Physical activity when young provides lifelong benefits to cortical bone size and strength in men

Abstract

The skeleton shows greatest plasticity to physical activity-related mechanical loads during youth but is more at risk for failure during aging. Do the skeletal benefits of physical activity during youth persist with aging? To address this question, we used a uniquely controlled cross-sectional study design in which we compared the throwing-to-nonthrowing arm differences in humeral diaphysis bone properties in professional baseball players at different stages of their careers (n = 103) with dominant-to-nondominant arm differences in controls (n = 94). Throwing-related physical activity introduced extreme loading to the humeral diaphysis and nearly doubled its strength. Once throwing activities ceased, the cortical bone mass, area, and thickness benefits of physical activity during youth were gradually lost because of greater medullary expansion and cortical trabecularization. However, half of the bone size (total cross-sectional area) and one-third of the bone strength (polar moment of inertia) benefits of throwing-related physical activity during youth were maintained lifelong. In players who continued throwing during aging, some cortical bone mass and more strength benefits of the physical activity during youth were maintained as a result of less medullary expansion and cortical trabecularization. These data indicate that the old adage of "use it or lose it" is not entirely applicable to the skeleton and that physical activity during youth should be encouraged for lifelong bone health, with the focus being optimization of bone size and strength rather than the current paradigm of increasing mass. The data also indicate that physical activity should be encouraged during aging to reduce skeletal structural decay.

Keywords: exercise; intracortical remodeling; osteoporosis; peak bone mass.

Fig. 1.

Overhand throwing loads the humeral diaphysis, inducing skeletal adaptation. (A and B) Median (and median absolute deviation) cross-sectional tensile (A) and shear (B) strains in the humerus of the throwing arm of an MLB player toward the end of the cocking stage of a fastball pitch showed strains throughout the diaphysis. Both tensile and shear strains were increased when the same forces were applied to the collateral, nonthrowing humerus. (C) Cross-sectional distribution of peak tensile strain in the bilateral humerus demonstrated reduced strains in the throwing arm. (D) Reconstructed CT images of the bilateral humerii in a representative MLB/MiLB player demonstrated a more robust diaphysis with visibly broader diameter on the throwing side. (E) Cross-sectional images of the humerii in D revealed substantially greater total and cortical bone areas and cortical thickness and smaller medullary area in the throwing arm. (F) Throwing substantially increased torsional bone strength (indicated by density-weighted polar moment of inertia) along the entire diaphysis, with strength nearly doubled toward the distal diaphysis. Data show the mean percent difference and 95% CI (shaded area) between the throwing arm and the nonthrowing arm in throwers normalized to the differences between the dominant arm and the nondominant arm in controls (^‡P < 0.001, unpaired t test). (G) The distal diaphysis in throwers had a more circular cross-section than seen in controls, as indicated by a maximum:minimum (I_MAX:I_MIN) second moment of area ratio closer to 1 (*P < 0.05, ANCOVA with the contralateral arm as the covariate).

Fig. 2.

Physical activity-related mechanical loading during youth conferred lifelong benefits in cortical bone size and estimated strength but not in cortical bone mass. (A) Peripheral QCT images of the midshaft humerus in representative former throwers show increased medullary expansion and cortex trabecularization (arrows) in the throwing arm with increasing years of detraining but maintenance of loading effects on overall bone cross-sectional size. (B–I) Graphs show the maintenance of the effects of physical activity during youth on cortical volumetric bone mineral density (B); cortical bone mineral content (C); trabecular/subcortical bone mineral content (D); total cross-sectional area (E); cortical cross-sectional area (F); medullary cross-sectional area (G); cortical thickness (H); and density-weighted polar moment of inertia (I). Data show the mean difference and 95% CI between the throwing and nonthrowing arms in former throwers normalized to the differences between the dominant and nondominant arms in controls. CIs greater or less than 0% indicate differences between the throwing and nonthrowing arms in throwers that are greater or less, respectively, than the differences between the dominant and nondominant arms in controls (*P < 0.05, ^†P < 0.01 and ^‡P < 0.001, unpaired t test). Source data are provided in Table S3.

Fig. 3.

Continued physical activity during aging maintained a proportion of the benefits in bone mass and more of the benefits in bone strength induced during youth. (A) Peripheral QCT images of the midshaft humerii in representative individuals showed less medullary expansion and cortical trabecularization (arrows) in the throwing arm of the continuing thrower than in the throwing arm of the former thrower. (B) Cortical bone mineral content and density-weighted polar moment of inertia were greater in continuing throwers than in former throwers and controls; cortical thickness was greater in continuing throwers than in former throwers; and trabecular/subcortical bone mineral content and medullary area were smaller in continuing throwers than in former throwers. Data show the mean percent difference and 95% CI between the throwing arm and the nonthrowing arm in throwers normalized to the differences between the dominant arm and the nondominant arm in controls. CIs greater than 0% indicate greater differences between the throwing arm and the nonthrowing arm in throwers than between the dominant arm and the nondominant arm in controls (^†P < 0.01; ^‡P < 0.001); § indicates significant differences between continuing and former throwers (P < 0.05; one-way ANOVA with Tukey post hoc comparisons).