Relationships of loading history and structural and material characteristics of bone: Development of the mule deer calcaneus

Abstract

If a bone's morphologic organization exhibits the accumulated effects of its strain history, then the relative contributions of a given strain stimulus to a bone's development may be inferred from a bone's hierarchical organization. The artiodactyl calcaneus is a short cantilever, loaded habitually in bending, with prevalent compression in the cranial (Cr) cortex, tension in the caudal (Cd) cortex, and shear in the medial and lateral cortices (i.e., neutral axis). Artiodactyl calcanei demonstrate unusually heterogeneous structural and material organization between these cortices. This study examines potential relationships between developmental morphologic variations and the functional strain distribution of the deer calcaneus. One calcaneus was obtained from each of 36 (fetus to adult) wild deer. Predominant collagen fiber orientation (CFO), microstructural characteristics, mineral content (% ash), and geometric parameters were determined from transversely cut segments. Radiographs were examined for arched trabeculae, which may reflect tension/compression stress trajectories. Results showed that cross-sectional shape changes with age from quasi-circular to quasi-elliptical, with the long axis in the cranial-caudal direction of habitual bending. Cranial ("compression") cortical thickness increased at a greater rate than the Cd ("tension") cortex. Fetal bones exhibited arched trabeculae. Percent ash was not uniform (Cr > Cd), and this disparity increased with age (absolute differences: 2.5% fetuses, 4.3% adults). Subadult bones showed progressively more secondary osteons and osteocyte lacunae in the Cr cortex, but the Cd cortex tended to have more active remodeling in the subadult and adult bones. Nonuniform Cr:Cd CFO patterns first consistently appear in the subadults, and are correlated with secondary bone formation and habitual strain mode. Medial and lateral cortices in these groups exhibited elongated secondary osteons. These variations may represent "strain-mode-specific" (i.e., tension, compression, shear) adaptations. The heterogeneous organization may also be influenced by variations in longitudinal strain magnitude (highest in the Cr cortex) and principal strain direction-oblique in medial-lateral cortices (where shear strains also predominate). Other factors such as local reductions in longitudinal strain may influence the increased remodeling activity of the Cd cortex. Some structural variations, such as arched trabeculae, that are established early in ontogeny may be strongly influenced by genetic- or epigenetic-derived processes. Material variations, such as secondary osteon population densities and CFO, which appear later, may be products of extragenetic factors, including microdamage.

Ontogeny of bone strain: the zygomatic arch in pigs

“…Like infant limb bones (Biewener and Bertram, 1994;Main and Biewener, 2004;Skedros et al, 2004), piglet zygomatic arches were straighter and rounder than those of juveniles. This geometry undoubtedly contributed to the high intra-and interindividual variability we observed in bone strain, because the bending direction of a straight cylinder is more sensitive to slight variations in loading direction than that of a curved cylinder or a beam (Bertram and Biewener, 1988).…”

“…The exceptionally high strains that were produced by stimulation of relatively small (Herring and Wineski, 1986) muscles suggest that, like infant long bones (Carrier and Leon, 1990;Heinrich et al, 1999;Skedros et al, 2004), piglet arches have low stiffness. Indeed, the entire piglet skull is probably relatively compliant, as indicated by the substantial strains produced on the arch by a distant load, the contralateral masseter.…”

“…In long bones and the mandible, ovate cross sections and curvatures develop in relation to mechanical loading from muscle contraction and weight bearing (Lanyon, 1980;Hall and Herring, 1990;Biewener and Bertram, 1994;Skedros et al, 2004). The growth changes in the zygomatic bone are clearly adaptive for the parasagittal-plane bending that predominated in older animals but was not seen during function in the piglets.…”

“…Thus, variable, unpredictable and potentially large bone strains could be encountered. The fact that infant limb bones are typically straighter and rounder than adult bones (Biewener and Bertram, 1994;Main and Biewener, 2004;Skedros et al, 2004) also suggests a less predictable loading environment (Bertram and Biewener, 1988). Higher variability in strain of younger animal limb bones has, in fact, been documented (Main and Biewener, 2004).…”

Characterization of the Spatial Arrangement of Secondary Osteons in the Diaphysis of Equine and Canine Long Bones

“…Newly formed osteons are defined as osteons, which are still poorly mineralized, as seen in backscattered electron images (Skedros et al, 2001). In the mature cortex of the deer's calcaneus the cortices under tension showed a greater number of newly formed osteons compared with the cortices under compression (Skedros et al, 2001;Skedros et al, 2004). A second class of osteons is that of ''atypical'' osteons, which include osteons with a noncentrally located canal, with a strongly elongated canal or even including more than one canal.…”