The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone

Abstract

In cortical bone, regional variations in predominant collagen fiber orientation (CFO) and other histocompositional (material) characteristics may represent biomechanically important adaptations related to specific strain modes of tension, compression, or shear. For example, regions habitually loaded in compression have relatively more oblique-to-transverse collagen compared to regions loaded in tension, which have relatively more longitudinal collagen (Carando et al., 1991;Kalmey and Lovejoy, 2002;Mason et al., 1995;Riggs et al., 1993a;Skedros, 2001;Skedros and Kuo, 1999;Skedros et al., 1996). Standard material tests (conducted This study examined relative influences of predominant collagen fiber orientation (CFO), mineralization (% ash), and other microstructural characteristics on the mechanical properties of equine cortical bone. Using strain-mode-specific (S-M-S) testing (compression testing of bone habitually loaded in compression; tension testing of bone habitually loaded in tension), the relative mechanical importance of CFO and other material characteristics were examined in equine third metacarpals (MC3s). This model was chosen since it had a consistent non-uniform strain distribution estimated by finite element analysis (FEA) near mid-diaphysis of a thoroughbred horse, net tension in the dorsal/lateral cortices and net compression in the palmar/medial cortices. Bone specimens from regions habitually loaded in tension or compression were: (1) tested to failure in both axial compression and tension in order to contrast S-M-S vs non-S-M-S behavior, and (2) analyzed for CFO, % ash, porosity, fractional area of secondary osteonal bone, osteon cross-sectional area, and population densities of secondary osteons and osteocyte lacunae. Multivariate multiple regression analyses revealed that in S-M-S compression testing, CFO most strongly influenced total energy (pre-yield elastic energy plus post-yield plastic energy); in S-M-S tension testing CFO most strongly influenced post-yield energy and total energy. CFO was less important in explaining S-M-S elastic modulus, and yield and ultimate stress. Therefore, in S-M-S loading CFO appears to be important in influencing energy absorption, whereas the other characteristics have a more dominant influence in elastic modulus, pre-yield behavior and strength. These data generally support the hypothesis that differentially affecting S-M-S energy absorption may be an important consequence of regional histocompositional heterogeneity in the equine MC3. Data inconsistent with the hypothesis, including the lack of highly longitudinal collagen in the dorsal-lateral 'tension' region, paradoxical histologic organization in some locations, and lack of significantly improved S-M-S properties in some locations, might reflect the absence of a similar habitual strain distribution in all bones. An alternative strain distribution based on in vivo strain measurements, without FEA, on non-Thoroughbreds showing net compression along the dorsal-palmar axis might be more characteristic of ...

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

“…However, our finding that the osteonal order in the investigated horse radius is independent of anatomic location does not support this hypothesis. The second investigated bone, the metacarpal of horses, has been shown to be loaded primarily in torsion (Skedros et al, 2006;Skedros et al, 2007). In our analysis, the metacarpal bone displays higher order at the lateral compared with the cranial location.…”

“…However, this observed anisotropy of the ACFs in the metacarpal bones cannot be explained based on purely torsional loading. It has been reported that some third metacarpals have a loading history of combined torsion with bending (Skedros et al, 2006), which would account for loss of rotational asymmetry.…”

“…The osteonal arrangement in different anatomical locations in two different types of bones in horses (radii, third metacarpals) and one type of bone in dogs (radii) were analyzed. These bones are often selected for structural analysis as they represent two different loading types: the radius is loaded habitually in bending while the third metacarpal bone of horses is loaded mostly in torsion (Skedros et al, 2006;Skedros et al, 2007). With this analysis, anatomical locations with higher/lower osteonal order within specific bones could be identified.…”

Variability in forelimb bone strains during non-steady locomotor activities in goats

“…This suggests that under variable locomotor conditions a curved bone will not see remarkably less varied principal strain orientations than a straight bone, but the curved bone will restrict the ratio of tension to compression to within a more predictable range for any given footfall, whereas a straight bone will experience more variable tension-to-compression ratios. In this case, a critical factor for preventing failure during non-steady activities may be the specific bone microstructure and collagen fiber orientation in the cortices of straight bones compared with curved bones (Skedros et al, 2006), which is a level of detail not examined in our study.…”

The Effects of Endurance Running Training on Young Adult Bone: Densitometry vs. Biomaterial Properties

“…As mentioned in previous studies, tissue-level properties can be divided into the inorganic mineral phase (e.g., hydroxyapatite), which determines tissue stiffness and strength, 80,81 and the organic bone matrix, which plays a key role in energy absorption, 82,83 It has been suggested that the networks of collagen, one of the major components of bone matrix, could affect the energy dissipation between the yield point and fracture point in bone tissue. [84][85][86] Collagen fiber orientation (CFO) has been measured by circularly polarized light microscopes as one parameter to represent the collagen network and to predict post-yield energy of bone tissue. 84 Hence, the post-yield behavior revealed by ERT rats' bone tissue could partially stem from a highly organized collagen fiber network.…”