Elsevier

Bone

Volume 34, Issue 2, February 2004, Pages 281-287
Bone

The relationship between muscle size and bone geometry during growth and in response to exercise

https://doi.org/10.1016/j.bone.2003.11.009Get rights and content

Abstract

As muscles become larger and stronger during growth and in response to increased loading, bones should adapt by adding mass, size, and strength. In this unilateral model, we tested the hypothesis that (1) the relationship between muscle size and bone mass and geometry (nonplaying arm) would not change during different stages of puberty and (2) exercise would not alter the relationship between muscle and bone, that is, additional loading would result in a similar unit increment in both muscle and bone mass, bone size, and bending strength during growth. We studied 47 competitive female tennis players aged 8–17 years. Total, cortical, and medullary cross-sectional areas, muscle area, and the polar second moment of area (Ip) were calculated in the playing and nonplaying arms using magnetic resonance imaging (MRI); BMC was assessed by DXA. Growth effects: In the nonplaying arm in pre-, peri- and post-pubertal players, muscle area was linearly associated BMC, total and cortical area, and Ip (r = 0.56–0.81, P < 0.09 to < 0.001), independent of age. No detectable differences were found between pubertal groups for the slope of the relationship between muscle and bone traits. Post-pubertal players, however, had a higher BMC and cortical area relative to muscle area (i.e., higher intercept) than pre- and peri-pubertal players (P < 0.05 to < 0.01), independent of age; pre- and peri-pubertal players had a greater medullary area relative to muscle area than post-pubertal players (P < 0.05 to < 0.01). Exercise effects: Comparison of the side-to-side differences revealed that muscle and bone traits were 6–13% greater in the playing arm in pre-pubertal players, and did not increase with advancing maturation. In all players, the percent (and absolute) side-to-side differences in muscle area were positively correlated with the percent (and absolute) differences in BMC, total and cortical area, and Ip (r = 0.36–0.40, P < 0.05 to < 0.001). However, the side-to-side differences in muscle area only accounted for 11.8–15.9% of the variance of the differences in bone mass, bone size, and bending strength. This suggests that other factors associated with loading distinct from muscle size itself contributed to the bones adaptive response during growth. Therefore, the unifying hypothesis that larger muscles induced by exercise led to a proportional increase in bone mass, bone size, and bending strength appears to be simplistic and denies the influence of other factors in the development of bone mass and bone shape.

Introduction

Muscle and bone are inextricably linked by common genes regulating body size and a shared loading environment [1]. Growth, in the presence of unloading, results in both a bone that lacks the specific shape that is unique for its function and a muscle that lacks functional capacity [2]. Thus, while the development of muscle and bone during growth is influenced by gravitational forces associated with body weight and physical activity, it is proposed that forces produced by muscle contractions dominate the skeleton's postnatal structural adaptation to loading [3], [4], [5]. Therefore, as muscles become larger and stronger during growth or in response to increased loading (exercise), bones should adapt to increased loads imparted by muscles by adding mass, size, and strength [3]. This biomechanical link between muscle and bone supports the concept of a ‘functional muscle–bone unit’, in which changes in muscle mass and strength should affect bone mass, size, and strength predictably and correspondingly [2]. While this concept of a ‘muscle–bone unit’ is supported by indirect evidence, there is little direct evidence to support the notion that an exercise-induced increment in muscle size and strength are associated with the adaptive response of the skeleton to loading during growth. The aim of this study was to investigate the relationship between muscle and bone during different stages of growth and in response to additional loading. More specifically, in this unilateral model, we tested the hypothesis that (1) the relationship between muscle size and bone mass and geometry (nonplaying arm) would not change during different stages of puberty and (2) exercise would not alter the relationship between muscle and bone, that is, additional loading would result in a similar unit increment in both muscle and bone mass, bone size, and bending strength during growth.

Section snippets

Subjects

Forty-seven pre-, peri-, and post-pubertal competitive female tennis players aged 8–17 years were recruited from tennis clubs located within metropolitan Melbourne, Australia. Players were included if they had been playing competitive tennis for a minimum of 2 years, and were currently playing at least 3 h/week. Thirty-four players were competing at a national, state and regional level, and 13 at a high standard club level. Forty girls were right-handed, and 33 girls used a double-handed

Muscle–bone relationship during growth (nonplaying arm)

In this unilateral model, the nonplaying arm represents the relationship between muscle and bone as developed during growth in the presence of loading due to everyday living. At all stages of puberty, there was a linear relationship between muscle area and BMC, total, medullary and cortical area, and Ip (r = 0.56–0.81, P ranging 0.09 to < 0.001). These relationships remained after adjusting for age and humeral length. Despite a trend for the slopes of the relationship between muscle and bone

Discussion

Muscle and bone are inextricably linked by common genes regulating size, their physical connection, and the shared loading environment. Thus, it is often assumed that an increase in muscle mass and strength results in a corresponding increase in bone mass and strength [2], [5]. In this study, we report that an exercise-induced increment in muscle size during growth was positively correlated with changes in bone mass, size, and strength. However, the greater muscle size accounted for only 12–16%

Acknowledgements

The authors would like to thank radiographers Amanda Hunt and Glenn Rush for their technical assistance, and Rinske Miller for her assistance with the MRI analysis. The authors are grateful to Associate Professor Damien Jolley for his statistical advice and Dr Cameron Blimkie for his helpful comments and suggestions. We would also like to thank the players and their parents for their time contributions to the study.

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    This study was funded by grants from the Australian Research Council Grant and the School of Health Sciences, Deakin University.

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