Local and global measurements show that damage initiation in articular cartilage is inhibited by the surface layer and has significant rate dependence

Abstract

Cracks in articular cartilage are a common sign of joint damage, but failure properties of cartilage are poorly understood, especially for damage initiation. Cartilage failure may be further complicated by rate-dependent and depth-dependent properties, including the compliant surface layer. Existing blunt impact methods do not resolve local cartilage inhomogeneities and traditional fracture mechanics tests induce crack blunting and may violate underlying assumptions of linear elasticity. To address this knowledge gap, we developed and applied a method to indent cartilage explants with a sharp blade and initiate damage across a range of loading rates (strain rates 0.5%/s-500%/s), while recording local sample deformation and strain energy fields using confocal elastography. To investigate the importance of cartilage's compliant surface, we repeated the experiment for samples with the surface removed. Bulk data suggest a critical force at which the tissue cuts, but local strains reveals that the deformation the sample can sustain before reaching this force is significantly higher in the surface layer. Bulk and local results also showed significant rate dependence, such that samples were easier to cut at faster speeds. This result highlights the importance of rate for understanding cracks in cartilage and parallels recent studies of rate-dependent failure in hydrogels. Notably, local sample deformation fields were well fit by classical Hookean elasticity. Overall, this study illustrates how local and global measurements surrounding the initiation of damage in articular cartilage can be combined to reveal the importance of cartilage's zonal structure in protecting against failure across physiologically relevant loading rates.

Cartilage articulation exacerbates chondrocyte damage and death after impact injury

“…30,31 Previous studies have shown the surface acts as the primary shear energy dissipating region with damage to this region exacerbating the effect of shear stress elsewhere in the tissue, which is consistent with the results of this study. [44][45][46] The protective nature of cartilage could be due to its inhomogeneous nature where the superficial layer is more compliant than the bulk, which results in the strain, and therefore the majority of cellular damage, being concentrated at the surface. 46,47 Next, the cellular damage caused by sliding motion is consistent with previous studies showing that the shear strain produced, at physiologic sliding speeds, similar levels of chondrocyte death at the superficial layer.…”

“…30 Minor superficial cracking without fibrillation was observed at the cartilage surface, which may be responsible for the increased damage in cartilage that was impacted before sliding is due to the integrity of the superficial layer being compromised, making it resemble cartilage samples in previous studies where the surface is removed before impact. 31,45 This shows the need of an alternative shear energy dissipation mechanism once the surface becomes compromised. Lubrication of the cartilage sliding surfaces has been shown to assist in this function with alteration to the lubricant's lubricating properties being capable of mitigating or agitating cell death.…”

Relaxation capacity of cartilage is a critical factor in rate- and integrity-dependent fracture

“…Large crack lengths and severe damage to microstructural features were induced under relatively high-frequency compressive loading 30 , 31 . Recently, the authors and others found that impact loading, simulating the onset of post-traumatic OA, caused fissures and cracks 32 – 34 and that crack nucleation in cartilage was largely rate-dependent 35 , 36 . In particular, the authors observed that the solid matrix around the crack surfaces underwent larger relaxation and rearrangement at the slow loading rate compared to the fast loading rate 36 .…”

A novel mechanobiological model can predict how physiologically relevant dynamic loading causes proteoglycan loss in mechanically injured articular cartilage

“…The results are compared to the experimentally observed FCD loss of cartilage around cracks in vitro in the absence of exogenous inflammatory cytokine challenge. We hypothesize that, due to the non-uniform strain distributions found earlier around cartilage lesions 30 , 33 , 34 , the strain-based algorithm in the models causes a non-uniform FCD loss. On the other hand, because fluid pressure at the inner crack surface is negligible and uniform through the crack depth, the FCD loss is hypothesized to be more uniformly distributed around lesions in the fluid velocity-controlled degeneration algorithm.…”