Bone Resists Fatigue Through Crack Deceleration at the Fibril Scale

Bone endures millions of cycles throughout its lifetime by accumulating damage at a rate slow enough to allow for cell-mediated repair, but the mechanisms that delay this fatigue failure remain poorly understood. While prior studies have focused on the fatigue response of macroscale architecture of bone, the role of it's nanoscale structure in resisting fatigue has been experimentally inaccessible. Here, we combine in-situ fatigue loading with synchrotron X-ray tomography and radiography to directly observe crack propagation in human bone with 21 nm spatial and 100 ms temporal resolution. We find that mineralized collagen fibrils decelerate crack growth through branching along the fibril axes, while orthogonal cracks are intermittently decelerated by nanoscale interfibrillar interfaces. These mechanisms suppress damage accumulation under physiological loads by an order of magnitude. Our findings uncover a previously unobserved toughening strategy at the nanoscale, providing insight as to how the hierarchical structure of bone bridges the timescale gap between mechanical damage and biological repair.