Ontogenetic structural and material variations in ovine calcanei: A model for interpreting bone adaptation

Abstract

Experimental models are needed for resolving relative influences of genetic, epigenetic, and nonheritable functionally induced (extragenetic) factors in the emergence of developmental adaptations in limb bones of larger mammals. We examined regional/ontogenetic morphologic variations in sheep calcanei, which exhibit marked heterogeneity in structural and material organization by skeletal maturity. Cross-sections and lateral radiographs of an ontogenetic series of domesticated sheep calcanei (fetal to adult) were examined for variations in biomechanically important structural (cortical thickness and trabecular architecture) and material (percent ash and predominant collagen fiber orientation) characteristics. Results showed delayed development of variations in cortical thickness and collagen fiber orientation, which correlate with extragenetic factors, including compression/tension strains of habitual bending in respective dorsal/plantar cortices and load-related thresholds for modeling/remodeling activities. In contrast, the appearance of trabecular arches in utero suggests strong genetic/epigenetic influences. These stark spatial/temporal variations in sheep calcanei provide a compelling model for investigating causal mechanisms that mediate this construction. In view of these findings, it is also suggested that the conventional distinction between genetic and epigenetic factors in limb bone development be expanded into three categories: genetic, epigenetic, and extragenetic factors.

Ontogeny of material stiffness heterogeneity in the macaque mandibular corpus

“…The hypothesis that the pattern of bending is associated with differences in elastic modulus as a consequence of functional adaptation (Skedros et al, 2004(Skedros et al, , 2007 is consistent with our data. This agreement is subject to a number of qualifications, however.…”

“…The second aspect of the calcaneal model (Skedros et al, 2004(Skedros et al, , 2007 of interest is the prediction that spatial heterogeneity will be an effect of age as a result of load history. As regional differences in elastic modulus seem to be largely insensitive to age (but not altogether independent of it), macaque mandibles do not appear to conform to this prediction, although the finding that the rank-ordering of modulus across regions becomes significantly consistent only in adults offers indirect support for the idea that the accumulation of a stress history ultimately conditions the spatial distribution of bone stiffness.…”

“…What limited comparative data there are on the stiffness of primate craniofacial bone suggests that scaling is not the predominant factor underlying interspecific variation in bone material properties, including elastic modulus . Skedros et al (2004Skedros et al ( , 2007 offer an ontogenetic model of bone adaptation that predicts changes in material stiffness are correlated with repetitive and predictable loading patterns. Under this rationale, we expect to see greater stiffness in older individuals as well as greater spatial heterogeneity in stiffness.…”

Mechanical properties of porcine femoral cortical bone measured by nanoindentation

“…Mineralized collagen fibrils, consisting of hydroxyapatite crystals and collagen molecules, are bone's building blocks. Very young bone tissue displays a woven structure, with fibrils showing no preferential orientation (Currey, 2002;Riggs et al, 1993;Skedros et al, 2007). As the bone matures, the woven bone changes to a lamellar bone with an organized lamellar appearance (Currey, 2002;Ross and Pawlina, 2006).…”

A weighted osteon morphotype score outperforms regional osteon percent prevalence calculations for interpreting cortical bone adaptation

“…Although there are examples where CFO/ WMGL analyses have been shown to be useful for predicting strain-mode distributions of habitual bending when secondary osteons are few or absent (Mason et al, 1995;, this method (typically) and the osteon morphotype scoring method (definitely) cannot be used in studies of bone adaptation during phases of growth or in some species or bones where osteon remodeling is infrequent or nonexistent McFarlin et al, 2008;Mulhern and Ubelaker, 2009). In other words, unlike CFO/WMGL analyses, osteon morphotype scoring is only reliable for detecting regional adaptation for bending when it is used in cases where the bone is sufficiently remodeled with secondary osteons (Riggs et al, 1993b;Skedros et al, 2007a).…”