume of adolescent fast bowler cricketers was signiﬁcantly larger ipsilateral to the dominant arm, and that the side of the asymmetry observed in controls was reversed (Engstrom et al., 2007). Hypertrophy of the lateral abdominal wall and QL 65

Low back pain is a common problem in tennis (Kibler, 2002) and not so frequent in soccer players (Junge & Dvorak, 2004). The risk of low back pain has been associated to the asymmetric hypertrophy of obliques and transversus abdominis, and/or QL (Engstrom et al., 2007; Hides et al., 2008, 2010; Clark et al., 2009). It is well documented that abdominal muscles functions as an operational stability system to protect the spine from injury (Tesh et al., 1987; Hodges et al., 2005; Hides et al., 2010). Animal studies have provided evidence that this mechanism of protection is effective when its action is symmetrical between sides (Hodges et al., 2003). The present study shows that OT was symmetric in soccer and asymmetric in tennis players. In addition, in the tennis players the degree of hypertrophy of OT decreased progressively in the rostrocaudal direction, while in the soccer players was similar along the whole muscle. As illustrated in Figure 4, the lower protection of OT in the more distal segments together with the greater hypertrophy of QL on this region could also raise the risk of low back pain in the tennis players (Hainline, 1995; Renkawitz et al., 2006; Engstrom et al., 2007; Hides et al., 2008, 2010; Clark et al., 2009). This study has some limitations. In the present investigation, the criterion for the inclusion of the participants in the tennis and soccer groups was a starting playing age before 12 years old. Recent studies suggest that pre-pubescent tennis players may develop muscle hypertrophy with training (Sanchis-Moysi et al., 2012). It remains unknown, however, whether a difference in the starting age in sports could have an inﬂuence on the degree of muscle hypertrophy of OTand QL. Future studies should include longitudinal designs with appropriate control groups, analyzing the active part of the career and the effect of inactivity on the degree of muscular asymmetry.

Conclusion The present study describes for the ﬁrst time the effects of professional soccer and tennis on the muscle volumes of OT and QL. Both sports were found to be associated with a similar increase in the muscle volume of OT (mean 30%, both sides considered conjointly). We also observed that in the soccer players OT was hypertrophied along the longitudinal axis, whereas in the tennis players the hypertrophy was circumscribed only to proximal segments. In addition, in tennis players the non-dominant OT was 18% greater than the dominant, while soccer players and controls had similar volumes in both sides. Finally we have shown that soccer and tennis practice could compensate the side-to-side asymmetry observed in the QL of the non-active controls by eliciting greater hypertrophy of the dominant compared with the non-dominant side. Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 This investigation may have important practical implications for coaches and clinicians. The large side-to-side asymmetry of OTand QL in the tennis players could indicate that the asymmetric hypertrophy of these muscles might play an important role in tennis performance (Sanchis-Moysi et al., 2010, 2011). It remains to be determined whether the degree of asymmetry of OT and QL could be associated to power generation during tennis strokes and whether training programs should be aimed at developing more symmetry to prevent common overload tennis injuries, i.e., low back pain.

Acknowledgements The authors wish to thank all professional soccer and tennis players who volunteered in these studies. Special thanks are given to Sa´nchez-Casal Tennis Academy, and particularly to Emilio Sa´nchez Vicario for his crucial collaboration. They would like to express their gratitude also to Hospital San Roque Maspalomas (Gran Canaria) for allowing them to use 66 J. Sanchis-Moysi et al.

their MRI facilities. This study was granted by Ministerio de Ciencia e Innovacio´n, Spain (DEP2010-21866).

References Bahr, R., Andersen, S. O., Loken, S., Fossan, B., Hansen, T., & Holme, I. (2004). Low back pain among endurance athletes with and without specific back loading—A cross-sectional survey of cross-country skiers, rowers, orienteerers, and nonathletic controls. Spine, 29 (4), 449–454. Bancroft, L. W., Peterson, J. J., Kransdorf, M. J., Berquist, T. H., & O’Connor, M. I. (2007). Compartmental anatomy relevant to biopsy planning. Seminars in Musculoskeletal Radiology, 11 (1), 16–27. Borghuis, A. J., Lemmink, K. A., & Hof, A. L. (2011). Core muscle response times and postural reactions in soccer players and non-players. Medicine & Science in Sports & Exercise, 43 (1), 108–114. Chow, J. W., Park, S. A., & Tillman, M. D. (2009). Lower trunk kinematics and muscle activity during different types of tennis serves. Sports Medicine, Arthroscopy, Rehabilitation, Therapy & Technology, 1 (1), 24. Clark, B. C., Walkowski, S., Conatser, R. R., Eland, D. C., & Howell, J. N. (2009). Muscle functional magnetic resonance imaging and acute low back pain: A pilot study to characterize lumbar muscle activity asymmetries and examine the effects of osteopathic manipulative treatment. Osteopathic Medicine and Primary Care, 3,7. Dorge, H. C., Anderson, T. B., Sorensen, H., & Simonsen, E. B. (2002). Biomechanical differences in soccer kicking with the preferred and the non-preferred leg. Journal of Sports Sciences, 20 (4), 293–299. Elliott, B. C. (2002). Biomechanics of tennis. In A. F. H. Renstrom (Ed.), Tennis (pp. 1–29). Oxford: Blackwell Science. Engstrom, C. M., Walker, D. G., Kippers, V., & Mehnert, A. J. (2007). Quadratus lumborum asymmetry and L4 pars injury in fast bowlers: A prospective MR study. Medicine & Science in Sports & Exercise, 39 (6), 910–917. Hainline, B. (1995). Low back injury. Clinics in Sports Medicine, 14 (1), 241–265. Hides, J., Fan, T., Stanton, W., Stanton, P., McMahon, K., & Wilson, S. (2010). Psoas and quadratus lumborum muscle asymmetry among elite Australian Football League players. British Journal of Sports Medicine, 44 (8), 563–567. Hides, J., Stanton, W., Freke, M., Wilson, S., McMahon, S., & Richardson, C. (2008). MRI study of the size, symmetry and function of the trunk muscles among elite cricketers with and without low back pain. British Journal of Sports Medicine, 42 (10), 809–813. Hodges, P. W., Eriksson, A. E., Shirley, D., & Gandevia, S. C. (2005). Intra-abdominal pressure increases stiffness of the lumbar spine. Journal of Biomechanics, 38 (9), 1873–1880. Hodges, P., Kaigle Holm, A., Holm, S., Ekstrom, L., Cresswell, A., Hansson, T., & Throstensson, A. (2003). Intervertebral stiffness of the spine is increased by evoked contraction of transversus abdominis and the diaphragm: In vivo porcine studies. Spine, 28 (23), 2594–2601. Housh, D. J., Housh, T. J., Johnson, G. O., & Chu, W. K. (1992). Hypertrophic response to unilateral concentric isokinetic resistance training. Journal of Applied Physiology, 73 (1), 65–70. Idoate, F., Calbet, J., Izquierdo, M., & Sanchis-Moysi, J. (2011). Soccer attenuates the asymmetry of rectus abdominis muscle observed in non-athletes. PLoS ONE, 6 (4), e19022. Jacob, T., Baras, M., Zeev, A., & Epstein, L. (2004). Physical activities and low back pain: A community-based Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013 study. Medicine & Science in Sports & Exercise, 36 (1), 9–15. Junge, A., & Dvorak, J. (2004). Soccer injuries: A review on incidence and prevention. Sports Medicine, 34 (13), 929–938. Kibler, W. B. (2002). Pathophysiology of tennis injuries—An overview. In P. Renstrom (Ed.), Tennis (pp. 147–154). Berlin: Blackwell Publishing. Kubo, T., Hoshikawa, Y., Muramatsu, M., Iida, T., Komori, S., Shibukawa, K., & Kanehisa, H. (2011). Contribution of Trunk Muscularity on Sprint Run. International Journal of Sports Medicine, 32 (3), 223–228. Kubo, T., Muramatsu, M., Hoshikawa, Y., & Kanehisa, H. (2010). Profiles of trunk and thigh muscularity in youth and professional soccer players. Journal of Strength & Conditioning Research, 24 (6), 1472–1479. Lee, R. C., Wang, Z., Heo, M., Ross, R., Janssen, I., & Heymsfield, S. B. (2000). Total-body skeletal muscle mass: Development and cross-validation of anthropometric prediction models. American Journal of Clinical Nutrition, 72 (3), 796–803. Marras, W. S., Jorgensen, M. J., Granata, K. P., & Wiand, B. (2001). Female and male trunk geometry: Size and prediction of the spine loading trunk muscles derived from MRI. Clinical Biomechanics, 16 (1), 38–46. Masuda, K., Kikuhara, N., Takahashi, H., & Yamanaka, K. (2003). The relationship between muscle cross-sectional area and strength in various isokinetic movements among soccer players. Journal of Sports Sciences, 21 (10), 851–858. Hypertrophy of the lateral abdominal wall and QL 67

Narici, M. V., Hoppeler, H., Kayser, B., Landoni, L., Claassen, H., Gavardi, C., Conti, M., & Cerretelli, P. (1996). Human quadriceps cross-sectional area, torque and neural activation during 6 months strength training. Acta Physiologica Scandinavica, 157 (2), 175–186. Raty, H. P., Kujala, U., Videman, T., Koskinen, S. K., Karppi, S. L., & Sarna, S. (1999). Associations of isometric and isoinertial trunk muscle strength measurements and lumbar paraspinal muscle cross-sectional areas. Journal of Spinal Disorders, 12 (3), 266–270. Renkawitz, T., Boluki, D., & Grifka, J. (2006). The association of low back pain, neuromuscular imbalance, and trunk extension strength in athletes. Spine, 6 (6), 673–683. Sanchis-Moysi, J., Idoate, F., Dorado, C., Alayon, S., & Calbet, J. A. L. (2010). Large asymmetric hypertrophy of rectus abdominis muscle in professinal tennis players. PLoS ONE, 5 (12), e15858. Sanchis-Moysi, J., Idoate, F., Izquierdo, M., Calbet, J. A. L., & Dorado, C. (2011). Iliopsoas and gluteal muscles are asymmetric in tennis but not in soccer players. PLoS ONE, 6 (7), e22858. Sanchis-Moysi, J., Idoate, F., Serrano-Sanchez, J. A., Dorado, C., & Calbet, J. A. (2012). Muscle hypertrophy in prepubescent tennis players: A segmentation MRI study. PLoS ONE, 7 (3), e33622. Tesh, K. M., Dunn, J. S., & Evans, J. H. (1987). The abdominal muscles and vertebral stability. Spine, 12 (5), 501–508. Verspeelt, P. (1995). A review of tennis related injuries in ﬂemish high-level tennis players. In H. Krahl, H. G. Pieper, W. B. Kibler, and P. Renstrom (Eds.), Tennis: Sports Medicine and Science (pp. 47–51). Dusseldorf: Rau-Verlag. Walden, M., Hagglund, M., & Ekstrand, J. (2005). UEFA Champions League study: A prospective study of injuries in professional football during the 2001–2002 season. British Journal of Sports Medicine, 39 (8), 542–546. Downloaded by [Univ Degli Studi di Verona] at 11:49 23 May 2013