The changing role of the superficial region in determining the dynamic compressive properties of articular cartilage during postnatal development.

OBJECTIVE: To explore how changes to the superficial region (SR) of articular cartilage during skeletal development impact its functional properties. It was hypothesised that a functional superficial region is not present in skeletally immature articular cartilage, and removal of this zone of the tissue would only negatively impact the dynamic modulus of the tissue with the attainment of skeletal maturity. METHODS: Porcine osteochondral cores were mechanically tested statically and dynamically with and without their respective superficial regions in confined and unconfined compression at different stages of postnatal development and maturation. A novel combination of histological, biochemical and imaging techniques were utilised to accurately describe changes to the superficial region during postnatal development. RESULTS: Articular cartilage was found to become stiffer and less permeable with age. The confined and unconfined dynamic modulus significantly decreased after removal of the superficial region in skeletally mature cartilage, whilst no significant change was observed in the 4 week old tissue. Biochemical analysis revealed a significant decrease in overall sGAG content with age (as % dry weight), whilst collagen content significantly increased with age, although the composition of the superficial region relative to the remainder of the tissue did not significantly change with age. Helium ion microscopy (HIM) revealed dramatic changes to the organization of the superficial region with age. CONCLUSIONS: The findings demonstrate that the superficial region of articular cartilage undergoes dramatic structural adaptation with age, which in turn plays a key role in determining the dynamic compressive properties of the tissue.

Postnatal changes to the mechanical properties of articular cartilage are driven by the evolution of its collagen network.

While it is well established that the composition and organisation of articular cartilage dramatically change during skeletal maturation, relatively little is known about how this impacts the mechanical properties of the tissue. In this study, digital image correlation was first used to quantify spatial deformation within mechanically compressed skeletally immature (4 and 8 week old) and mature (1 and 3 year old) porcine articular cartilage. The compressive modulus of the immature tissue was relatively homogeneous, while the stiffness of mature articular cartilage dramatically increased with depth from the articular surface. Other, well documented, biomechanical characteristics of the tissue also emerged with skeletal maturity, such as strain-softening and a depth-dependent Poisson's ratio. The most significant changes that occurred with age were in the deep zone of the tissue, where an order of magnitude increase in compressive modulus (from 0.97 MPa to 9.4 MPa for low applied strains) was observed from 4 weeks postnatal to skeletal maturity. These temporal increases in compressive stiffness occurred despite a decrease in tissue sulphated glycosaminoglycan content, but were accompanied by increases in tissue collagen content. Furthermore, helium ion microscopy revealed dramatic changes in collagen fibril alignment through the depth of the tissue with skeletal maturity, as well as a fivefold increase in fibril diameter with age. Finally, computational modelling was used to demonstrate how both collagen network reorganisation and collagen stiffening play a key role in determining the final compressive mechanical properties of the tissue. Together these findings provide a unique insight into evolving structure-function relations in articular cartilage.

The role of the superficial region in determining the dynamic properties of articular cartilage.

OBJECTIVE: The objective of this study was to elucidate the role of the superficial region of articular cartilage in determining the dynamic properties of the tissue. It is hypothesised that removal of the superficial region will influence both the flow dependent and independent properties of articular cartilage, leading to a reduction in the dynamic modulus of the tissue. METHODS: Osteochondral cores from the femoropatellar groove of three porcine knee joints were subjected to static and dynamic loading in confined or unconfined compression at increasing strain increments with and without their superficial regions. Equilibrium moduli and dynamic moduli were measured and the tissue permeability was estimated by fitting experimental data to a biphasic model. RESULTS: Biochemical analysis confirmed a zonal gradient in the tissue composition and organisation. Histological and PLM analysis demonstrated intense collagen staining in the superficial region of the tissue with alignment of the collagen fibres parallel to the articular surface. Mechanical testing revealed that the superficial region is less stiff than the remainder of the tissue in compression, however removal of this region from intact cores was found to significantly reduce the dynamic modulus of the remaining tissue, suggesting decreased fluid load support within the tissue during transient loading upon removal of the superficial region. Data fits to a biphasic model predict a significantly lower permeability in the superficial region compared to the remainder of the tissue. CONCLUSIONS: It is postulated that the observed decrease in the dynamic moduli is due at least in part to the superficial region acting as a low permeability barrier, where its removal decreases the tissue's ability to maintain fluid load support. This result emphasises the impact that degeneration of the superficial region has on the functionality of the remaining tissue.