Secondary osteons scale allometrically in mammalian humerus and femur

Abstract

Intra-cortical bone remodelling is a cell-driven process that replaces existing bone tissue with new bone tissue in the bone cortex, leaving behind histological features called secondary osteons. While the scaling of bone dimensions on a macroscopic scale is well known, less is known about how the spatial dimensions of secondary osteons vary in relation to the adult body size of the species. We measured the cross-sectional area of individual intact secondary osteons and their central Haversian canals in transverse sections from 40 stylopodal bones of 39 mammalian species (body mass 0.3–21 000 kg). Scaling analysis of our data shows that mean osteonal resorption area (negative allometry, exponent 0.23,R2 0.54,p<0.005) and Haversian canal area (negative allometry, exponent 0.31,R2 0.45,p<0.005) are significantly related to body mass, independent of phylogeny. This study is the most comprehensive of its kind to date, and allows us to describe overall trends in the scaling behaviour of secondary osteon dimensions, supporting the inference that the osteonal resorption area may be limited by the need to avoid fracture in smaller mammalian species, but the need to maintain osteocyte viability in larger mammalian species.

Limb bone scaling in hopping macropods and quadrupedal artiodactyls

“…The lack of differential cross-sectional scaling in the macropod hindlimb despite their hopping behaviour led us to the speculation that their bones might have enhanced fatigue damage repair by increased remodelling, thus reducing the need for extra bone mass. We failed to find secondary osteonal remodelling in a Macropus giganteus femur sample, which was somewhat unusual for an animal of 33kg body mass [76]. Absence of secondary osteons may relate to the single sample failing to include any by chance, a load-related suppression of remodelling protecting bone from local weakening due to osteoclastic resorption [57], or infilling of existing osteons as occurs in horses after moderate-intensity training [77].…”

“…The current and other studies of bone organ allometry assume no size-related variation in bone microstructure or physiology and that all mammalian bone has similar biomechanical and mechanobiological behavior. Our recent work demonstrated that secondary osteons are wider in larger animals and narrower in smaller animals [76], and that trabeculae are thicker and more widely spaced in larger animals [78] indicating that biophysical constraints or cellular behaviour may vary among mammals and potentially interact with whole-bone-level scaling. Integration of macro-and micro-level perspectives in future scaling studies could be particularly informative.…”

Limb bone scaling in hopping macropods and quadrupedal artiodactyls

“…The lack of differential cross-sectional scaling in the macropod hindlimb despite their hopping behaviour led us to the speculation that their bones might have enhanced fatigue damage repair by increased remodelling, thus reducing the need for extra bone mass. We failed to find secondary osteonal remodelling in a Macropus giganteus femur sample, which was somewhat unusual for an animal of 33 kg body mass [ 77 ]. The absence of secondary osteons may relate to the single sample failing to include any by chance, a load-related suppression of remodelling protecting bone from local weakening due to osteoclastic resorption [ 59 ], or infilling of existing osteons as occurs in horses after moderate-intensity training [ 78 ].…”

“…The current and other studies of bone organ allometry assume no size-related variation in bone microstructure or physiology and that all mammalian bone has similar biomechanical and mechanobiological behaviour. Our recent work demonstrated that secondary osteons are wider in larger animals and narrower in smaller animals [ 77 ], and that trabeculae are thicker and more widely spaced in larger animals [ 79 ], indicating that biophysical constraints or cellular behaviour may vary among mammals and potentially interact with whole-bone level scaling. Integration of macro- and micro-level perspectives in future scaling studies could be particularly informative.…”

Modeling Rare Bone Diseases in Animals

“…While osteon-like structures can occasionally be observed in mice and rats, these structures lack the organization seen in larger vertebrates. A recent study has shown that osteon size positively correlates with body mass in mammals and suggested that the lack of clear osteons in small mammals may be related to the need to avoid fractures (56). Be that as it may, dysregulation of Haversian remodeling, such as may occur with aging, remains difficult to study in rodents (57).…”