Abstract
Bone continuously adapts to its mechanical environment by structural reorganization to maintain mechanical strength. As the adaptive capabilities of bone are portrayed in its nano- and microstructure, the existence of dark and bright osteons with contrasting preferential collagen fiber orientation (longitudinal and oblique-angled, respectively) points at a required tissue heterogeneity that contributes to the excellent fracture resistance mechanisms in bone. Dark and bright osteons provide an exceptional opportunity to deepen our understanding of how nanoscale tissue properties influence and guide fracture mechanisms at larger length scales. To this end, a comprehensive structural, compositional, and mechanical assessment is performed using circularly polarized light microscopy, synchrotron nanocomputed tomography, focused ion beam/scanning electron microscopy, quantitative backscattered electron imaging, Fourier transform infrared spectroscopy, and nanoindentation testing. To predict how the mechanical behavior of osteons is affected by shifts in collagen fiber orientation, finite element models are generated. Fundamental disparities between both osteon types are observed: dark osteons are characterized by a higher degree of mineralization along with a higher ratio of inorganic to organic matrix components that lead to higher stiffness and the ability to resist plastic deformation under compression. On the contrary, bright osteons contain a higher fraction of collagen and provide enhanced ductility and energy dissipation due to lower stiffness and hardness.
Highlights
Bone continuously adapts to its mechanical environment by structural reorganization to maintain mechanical strength
Bone is able to withstand complex physiological loading patterns by capable fracture resistance mechanisms, both intrinsic and extrinsic.[15−17] Many factors guide the fracture resistance of bone including the structural integrity on the nano- and microscale, the bone mineral density distribution, the mineral quality, and the accumulation of microcracks.[18−21] This extends to the organic part of the matrix where alterations in collagen quality have been shown to have an adverse effect on the mechanical competence.[22−24] The importance of collagen for fracture resistance is emphasized by clinically challenging disorders like osteogenesis imperfecta or Paget’s disease, both of which are characterized by impaired collagen formation and organization leading to increased fracture susceptibility.[25−27] the orientation of collagen fibers is considered as an contributor to bone’s ability to resist fracture.[28,29]
To unravel the necessity of both types of osteons to exist within the femoral diaphysis we comprehensively assess the structure, composition, and mechanical properties of dark osteons composed of collagen fibers running parallel to the long axis and bright osteons predominantly built from oblique-angled fibers
Summary
Bone continuously adapts to its mechanical environment by structural reorganization to maintain mechanical strength. Pattern of both osteon types, neglecting the degree of mineralization, corresponds to that of the loading forces acting on the bone.[34−36] In quadrupedal mammalians, where angulation of the joints leads to significant bending stresses,[37,38] the distribution of dark and bright osteons coincides with the distribution of tensile and compressive stresses.[39−41] The dependency of population densities of distinct osteon types with specific loading modes suggests that collagen fibers align according to specific strain modes and serve different mechanical functions.[42−44] in bipedal human femoral bone, the diaphysis is primarily loaded in compression with little impact of bending and tensile forces.[45−47] In view of this rather uniform loading scenario, spatial changes in the preferential CFO of osteons might serve further mechanical functions beyond the resistance to tensile and compressive stresses indicating a more profound mechanical function of dark and bright osteons This is further supported by the fact that, even though the overall CFO pattern appeared nonrandomly distributed, no single pattern of CFO was found to exist in the human diaphyseal femur, suggesting that the microstructure is sensitive to individual adaptation.[30] In this study, we aim to reinterpret the role of dark and bright osteons in bone that is predominantly under compression to elucidate the necessity of both types to coexist within the femoral diaphysis
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