Strain-rate stiffening of cortical bone: observations and implications from nanoindentation experiments

While bone mineralization is considered to be responsible for its stiffness, bone durability partially associated with the time-dependent viscoelasticity of matrix proteins is still poorly elucidated. Here we demonstrate a novel mechanism of highly mineralized bone durability almost independent of inherent viscoelastic behaviour along with a protocol for measuring the mechanical properties of mineralized tissues. Strain-rate nanoindentation tests showed substantial stiffening of the highly mineralized calvarial bone, whereas large creep or stress relaxation was observed during constant load or displacement tests, respectively. Based on the lower viscoelasticity of the highly mineralized structure, such large time-dependent response appears to be associated with nanoscale dimensional recovery, rather than viscoelastic behaviour, implying the inverse namely strain-rate dependent dilatant behaviour. This dilatant expansion increased the indenter penetration resistance into the surface, enhancing instantaneous stiffness. The associated stiffening and higher effective elastic modulus were highly strain-rate dependent and more readily observed in more highly mineralized tissues such as the calvarial bone. Such strain-rate stiffening and consequent dimensional recovery may be vital responses of bone tissues against excessive deformation to maintain tissue integrity.