Elsevier

Bone

Volume 37, Issue 4, October 2005, Pages 457-466
Bone

Bone geometry in response to long-term tennis playing and its relationship with muscle volume: A quantitative magnetic resonance imaging study in tennis players

https://doi.org/10.1016/j.bone.2005.05.014Get rights and content

Abstract

The benefit of impact-loading activity for bone strength depends on whether the additional bone mineral content (BMC) accrued at loaded sites is due to an increased bone size, volumetric bone mineral density (vBMD) or both. Using magnetic resonance imaging (MRI) and dual energy X-ray absorptiometry (DXA), the aim of this study was to characterize the geometric changes of the dominant radius in response to long-term tennis playing and to assess the influence of muscle forces on bone tissue by investigating the muscle–bone relationship. Twenty tennis players (10 men and 10 women, mean age: 23.1 ± 4.7 years, with 14.3 ± 3.4 years of playing) were recruited. The total bone volume, cortical volume, sub-cortical volume and muscle volume were measured at both distal radii by MRI. BMC was assessed by DXA and was divided by the total bone volume to derive vBMD. Grip strength was evaluated with a dynamometer. Significant side-to-side differences (P < 0.0001) were found in muscle volume (+9.7%), grip strength (+13.3%), BMC (+13.5%), total bone volume (+10.3%) and sub-cortical volume (+20.6%), but not in cortical volume (+2.6%, ns). The asymmetry in total bone volume explained 75% of the variance in BMC asymmetry (P < 0.0001). vBMD was slightly higher on the dominant side (+3.3%, P < 0.05). Grip strength and muscle volume correlated with all bone variables (except vBMD) on both sides (r = 0.48–0.86, P < 0.05–0.0001) but the asymmetries in muscle parameters did not correlate with those in bone parameters. After adjustment for muscle volume or grip strength, BMC was still greater on the dominant side. This study showed that the greater BMC induced by long-term tennis playing at the dominant radius was associated to a marked increase in bone size and a slight improvement in volumetric BMD, thereby improving bone strength. In addition to the muscle contractions, other mechanical stimuli seemed to exert a direct effect on bone tissue, contributing to the specific bone response to tennis playing.

Introduction

Impact-loading activity is now considered as an effective strategy to improve bone health. The skeletal sites which are submitted to mechanical stimuli display greater values of bone mineral content than the unloaded sites, as demonstrated by dual energy X-ray absorptiometry (DXA) data [1], [2]. Recently, it has been shown that weight bearing activities were associated with higher bone mineral density when they induced high impacts (volleyball, hurdling) rather than low impacts (orienteering, cross-country skiing) [3]. This observation has been reinforced by the comparison of the dominant and nondominant upper limbs in tennis or squash players [4], [5], [6], [7], [8], [9], [10], [11]. Tennis strokes provoke repetitive mechanical strains in the dominant forearm, due to racket vibrations [12], torsional forces [13] and muscle contractions [14]. Additionally, studying unilateral activities enables an elimination of the confounding effects of genetic, hormonal and nutritional factors.

Bone mineral accrual affects bone mechanical strength. The magnitude of the change in bone strength depends partly on whether the “extra” bone mineral content is associated with an increase in bone size, volumetric bone mineral density (vBMD) or both. The gain in bone resistance to compressive, bending or torsional loads is indeed more pronounced when the new added mineral mass is placed further from the neutral axis of the bone, inducing an increase in bone size [15], [16], [17], [18].

In the past 10 years, most of the human studies dealing with bone and exercise were based on DXA data. Nevertheless, estimating bone volume requires three-dimensional techniques. The use of peripheral quantitative computed tomography (pQCT) made a breakthrough in the understanding of the bone response to mechanical loading. By its capacity to measure both bone mineral content and three-dimensional bone geometry at appendicular sites, this device gave the opportunity to assess vBMD. Mechanical loading has been shown to exert a limited effect on cortical vBMD in long bone diaphyses, the effect being slightly negative [19], [20] or not significant [20], [21], [22] whereas loading induced a clear positive effect on trabecular vBMD in long bone epiphyses [19], [22], [23]. The greatest changes in gross geometry were found in long bone diaphyses, where a marked increase in total bone cross-sectional area was observed [19], [20], [23].

Muscle forces have been proposed to be the largest voluntary loads to which bone has to adapt in order to keep its mechanical environment stable [24]. Understanding the muscle–bone relationship could certainly help to better describe the mechanisms by which bone responds to mechanical stimuli during physical activity.

With regard to this objective, magnetic resonance imaging (MRI) is a promising nonionizing 3D-technique. It has already been used to study the effects of growth [25], [26] or mechanical loading on bone geometry [27], [28], [29], as being a valid and reproducible method [30], [31]. The major advantage of MRI technology lies in its capacity to measure the cross-sectional area of both muscle and bone on multiple contiguous slices, and thus to study the muscle–bone interaction [29], [32]. DXA is considered as the gold standard method to determine bone mineral content. Combining the two techniques enables an estimate of vBMD, provided that DXA-derived bone mineral content and MRI-derived total bone volume are carefully measured on the same region of interest [33].

The objectives of this study were (1) to characterize the bone response to loading in terms of bone geometry and volumetric bone mineral density in young adults who started playing tennis prior to puberty, and (2) to assess the role of muscle forces in the bone response by investigating the muscle–bone relationship.

Section snippets

Subjects

Twenty regional-level tennis players (10 men and 10 women, all Caucasian) were recruited in the neighborhood of Orléans (France). Subjects comprised a sub-sample of volunteers from a larger study [34], who accepted to take part in a thorough analysis including MRI scanning. All were right-handed. They had been practicing tennis for 10 to 20 years, except one player who had experienced 7.4 years of practice. The subjects were still playing tennis at the time of the experiments and they took part

General descriptive characteristics of the subjects

The characteristics of the subjects are given in Table 1. The male subjects were significantly older, taller and heavier than their female counterparts (P < 0.05). No difference was found between men and women with regard to tennis playing history although a tendency was observed towards a longer tennis practice in male players.

Asymmetry between the dominant and nondominant forearm

In the whole sample, muscle volume, grip strength, BMC, total bone volume and sub-cortical volume were greater at the dominant radius than at its nondominant counterpart

Discussion

This study showed that long-term tennis players displayed a greater bone mass at the dominant distal radius, which was associated to a marked increase in bone size and a slight improvement in volumetric BMD.

The increase we found in BMC at the dominant distal radius was consistent with previous findings obtained by pQCT at the same site, values ranging from +12% to +14.7% [19], [20], [23]. In the present study, the asymmetry in total bone volume explains 75% of the variance in BMC asymmetry,

Acknowledgments

The authors are deeply grateful to the staff of the MRI department (Hospital of Orléans) for their technical assistance and precious help. We wish to thank S. Deval for providing the dedicated wrist coil. Special thanks to the subjects for their selfless contribution. This research was supported by a grant from the Region Centre and the Inserm (Institut National de la Santé Et de la Recherche Médicale).

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