Post-yield behavior and failure mechanisms of murine cortical bone at the microscale across different ages depend on alterations in mineralized collagen fibrils’ arrangement

Aging increases the incidence of clinical bone fractures. Mechanisms by which bones dissipate energy and prevent failure may change with age, potentially due to changes in physical and mechanical properties of components, as well as architectural variations over multiple length scales. However, the relationship between damage mechanisms and multi-scale structural alterations during aging remains unclear. The study aims to investigate the mechanical performance of cortical bone at the microscale during aging and its correlation with microstructural alterations, with a focus on mineralized collagen fibril organization. In-situ micropillar compression tests were conducted on dry femurs of five young (3-month), five adult (8-month), and five aged (18-month) mice to evaluate apparent modulus, post-yield behavior, and failure mechanisms. Scanning electron microscopy, transmission electron microscopy, and electron diffraction were employed for microscopic analysis. Dominant failure modes were found to vary with age. The young and adult groups were prone to shear-dominated failure, while the aged group was dominated by splitting failure. The adult group consistently demonstrated the highest apparent modulus and strength, along with high ductility. Notably, the young and aged groups exhibited progressive failure, achieving comparable toughness to the adult group in their dominant fracture modes, with 49 ± 16 MJ/m³ (young) vs. 54 ± 19 MJ/m³ (adult) in shearing, and 49 ± 15 MJ/m³ (aged) vs. 41 ± 13 MJ/m³ (adult) in splitting, respectively. The dominant toughening mechanisms transitioned from fibril pull-out and bridging to fibril kinking and crack deflection with advancing age. Findings highlight the crucial role of mineralized collagen fibrils’ arrangement in governing age-related adaptive alterations in bone failure mechanisms. Statement of significance The general consensus is that aging significantly increases the fracture risk of bone, often due to age-related loss in bone mass. However, the impact of age-related structural changes on bone mechanical behavior across multiple length scales remains unclear. This study revealed that the cortical bone of both young and aged individuals exhibited progressive failure and achieved comparable toughness to the adults at the microscale, which could be attributed to changes in toughening mechanisms directly linked to age-related variations in bone structure. Findings in this study present new insights into multiscale bone mechanics across life stages, which lays a foundation for future studies on bone mechanics and could facilitate the optimal design of damage-resistant materials.