Mammalian cortical bone in tension is non-Haversian

Abstract

Cortical bone, found in the central part of long bones like femur, is known to adapt to local mechanical stresses. This adaptation has been linked exclusively with Haversian remodelling involving bone resorption and formation of secondary osteons. Compared to primary/plexiform bone, the Haversian bone has lower stiffness, fatigue strength and fracture toughness, raising the question why nature prefers an adaptation that is detrimental to bone's primary function of bearing mechanical stresses. Here, we show that in the goat femur, Haversian remodelling occurs only at locations of high compressive stresses. At locations corresponding to high tensile stresses, we observe a microstructure that is non-Haversian. Compared with primary/plexiform bone, this microstructure's mineralisation is significantly higher with a distinctly different spatial pattern. Thus, the Haversian structure is an adaptation only to high compressive stresses rendering its inferior tensile properties irrelevant as the regions with high tensile stresses have a non-Haversian, apparently primary microstructure.

Utility of osteon circularity for determining species and interpreting load history in primates and nonprimates

“…This preferential adaptation for shear strains has been called the "shear resistance-priority hypothesis," which is based on the relatively deficient mechanical properties of bone loaded in shear when compared with tension and compression (Skedros, 2012;Skedros et al, 2015). This is an important consideration; attempts at correlating load history with regional variations in histomorphological characteristics (i.e., between regions of the same cross-section) may be unsuccessful if it is anticipated that unidirectional bending is sufficient for evoking regional differences in matrix adaptations when the habitual loading is actually much more complex (i.e., shear strains are prevalent and diffusely distributed; Figure 1; Goldman et al, 2003;Havill et al, 2013;Mayya et al, 2013;Skedros, 2012;Skedros et al, 2015). In other words, the shear-related histomorphological adaptations in these bones do not exhibit the more obvious marked regional variations in the matrix ultrastructural anisotropy (e.g., predominant CFO) seen in bones that receive habitual bending.…”

Understanding the structure–property relationship in cortical bone to design a biomimetic composite

“…The difference in the microstructure unravels the question of the different mechanical responses shown by different samples. This is an experimental proof of the adaptation of bone microstructure to the local mechanical stresses, already proposed by other authors [63].…”

“…The changes in the mechanical response are due to a change in the microstructure. Indeed, as previously shown in [63], bone microstructure varies in the cross section and along the femur length, and this represents an adaptation to local mechanical stimuli. In particular, the Haversian structure is thought to be an adaptation to high compressive stresses.…”

Splitting fracture in bovine bone using a porosity-based spring network model

“…However, several studies have used dry bone properties as an indicator for comparative bone quality considering that the testing methodologies for dry bone are significantly simpler [49 -52]. In the optical micrograph of the longitudinal face, shown in figure 1b, layers of woven bone were present between arrays of primary osteons that is typical of plexiform bone [14,25,31].…”

“…On the contrary, in cortical/compact bone, Haversian microstructure has higher porosity than plexiform bone [29,30], yet has higher compressive strength [25,30]. Furthermore, it has been recently argued that plexiform bone is remodelled into Haversian bone only in regions where the bone experiences high compressive stresses [25,31]. If indeed the plexiform bone is unsuitable for bearing compressive loads, the structure and arrangements of its pores, and not just the mean porosity, must be playing a crucial role in the failure process under compression.…”