Functional analysis of postnatal collagen network remodelling in articular cartilage

Healthy adult articular cartilage (AC) has a typical depth-dependent composition and structure that results in a tissue stiffness gradient: AC stiffness increases with increasing distance from the articular surface. This gradient is important for normal functioning of the mature joint, but is absent at birth and develops in early life. AC is a hydrated porous tissue in which the collagen network comprises ~75% of the solid mass. We investigated the development of the collagen network in 50 sheep divided over ten sample points between birth and maturity. We assessed three collagen network parameters: predominant collagen fibril orientation, collagen density, and collagen network anisotropy. Results were used in a numerical model to estimate the contributions of the development of each of these parameters to the development of the AC stiffness gradient. Predominant fibril orientation changed from parallel to the articular surface at birth, to a depth-dependent arcade-like structure. Collagen reorientation was finished before sexual maturity (36 weeks). Collagen density increased over the full tissue depth, increased most adjacent to the bone, and had not yet stabilised at 72 weeks. The numerical simulations show that collagen reorientation alone can result in a stiffness gradient that spans an order of magnitude. Based on the simulations, we hypothesize that reorientation of fibrils and increase in collagen density serve distinct functional roles: reorientation functions to establish the stiffness gradient, and collagen density increases to reduce fibril strains that tend to increase due to reorientation.