The Ultrastructure of Bone and Its Relevance to Mechanical Properties

Detailed descriptions of the structural features of bone abound in the literature; however, the mechanical properties of bone, in particular those at the micro- and nano-structural level, remain poorly understood. This paper surveys the mechanical data that are available, with an emphasis on the relationship between the complex hierarchical structure of bone and its mechanical properties. Attempts to predict the mechanical properties of bone by applying composite rule of mixtures formulae have been only moderately successful, making it clear that an accurate model should include the molecular interactions or physical mechanisms involved in transfer of load across the bone material subunits. Models of this sort cannot be constructed before more information is available about the interactions between the various organic and inorganic components. Therefore, further investigations of mechanical properties at the 'materials level', in addition to the studies at the 'structural level' are needed to fill the gap in our present knowledge and to achieve a complete understanding of the mechanical properties of bone.

▪ Abstract The term bone refers to a family of materials, all of which are built up of mineralized collagen fibrils. They have highly complex structures, described in terms of up to 7 hierarchical levels of organization. These materials have evolved to fulfill a variety of mechanical functions, for which the structures are presumably fine-tuned. Matching structure to function is a challenge. Here we review the structure-mechanical relations at each of the hierarchical levels of organization, highlighting wherever possible both underlying strategies and gaps in our knowledge. The insights gained from the study of these fascinating materials are not only important biologically, but may well provide novel ideas that can be applied to the design of synthetic materials.

Properties of the organic matrix of bone as well as its function in the microstructure could be the key to the remarkable mechanical properties of bone. Previously, it was found that on the molecular level, calcium-mediated sacrificial bonds increased stiffness and enhanced energy dissipation in bone constituent molecules. Here we present evidence for how this sacrificial bond and hidden length mechanism contributes to the mechanical properties of the bone composite, by investigating the nanoscale arrangement of the bone constituents and their interactions. We find evidence that bone consists of mineralized collagen fibrils and a non-fibrillar organic matrix, which acts as a 'glue' that holds the mineralized fibrils together. We believe that this glue may resist the separation of mineralized collagen fibrils. As in the case of the sacrificial bonds in single molecules, the effectiveness of this mechanism increases with the presence of Ca2+ ions.