Aging-related mechanical degradation of cortical bone is driven by microstructural changes in addition to porosity

Abstract

This study aims to gain mechanistic understanding of how aging-related changes in the microstructure of cortical bone drive mechanical consequences at the macroscale. To that end, cortical bone was modeled as a bundle of elastic-plastic, parallel fibers loaded in uniaxial tension, which comprised osteons and interstitial tissue. Distinct material properties were assigned to each fiber in either the osteon or interstitial fiber "families." Models representative of mature (20-60 yrs.) bone, and elderly (60+) bone were created. Aging-related changes were modeled along three independent dimensions: (i) increased porosity, (ii) increased ratio of osteon fibers relative to interstitial fibers, and (iii) a change in fiber material properties. The model captured decreases in modulus, yield stress, yield strain, ultimate stress, ultimate strain, and toughness with age of 14%, 11%, 8%, 6%, 20%, and 30%, respectively. In both mature and elderly bundles, rupture of the interstitial fibers drove the initial loss of strength following the ultimate point. Plasticity and more gradual rupture of the osteons drove the remainder of the response. Both the onset and completion of interstitial fiber rupture occurred at lower strains in the elderly vs. mature case. Changes along all three dimensions were required for the model to capture aging-related decline in the strength, ductility, and toughness of cortical bone. These findings point to the importance of studying microstructural changes beyond porosity, such as the area fraction of osteons and the microconstituent material properties of osteon and interstitial tissue, in order to further our understanding of aging-related changes in bone.