On How Degeneration Influences Load-bearing in the Cartilage-bone System: a Microstructural and Micromechanical Study

Objective: This study investigated the microanatomical response to compression of intact and degenerate cartilage-on-bone samples with the aim of elucidating the functional consequences of articular surface disruption and related matrix changes.

Method: Two groups of mature bovine patellae were identified at the time of harvest; those with intact cartilage and those with cartilage exhibiting mild to severe degeneration. Cartilage-on-bone samples were statically compressed (7 MPa) to near-equilibrium using an 8-mm diameter cylindrical indenter, and then formalin-fixed in this deformed state. Following mild decalcification full-depth cartilage-bone sections, incorporating the indentation profile and beyond, were studied in their fully hydrated state using differential interference contrast optical microscopy (DIC).

Results: Differences in matrix texture, degree of disruption of the articular surface layer (or its complete absence), number of tidemarks and absence or presence of vascularization of the calcified cartilage zone were all observable features that provided clear differentiation between the normal and degenerate tissues. Under load a chevron-type shear discontinuity characterized those samples in which the strain-limiting surface layer was still largely intact. The extent to which this shear discontinuity advanced into the adjacent non-directly loaded cartilage continuum was influenced by the integrity of the cartilage general matrix. For those tissues deficient in a strain-limiting articular surface there was no shear discontinuity, the cartilage deformation field was instead shaped primarily by its osteochondral attachment and a laterally-directed compressive collapse of a much weakened matrix. In the degenerate samples the altered matrix textures associated with different regions of the deformation field are interpreted in terms of an intrinsic fibrillar architecture that is weakened by two fundamental processes: (1) a de-structuring resulting from a reduction in connectivity between fibrils and (2) subsequent aggregation of these now disconnected fibrils.

Conclusion: DIC microscopy provides a high-resolution description of the integrated osteochondral tissue system across the full continuum of matrices, from normal to severely degenerate. Our study demonstrates the important functional role played by the strain-limiting articular surface, the consequences associated with its disruption, as well as the loss of effective stress transmission associated with a 'de-structured' general matrix. The study also provides new insights into the integration of cartilage with both its subchondral substrate and the wider continuum of non-directly loaded cartilage.