Load-bearing in cortical bone microstructure: Selective stiffening and heterogeneous strain distribution at the lamellar level

An improved understanding of bone mechanics is vital in the development of evaluation strategies for patients at risk of bone fracture. The current evaluation approach based on bone mineral density (BMD) measurements lacks sensitivity, and it has become clear that as well as bone mass, bone quality should also be evaluated. The latter includes, among other parameters, the bone matrix material properties, which in turn depend on the hierarchical structural features that make up bone as well as their composition. Optimal load transfer, energy dissipation and toughening mechanisms have, to some extent, been uncovered in bone. Yet, the origin of these properties and their dependence upon the hierarchical structure and composition of bone are largely unknown. Here we investigate load transfer in the osteonal and sub-osteonal levels and the mechanical behaviour of osteonal lamellae and interlamellar areas during loading. Using cantilever-based nanoindentation, in situ microtensile testing during atomic force microscopy (AFM) and digital image correlation (DIC), we report evidence for a previously unknown mechanism. This mechanism transfers load and movement in a manner analogous to the engineered “elastomeric bearing pads” used in large engineering structures. μ-RAMAN microscopy investigations showed compositional differences between lamellae and interlamellar areas. The latter have lower collagen content but an increased concentration of noncollagenous proteins (NCPs). Hence, NC-enriched areas on the microscale might be similarly important for bone failure as ones on the nanoscale. Finally, we managed to capture stable crack propagation within the interlamellar areas in a time-lapsed fashion, proving their significant contribution towards fracture toughness.