Bone indentation recovery time correlates with bond reforming time

Abstract

Despite centuries of work, dating back to Galileo, the molecular basis of bone's toughness and strength remains largely a mystery. A great deal is known about bone microsctructure and the microcracks that are precursors to its fracture, but little is known about the basic mechanism for dissipating the energy of an impact to keep the bone from fracturing. Bone is a nanocomposite of hydroxyapatite crystals and an organic matrix. Because rigid crystals such as the hydroxyapatite crystals cannot dissipate much energy, the organic matrix, which is mainly collagen, must be involved. A reduction in the number of collagen cross links has been associated with reduced bone strength and collagen is molecularly elongated ('pulled') when bovine tendon is strained. Using an atomic force microscope, a molecular mechanistic origin for the remarkable toughness of another biocomposite material, abalone nacre, has been found. Here we report that bone, like abalone nacre, contains polymers with 'sacrificial bonds' that both protect the polymer backbone and dissipate energy. The time needed for these sacrificial bonds to reform after pulling correlates with the time needed for bone to recover its toughness as measured by atomic force microscope indentation testing. We suggest that the sacrificial bonds found within or between collagen molecules may be partially responsible for the toughness of bone.

Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales

“…Each level of the hierarchical structure influences the deformation and fracture of human cortical bone; the smaller levels affect the intrinsic toughness, whereas the higher length scales impact the extrinsic toughness. At the nanoscale, the polymeric nature of the collagen molecules allows them to uncoil and slide with respect to one another by breaking sacrificial bonds that absorb energy (2,6). Sacrificial bonding also exists within higher levels of the hierarchy through shearing/stretching of the interfibrillar matrix and between fibrils (fibrillar sliding) (1,3,4).…”

X-ray diffraction as a promising tool to characterize bone nanocomposites

“…The geometrical arrangement of mineral particles is also considered to play an important role, as the tensile stress transmitted through the matrix on the composite may be arising from shear [30,31]. The toughness of bone composites is further said to arise from glue-like sacrificial bonds in the collagen matrix [32][33][34], where the ability and duration of reforming such bonds after pulling are correlated with the time needed for the bone to recover its toughness.…”

Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils

“…Moreover, AFM probes the surface of materials, and can thus provide only 2D information on the organization of the ultrastructure. This is why AFM's numerous applications in bone research [253,254] have been mainly focused on the study of its mechanical properties at a tissue [255][256][257] and single fibril level [258][259][260], while very few studies have investigated the organization of the mineralized collagen fibrils [261,262] ( figure 15). However, similarly to TEM, AFM has been extensively used to examine bone features at the nanometre scale, such as the size of mineral platelets [13,264], collagen fibril characteristics (e.g.…”