The etiology of hip fractures remains unclear but might be elucidated by an improved understanding of the microstructural failure mechanisms of the human proximal femur during a sideways fall impact. In this context, we biomechanically tested 12 cadaver proximal femurs (aged 76 AE 10 years; 8 female, 4 male) to directly measure strength for a sideways fall and also performed microcomputed tomography (CT)-based, nonlinear finite element analysis of the same bones (82-micron-sized elements, $120 million elements per model) to estimate the amount and location of internal tissue-level failure (by ductile yielding) at initial structural failure of the femur. We found that the correlation between the directly measured yield strength of the femur and the finite element prediction was high (R 2 ¼ 0.94, p < 0.0001), supporting the validity of the finite element simulations of failure. In these simulations, the failure of just a tiny proportion of the bone tissue (1.5% to 6.4% across all bones) led to initial structural failure of the femur. The proportion of failed tissue, estimated by the finite element models, decreased with decreasing measured femoral strength (R 2 ¼ 0.88, p < 0.0001) and was more highly correlated with measured strength than any measure of bone volume, mass, or density. Volumewise, trabecular failure occurred earlier and was more prominent than cortical failure in all femurs and dominated in the very weakest femurs. Femurs with low measured strength relative to their areal bone mineral density (BMD) (by dual-energy X-ray absorptiometry [DXA]) had a low proportion of trabecular bone compared with cortical bone in the femoral neck (p < 0.001), less failed tissue (p < 0.05), and low structural redundancy (p < 0.005). We conclude that initial failure of the femur during a sideways fall is associated with failure of just a tiny proportion of the bone tissue, failure of the trabecular tissue dominating in the very weakest femurs owing in part to a lack of structural redundancy.

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To provide mechanistic insight into the etiology of osteoporotic wedge fractures, we investigated the spatial distribution of tissue at the highest risk of initial failure within the human vertebral body for both forward flexion and uniform compression loading conditions. Micro-CT-based linear elastic finite element analysis was used to virtually load 22 human T9 vertebral bodies in either 5° of forward flexion or uniform compression; we also ran analyses replacing the simulated compliant disc (E = 8 MPa) with stiff polymethylmethacrylate (PMMA, E = 2,500 MPa. As expected, we found that, compared to uniform compression, forward flexion increased the overall endplate axial load on the anterior half of the vertebra and shifted the spatial distribution of high-risk tissue within the vertebra towards the anterior aspect of the vertebral body. However, despite that shift, the high-risk tissue remained primarily within the central regions of the trabecular bone and endplates, and forward flexion only slightly altered the ratio of cortical-to-trabecular load sharing at the mid-vertebral level (mean ± SD for n = 22: 41.3% ± 7.4% compression; 44.1% ± 8.2% forward flexion). When the compliant disc was replaced with PMMA, the anterior shift of high-risk tissue was much more severe. We conclude that, for a compliant disc, a moderate degree of forward flexion does not appreciably alter the spatial distribution of stress within the vertebral body.

The role of tissue-level post-yield behavior on the apparent-level strength of trabecular bone is a potentially important aspect of bone quality. To gain insight into this issue, we compared the apparent-level strength of trabecular bone for the hypothetical cases of fully brittle versus fully ductile failure behavior of the trabecular tissue. Twenty human cadaver trabecular bone specimens (5 mm cube; BV/TV = 6–36%) were scanned with micro-CT to create 3D finite element models (22-micron element size). For each model, apparent-level strength was computed assuming either fully brittle (fracture with no tissue ductility) or fully ductile (yield with no tissue fracture) tissue-level behaviors. We found that the apparent-level ultimate strength for the brittle behavior was only about half the value of the apparent-level 0.2%-offset yield strength for the ductile behavior, and the ratio of these brittle to ductile strengths was almost constant (mean ± SD = 0.56 ± 0.02; n=20; R2 = 0.99 between the two measures). As a result of this small variation, although the ratio of brittle to ductile strengths was positively correlated with the bone volume fraction (R2=0.44, p=0.01) and structure model index (SMI, R2=0.58, p<0.01), these effects were small. Mechanistically, the fully ductile behavior resulted in a much higher apparent-level strength because in this case about 16-fold more tissue was required to fail than for the fully brittle behavior; also, there was more tensile- than compressive-mode of failure at the tissue level for the fully brittle behavior. We conclude that, in theory, the apparent-level strength behavior of human trabecular bone can vary appreciably depending on whether the tissue fails in a fully ductile versus fully brittle manner, and this effect is largely constant despite appreciable variations in bone volume fraction and microarchitecture.

The mechanisms of age-related vertebral fragility remain unclear, but may be related to the degree of “structural redundancy” of the vertebra, that is, its ability to safely redistribute stress internally after local trabecular failure from an isolated mechanical overload. To better understand this issue, we performed biomechanical testing and nonlinear micro-CT-based finite element analysis on 12 elderly human thoracic ninth vertebral bodies (ages 76.9 ± 10.8 years). After experimentally overloading the vertebrae to measure strength, we used the nonlinear finite element analysis to estimate the amount of failed tissue and understand failure mechanisms. We found that the amount of failed tissue per unit bone mass decreased with decreasing bone volume fraction (r2 = 0.66, p < 0.01). Thus, for the weak vertebrae with low bone volume fraction, overall failure of the vertebra occurred after failure of just a tiny proportion of the bone tissue (< 5%). This small proportion of failed tissue had two sources: the existence of fewer vertically oriented load paths to which load could be redistributed from failed trabeculae; and the vulnerability of the trabeculae in these few load paths to undergo bending-type failure mechanisms, which further weaken the bone. Taken together, these characteristics suggest that diminished structural redundancy may be an important aspect of age-related vertebral fragility: vertebrae with low bone volume fraction are highly susceptible to collapse since so few trabeculae are available for load redistribution if the external loads cause any trabeculae to fail.