Muscle Strength, Bone Mass, and Age-Related Bone Loss

Abstract

THE EFFECTS OF DISUSE, or conversely, of elevated physical activity on muscle strength and bone mass are well known. Disuse causes muscle wasting and bone loss; physical activity increases muscle strength and bone mass. The association between muscle strength and bone mass is therefore clearly established, although neither the dominant effect of muscle on bone mass, nor the cause and effect relationship is established by these simple correlations alone. Frost1 proposes that "voluntary muscle forces … dominate a bone's postnatal structural adaptations to mechanical usage, modified … by body weight and one's voluntary physical activity." Neither body weight nor physical activity is independent of muscle mass, but it is true that muscle forces place greater loads on bones than do gravitational forces associated with weight. This was shown theoretically nearly 50 years ago by Pauwels,2 and is easily deduced from a simple analysis of muscle pull and levers such as the one described by Frost. More recently, this has been demonstrated using experimental data from implanted hip prostheses.3 This analysis shows that >70% of the bending moments on a bone are transmitted by muscle force rather than body weight. Computational models employing finite elements together with the application of computer-aided optimization to predict femoral geometry during growth are unable to simulate the morphology of the femoral shaft without the addition of muscle forces.4 Application of various combinations of axial, bending, and torsional loading to a cylinder were not able to generate femoral diaphyseal morphology when compared with the cross-sectional geometry of real bones, but the introduction of adductor muscle forces in various combinations with these loadings did produce geometries comparable to observed femoral geometry. Therefore, based on the predictions of theoretical analyses and computational models, and based on supporting experimental data, it is well established that forces applied to bone are primarily the result of muscular contraction. To demonstrate that muscle force dominates skeletal adaptation requires that greater muscle mass/strength is associated with greater bone mass, independent of body size contributions. A multitude of studies have shown such correlations,5-9 but have not always demonstrated their independence from other body size measures.10 Schonau et al.,8 for example, show that as much as 76% of the variation in bone strength index in the distal radius can be explained by grip strength alone. However, high correlations between muscle strength/mass at one site and bone strength/mass at another unrelated site suggest that the relationship may be related to other confounding factors,11 or to stimuli that have independent effects on both systems.12 Myburgh et al.5 showed that 67% of the bending rigidity of the ulna can be explained by biceps strength, but the biceps has no attachment to the ulna and would not directly generate loads on the ulna. Likewise, muscle strength of the quadriceps and hamstring muscles independently predicts bone mineral density (BMD) of the humerus and spine.13 Inferences about the direct effect of muscle strength on bone adaptation based on such correlations are spurious. Still, there are studies that demonstrate that muscle strength has effects on bone mass or BMD that are independent of age, weight, height, or years of estrogen use.6,14,15 The effect of muscle strength on bone mass has been complicated somewhat by the failure to find correlations between muscle strength and bone mass in subjects with normal or even elevated bone density. In the hormonally replete adult, mechanostat theory16 predicts that once skeletal loading by muscle activity brings bone density to within the normal range, remodeling will be suppressed. Because modeling is inactive or slow in adults, higher bone masses will not be achieved. Consequently, correlations between muscle strength and BMD in active or athletic individuals are generally not high13,17,18 but are not expected to be. The absence of a correlation between muscle strength and bone mass in active subjects is not a sufficient argument against the idea that muscle force exerts a dominant effect over bone's structural adaptation. To demonstrate rigorously that voluntary muscle forces dominate the adaptation of bone it is necessary to show that a decline in muscle mass precedes a decline in bone strength under conditions of disuse or hormonal insufficiency, and conversely that muscle strength increases before bone mass under conditions of hypervigorous mechanical usage or the re-establishment of hormonal balance. The time course for the development of muscle weakness relative to bone loss following injury, and reversal of these trends subsequent to rehabilitation and recovery, recently was shown nicely during a "fortuitous" experiment in which a knee ligament rupture occurred during a strength training program.7 In this study, a healthy, phy