Contribution of extrafibrillar matrix to the mechanical behavior of bone using a novel cohesive finite element model.

The mechanical behavior of bone is determined at all hierarchical levels, including lamellae (the basic building block of bone) that are comprised of mineralized collagen fibrils and extrafibrillar matrix. The mechanical behavior of mineralized collagen fibrils has been investigated intensively using both experimental and computational approaches. Yet, the contribution of the extrafibrillar matrix to bone mechanical properties is poorly documented. In this study, we intended to address this issue using a novel cohesive finite element (FE) model, in conjunction with the experimental observations reported in the literature. In the FE model, the extrafibrillar matrix was considered as a nanocomposite of hydroxyapatite (HA) crystals bounded through a thin organic interface modeled as a cohesive interfacial zone. The parameters required by the cohesive FE model were defined based on the experimental data reported in the literature. This hybrid nanocomposite model was tested in two loading modes (i.e. tension and compression) and under two hydration conditions (i.e. wet and dry). The simulation results indicated that (1) the failure modes of the extrafibrillar matrix predicted using the cohesive FE model were closely coincided with those experimentally observed in tension and compression tests; (2) the pre-yield deformation (i.e. internal strain) of HA crystals with respect to the applied strain was consistent with that obtained from the synchrotron X-ray scattering measurements irrespective of the loading modes and hydration status; and (3) the mechanical behavior of the extrafibrillar matrix was dictated by the properties of the organic interface between the HA crystals. Taken together, we postulate that the extrafibrillar matrix plays a major role in the pre-yield deformation and the failure mode of bone, thus, giving rise to important insights in the ultrastructural origins of bone fragility.