Fibrillar-Level Strain Gradients Across the Calcified Bone-Cartilage Interface

The bone-cartilage interface (BCI) and underlying calcified plate is a universal feature in diarthrodial joints. The BCI is an important mechanically-graded interface subjected to shear and compressive strains, and changes at the BCI have been linked to osteoarthritis progression. Here we report the existence of a physiological internal strain gradient (pre-strain) across the BCI at the ultrastructural scale of the extracellular matrix constituents, specifically the collagen fibril. We use X-ray scattering that probes changes in the axial periodicity of fibril-level D-stagger of tropocollagen molecules in the matrix fibrils, as a measure of microscopic pre-strain. We find that mineralized collagen nanofibrils in the calcified BCI are in tension pre-strain relative to the underlying trabecular bone. This behaviour contrasts with the previously accepted notion that fibrillar pre-strain (or D-stagger) in collagenous tissues always reduces with mineralization due to reduced hydration and associated swelling pressure. Within the calcified tissue, a finer-scale gradient in pre-strain over ~50 micron is likely linked to the tidemark. The increased fibrillar pre-strain at the BCI is linked to prior research reporting large tissue-level residual strains under compression. The findings may have biomechanical adaptative significance: higher in-built molecular level resilience/damage resistance to physiological compression, and the disruption of the molecular-level pre-strains during remodelling of the BCI may be a potential factor in osteoarthritis based degeneration.