Analysis of a tension/compression skeletal system: Possible strain‐specific differences in the hierarchical organization of bone

Abstract

Examination of a simple skeletal cantilevered beam-like bone (artiodactyl calcaneus) suggests that regional differences in strain magnitude and mode (tension vs. compression) reflect regional adaptation in the structural/material organization of bone. The artiodactyl (e.g., sheep and deer) calcaneus has a predominant loading condition typified by the unambiguous presence of prevailing compressive and tensile strains on opposite cortices. Bone habitually loaded in bending may accommodate regional disparities in loading conditions through modifications of various aspects of its organization. These include overall bone build (gross size and shape), cross-sectional shape, cortical thickness, and mineral content. Cross-sections taken along the calcaneal body exhibited cranial-caudal elongation with the compression (cranial) cortex thicker than the tension cortex (P < 0.01). Mineral content (ash fraction) was significantly greater in the compression cortex (P < 0.01), averaging 6.6% greater than in the tension cortex. Strong positive correlations were found between mineral content and section location in both the tension (r2 = 0.955) and compression (r2 = 0.812) cortices. These correlations may reflect functional adaptations to the linear increases in stress that are known to occur in the distal-to-proximal direction in simple, unidirectionally loaded cantilevered beams. According to engineering principles, the roughly triangular transverse cross-sectional geometries and thicker compression cortex are features consistent with a short cantilevered structure designed to resist unidirectional bending. Known differences in mechanical properties of bone in tension vs. compression suggest that these regional differences in cortical thickness and mineralization may be related to differences in strain mode. These structural/material dissimilarities, however, may be related to regional variations in strain magnitude, since bending and axially directed stresses in a simple cantilevered structure produce greater strain magnitudes in the compression domain. It is possible that the superimposed habitual strain magnitudes enhance strain-mode-specific adaptive responses. We hypothesize that these structural/material differences reflect the capacity of bone to process local information and produce a regionally heterogeneous organization that is appropriate for prevailing loading conditions.