Effect of modifications in mineralized collagen fibril and extra-fibrillar matrix material properties on submicroscale mechanical behavior of cortical bone

A key length scale of interest in assessing the fracture resistance of bone is the submicroscale which is composed of mineralized collagen fibrils (MCF) and extra-fibrillar matrix (EFM). Although the processes through which the submicroscale constituents of bone contribute to the fracture resistance in bone have been identified, the extent of the modifications in submicroscale mechanical response due to the changes in individual properties of MCFs and EFM has not been determined. As a result, this study aims to quantify the influence of individual MCF and EFM material property modifications on the mechanical behavior (elastic modulus, ultimate strength, and resistance to failure) of bone at the submicroscale using a novel finite element modeling approach that incorporate 3D networks of MCFs with three different orientations as well as explicit representation of EFM. The models were evaluated under tensile loading in transverse (representing MCF separation) and longitudinal (representing MCF rupture) directions. The results showed that the apparent elastic modulus at the submicroscale under both loading directions for all orientations was only affected by the change in the elastic modulus of MCFs. MCF separation and rupture strengths were mainly dependent on the ultimate strength of EFM and MCFs, respectively, with minimal influence of other material properties. The extent of damage during MCF separation increased with increasing ultimate strength of EFM and decreased with increasing fracture energy of EFM with minimal contribution from elastic modulus of MCFs. For MCF rupture, there was an almost one-to-one linear relationship between the percent change in fracture energy of MCFs and the percent change in the apparent submicroscale fracture energy. The ultimate strength and elastic modulus of MCFs had moderate to limited influence on the MCF rupture fracture energy. The results of this study quantified the extent of changes that may be seen in the energy dissipation processes during MCF rupture and separation relative to the changes in the individual constituents of the tissue. This new knowledge significantly contributes to improving the understanding of how the material property alterations at the submicroscale that can occur due to diseases, age-related changes, and treatments affect the fracture processes at larger length scales.