The ‘muscle-bone unit’ during the pubertal growth spurt
Introduction
It has been known for more than three decades that muscle mass and bone mass are closely associated [1]. More recently, analogous correlations have been found by using densitometric surrogate measures of muscle mass (lean body mass, LBM) and bone mass (bone mineral content, BMC). The correlation between these two parameters is especially close during growth and development [2], [3], [4], [5], [6]. It has also been observed that the sequence of timing for peak accrual in the soft tissues and BMC is similar in both sexes [7].
Mechanostat theory postulates that the statistical association between LBM and BMC reflects a direct cause-and-effect relationship [8], [9]. According to this hypothesis, the skeleton continually adapts its strength to the loads to which it is exposed to keep bone deformation within safe limits. The largest physiological loads on the skeleton result from muscle contraction, which puts several fold larger stresses on the skeleton than the simple effect of gravity [10], [11]. Mechanostat theory therefore predicts that the increasing muscle mass (and thus muscle force) during development creates the stimulus for the increase in bone mass (and thus in bone strength).
Although mechanostat theory primarily is an attempt to explain bone physiology and pathophysiology, its conclusions have direct implications on how bone disorders in children are assessed and treated. If muscle forces drive bone development, then analyses of muscle function should be added to the armamentarium of clinicians diagnosing bone disorders. Many bone disorders may at least partly be due to muscle disuse or dysfunction, opening a new field of potential targets for therapeutic interventions [12]. Given these far-reaching implications of mechanostat theory, it is important to evaluate it from as many different angles as possible.
If muscle force during development really drives bone strength as mechanostat theory postulates, then the increase in muscle development must precede and should determine the increase in BMC. Examining the adolescent growth spurts in lean and bone tissue provides a model to test this hypothesis in healthy children. The maximal rates of LBM and BMC accretion during this period can serve as markers to establish the temporal sequence of developmental events. In this longitudinal study, we therefore investigated the relationship between pubertal peak velocity in lean body mass accretion (PVLBM) and peak velocity in bone mineral content accretion (PVBMC). For comparison, peak height velocity (PHV) was also analyzed, as this is a well-established marker of pubertal events.
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Subjects
All subjects were participants in the University of Saskatchewan Pediatric Bone Mineral Study. Of 375 eligible students attending two elementary schools in Saskatoon, Canada, 113 boys and 115 girls, ranging in age from 8 to 14 years, were initially enrolled in this multiyear longitudinal study. Height and weight were taken on all subjects every 6 months. Dual-Energy X-ray Absorptiometry (DXA) scans were performed annually.
Only those subjects who clearly showed a peak in their height and BMC
Results
PHV preceded the peak in total body LBM by an average of 0.39 (SD 0.57) years in girls and by 0.30 (SD 0.49) years in boys (Fig. 1; Table 1). The peak in total body PVLBM preceded the peak in total body PVBMC (P < 0.001 in both sexes) by an average of 0.51 (SD 0.47) years in girls and by 0.36 (SD 0.47) years in boys. Total body PVLBM occurred before total body PVBMC in 59 (87%) of the girls and in 54 (77%) of the boys. A multiple regression model that tested sex, PHV, and total body PVLBM as
Discussion
In this study, we compared the maximal accretion rates for a marker of muscle force (LBM) and a surrogate measure of bone strength (BMC). Both at the level of the entire body and in the upper and lower extremities, the maximal rate of LBM accrual occurred a few months before the maximal increase in BMC, and the peak rates of change in these two measures were closely correlated. These observations are in accordance with the postulate from mechanostat theory that the increase in muscle force
Acknowledgements
This work was supported in part by a grant from the National Health Research and Development Program, Health Canada (D.A.B.) and by the Shriners of North America (F. R.).
References (20)
- et al.
Relation between bone mass and muscle weight
Lancet
(1970) - et al.
Influence of body composition on bone mineral content in children and adolescents
Am. J. Clin. Nutr.
(1996) Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample
Bone
(2003)- et al.
Regional and total body bone mineral content, bone mineral density, and total body tissue composition in children 8–16 years of age
Calcif. Tissue Int.
(1993) - et al.
Determinants of bone mass in 10- to 26-year-old females: a twin study
J. Bone Miner. Res.
(1995) - et al.
Lean body mass and leg power best predict bone mineral density in adolescent girls
Med. Sci. Sports Exerc.
(1999) - et al.
Lean mass and physical activity as predictors of bone mineral density in 16–20-year old women
J. Intern. Med.
(1999) - et al.
Timing and magnitude of peak height velocity and peak tissue velocities for early, average, and late maturing boys and girls
Am. J. Human Biol.
(2001) Muscle, bone, and the Utah paradigm: a 1999 overview
Med. Sci. Sports Exerc.
(2000)- et al.
The developing bone: slave or master of its cells and molecules?
Pediatr. Res.
(2001)
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