Multiscale mechano-biological characterization of necrotic, sclerotic, and healthy zones in femoral head osteonecrosis: linking viscoelastic heterogeneity to mechanical failure.

Osteonecrosis of the femoral head (ONFH) is a progressive disorder characterized by regional trabecular bone deterioration that ultimately results in collapse. While elastic property changes in diseased bones are well documented, the contribution of region-specific viscoelastic behavior and its relationship to multiscale microarchitecture and composition remain insufficiently defined. Eighteen femoral heads (mean age: 40.8 ± 7.1 years; 15 males, 3 females; diagnosis: Ficat Stage III/IV) were retrieved during total hip arthroplasty. Patient-matched trabecular cores were harvested from three distinct zones: necrotic (NCZ), sclerotic (SCZ), and healthy (HZ). Bone quality was evaluated using micro-CT, uniaxial compression, nanoindentation, FTIR, and XRD. Viscoelasticity was characterized via stress relaxation and dynamic mechanical analysis (DMA) tests. The NCZ demonstrated microarchitectural decay (bone volume/total volume reduced by 54.54%, p < 0.001) and lower elastic modulus (reduced by 60.25%, p < 0.001) compared to SCZ. DMA revealed that while the NCZ exhibited the lowest storage modulus (E'), it showed a trend toward greater matrix-dominated stress relaxation (~ 25% increase). Conversely, the SCZ exhibited a 60% increase in E' (p < 0.01) but significantly reduced damping and post-yield energy than NCZ, consistent with a stiff yet brittle phenotype. Stress relaxation correlated strongly with mineral/matrix ratio (r = - 0.71) and collagen maturity (r = - 0.64), with collagen spectral markers significantly predicting microscale mechanical properties. ONFH induces profound viscoelastic and structural heterogeneity. This zonal mismatch between the compliant necrotic core and the stiff, brittle sclerotic rim likely promotes stress concentrations, driving structural instability and subchondral failure.