Dissociation of mineral and collagen orientations may differentially adapt compact bone for regional loading environments: Results from acoustic velocity measurements in deer calcanei

In limb bone diaphyses, it is hypothesized that collagen and extra-fibrillar mineral are aligned differently in relatively simple loading conditions (e.g., habitual longitudinal compression) when compared to complex or potentially deleterious strain environments (e.g., habitual shear or tension). These putative differences in collagen/mineral organization might be adaptations that enhance toughness and fatigue resistance by controlling the direction of microdamage propagation. This study examined relationships between the non-uniform strain distribution of wild deer calcanei and elastic anisotropy of cortical bone specimens in three preparations: (1) demineralized (collagen only), (2) deproteinized (mineral only), and (3) untreated. Using simulated functional loading, the following strain data were obtained from the dorsal “compression”, plantar “tension”, and medial and lateral (“neutral axis”) cortices of one calcaneus of each of seven pairs: (1) peak strain magnitude, (2) prevalent/predominant strain mode (compression, tension, shear), and (3) principal strain orientation with respect to the bone’s long axis. In the contralateral calcanei, elastic anisotropy ratios (ARs) were calculated using acoustic velocity (longitudinal and transverse) measurements from a pair of orthogonally sliced specimens (representing each of three preparation types) from each cortex. In a separate set of seven adult calcanei, predominant collagen fiber orientation (CFO) was measured using circularly polarized light (CPL) in the four cortical locations. Results showed that, in general, elastic anisotropy was significant in each region, with ARs being significantly different from isotropy (where AR = 1.0). Compared to CFO, mineral orientation more strongly influenced this anisotropy, which was most notable in the plantar “tension” cortex. High correlations (r values from −0.675 to −0.734, P < 0.05) were found between collagen anisotropy obtained from acoustic data when compared to the CPL data. Significant correlations of mineral and collagen anisotropy were also found between strain mode, magnitude, and orientation (all r values −0.750). The habitual compression, tension, and shear (neutral axis) regions also had different collagen/mineral organizations, which may be important in accommodating the well-known disparity in the mechanical properties of bone in these loading modes.