Effects of Aging on the Toughness of Human Cortical Bone: A Study from Nano to Macro Size-Scales

Abstract

Age-related deterioration of both the fracture properties and the architecture of bone, coupled with increased life expectancy, are factors leading to the increasing incidence of bone fracture in the elderly. In order to facilitate the development of treatments which counter this increased fracture risk, a thorough understanding of how fracture properties degrade with age is required. The present study describes ex vivo fracture experiments to quantitatively assess the effects of aging on the fracture toughness of human cortical bone in the longitudinal direction. Because cortical bone exhibits rising crack-growth resistance with crack extension, we depart from most previous studies by evaluating the toughness in terms of resistance-curve (R-curve) behavior, measured for bone taken from donors 34 to 99 years old. Using this approach, both the crack-initiation and crack-growth toughness are determined and are found to deteriorate with age; the initiation toughness decreases ~40% from 40 to 100 years, while the growth toughness is effectively eliminated over the same age range. Evidence from x-ray synchrotron tomography is provided to support the hypothesis that the reduction in crack-growth toughness is associated primarily with a degradation in the degree of extrinsic toughening, in particular involving crack bridging at the microstructural level in the wake of the crack. Atomic force microscope-based nanoidentation of individual collagen fibers revealed changes at the collagen fibrillar level and deep-ultraviolet Raman spectroscopy showed that the cross-linking at the nanostructural level also changes with age. These results should provide for a better mechanistic understanding of the increased propensity for bone fracture with age.