Nanoscale deformation mechanisms and yield properties of hydrated bone extracellular matrix

Schwiedrzik, Jakob; Taylor, Aidan; Casari, Daniele; Wolfram, Uwe; Zysset, Philippe; Michler, Johann

Acta Biomaterialia 60 (2017)

Bone features a hierarchical architecture combining antagonistic properties like toughness and strength. In order to better understand the mechanisms leading to this advantageous combination, its postyield and failure behaviour was analyzed on the length scale of a single lamella. Micropillars were compressed to large strains under hydrated conditions to measure their anisotropic yield and post-yield behaviour. An increase in strength compared to the macroscale by a factor of 1.55 and a strong influence of hydration with a decrease by 60% in yield stress compared to vacuum conditions were observed. Post-compression transmission electron microscopic analysis revealed anisotropic deformation mechanisms. In axial pillars, where fibrils were oriented along the loading axis, kink bands were observed and shear cracks emerged at the interface of ordered and disordered regions. Micromechanical analysis of fibril kinking allowed an estimate of the extrafibrillar matrix shear strength to be made: 120±40 MPa. When two opposing shear planes met a wedge was formed, splitting the micropillar axially in a mode 1 crack. Making use of an analytical solution, the mode 1 fracture toughness of bone extracellular matrix for splitting along the fibril direction was estimated to be 0.07 MPam. This is 1–2 orders of magnitude smaller than on the macroscale, which may be explained by the absence of extrinsic toughening mechanisms. In transverse pillars, where fibrils were oriented perpendicular to the loading axis, cracks formed in regions where adverse fibril orientation reduced the local fracture resistance. This study underlines the importance of bone’s hierarchical microstructure for its macroscopic strength and fracture resistance and the need to study structure-property relationships as well as failure mechanisms under hydrated conditions on all length scales. Statement of Significance Bone’s hierarchical architecture combines toughness and strength. To understand the governing deformation mechanisms, its postyield behaviour was analyzed at the microscale. Micropillars were compressed in physiological solution; an increased strength compared to macroscale and an influence of hydration was found. Transmission electron microscopy revealed cracks forming in regions with adverse fibril orientation in transverse pillars. In axial pillars kink bands were observed and shear cracks emerged at the interface of ordered and disordered regions. It was estimated that bone’s fracture toughness for splitting between fibrils is significantly smaller than on the macroscale. This study underlines the importance of bone’s hierarchical microstructure and the need to study structure-property relationships on all length scales.

http://doi.org/10.1016/j.actbio.2017.07.030