Regional variability in secondary remodeling within long bone cortices of catarrhine primates: the influence of bone growth history

Abstract

Secondary intracortical remodeling of bone varies considerably among and within vertebrate skeletons. Although prior research has shed important light on its biomechanical significance, factors accounting for this variability remain poorly understood. We examined regional patterning of secondary osteonal bone in an ontogenetic series of wild-collected primates, at the midshaft femur and humerus of Chlorocebus (Cercopithecus) aethiops ( n = 32) and Hylobates lar ( n = 28), and the midshaft femur of Pan troglodytes ( n = 12). Our major objectives were: 1) to determine whether secondary osteonal bone exhibits significant regional patterning across inner, mid-cortical and outer circumferential cortical rings within cross-sections; and if so, 2) to consider the manner in which this regional patterning may reflect the influence of relative tissue age and other circumstances of bone growth. Using same field-of-view images of 100-μ m-thick cross-sections acquired in brightfield and circularly polarized light microscopy, we quantified the percent area of secondary osteonal bone (%HAV) for whole cross-sections and across the three circumferential rings within cross-sections. We expected bone areas with inner and middle rings to exhibit higher %HAV than the outer cortical ring within cross-sections, the latter comprising tissues of more recent depositional history. Observations of primary bone microstructural development provided an additional context in which to evaluate regional patterning of intracortical remodeling. Results demonstrated significant regional variability in %HAV within all skeletal sites. As predicted,%HAV was usually lowest in the outer cortical ring within cross-sections. However, regional patterning across inner vs. mid-cortical rings showed a more variable pattern across taxa, age classes, and skeletal sites examined. Observations of primary bone microstructure revealed that the distribution of endosteally deposited bone had an important influence on the patterning of secondary osteonal bone across rings. Further, when present, endosteal compacted coarse cancellous bone always exhibited some evidence of intracortical remodeling, even in those skeletal sites exhibiting comparatively low %HAV overall. These results suggest that future studies should consider the local developmental origin of bone regions undergoing secondary remodeling later in life, for an improved understanding of the manner in which developmental and mechanical factors may interact to produce the taxonomic and intraskeletal patterning of secondary bone remodelling in adults.

Mapping human long bone compartmentalisation during ontogeny: A new methodological approach

“…The use of affine techniques, such as those used by geologists in mineral research, can enrich the analysis: (i) the use of polarised light (linear or circular) combined with a quartz wedge (Schultz, 1999(Schultz, , 2001Chinsamy, 2005) allows for the assessment of the changes in the collagen fibre orientation (Bromage et al, 2003;Goldman et al, 2009); and (ii) mineral composition and bone crystallinity analyses (i.e., spectroscopy) can corroborate if the differences observed in the histology description are correlated to the mineral content and crystal configuration during ontogeny. Finally, the images obtained by microscope are assembled and studied using manual or semi-manual methods (McFarlin, 2006;McFarlin et al, 2008) or computer-aided methods that helps to interpret large numbers of images (Shamir et al, 2010), or the images can be automatically analysed using specialised software (Girondot and Laurin, 2003).…”

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

“…The consistency of these findings with respect to the primate and nonprimate bones suggests that the ''interspecies differences'' that tend to preclude comparative histological analyses in anthropological studies (e.g., comparing primate with artiodactyl bone) may be less restrictive in the context of these characteristics. 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).…”

“…Osteon-and CFO-related measurements are finding increased use in studies that are aimed at inferring load history in bones or bone regions that are not amenable to in vivo strain measurement, including primate bones (Skedros and Kuo, 1999;Kalmey and Lovejoy, 2002;Goldman et al, 2003Goldman et al, , 2009Skedros et al, , 2007bMcFarlin et al, 2008). As discussed in our recent study (Skedros et al, 2009), these correlative studies are couched in perspective of experimental biomechanical data showing that regional concentrations of specific osteon morphotypes and/or regional variations in predominant CFO are, independent of the mere presence of osteons, important for conferring mechanical ''toughness'' for nonuniform strain distributions (Riggs et al, 1993a,b;Hiller et al, 2003;Bigley et al, 2006;Skedros et al, 2006).…”

“…Additional studies are needed to determine the influences that the more reliable characteristicsosteon MTSs and CFO/WMGL-have in affecting tissue mechanical properties of bone at a local level in additional contexts, including growth, aging, and metabolic stress. Investigations are also needed to determine if osteon MTSs and/or CFO/WMGL are potentially more revealing in studies where osteon density and related non-MTS or non-CFO/WMGL data have failed to show correlations with load history in the bones of humans and other primates (Drapeau and Streeter, 2006;Pfeiffer et al, 2006;McFarlin et al, 2008;Britz et al, 2009;Mulhern and Ubelaker, 2009).…”

“…Published 2010 The microstructure of limb bone shafts has been extensively scrutinized over the past few decades, with a major goal in physical anthropology of finding histological correlates of local load history (e.g., osteon density) that can be applied to the fossil record or to bones that are not amenable to in vivo strain measurement. For example, studies in physical anthropology that are aimed at identifying regional histological adaptation in diaphyses of limb bones often rely on correlation analyses between specific microstructural/ultrastructural characteristics and strain-related characteristics of load history at a local level (e.g., between different bones of the same skeleton or between anterior and posterior cortices of the same transverse section at mid-diaphysis) (Abbott et al, 1996;Kalmey and Lovejoy, 2002;Skedros et al, , 2006Drapeau and Streeter, 2006;Pfeiffer et al, 2006;Ural and Vashishth, 2006;McFarlin et al, 2008). An important advance in studies of osteonal bone adaptation is the identification of regional variations in the population densities of specific types of secondary osteons (Haversian systems) that can significantly influence local mechanical properties (Hiller et al, 2003;Bigley et al, 2006).…”