Level dependent alterations in human facet cartilage mechanics and bone morphometry with spine degeneration

Abstract

The zygapophyseal joints of the spine, also known as the facet joints, are paired diarthrodial joints posterior to the intervertebral disc and neural elements. The pathophysiology of facet osteoarthritis (OA), as well as crosstalk between the disc and facets, remains largely understudied compared to disc degeneration. The purpose of this study was to characterize alterations to human facet cartilage and subchondral bone across a spectrum of degeneration and to investigate correlations between disc and facet degeneration. Human lumbar facet articular surfaces from six independent donors were subject to creep indentation mechanical testing to quantify cartilage mechanical properties, followed by microcomputed tomography (µCT) analyses for subchondral bone morphometry. The degenerative state of each articular surface was assessed via macroscopic scoring and via Osteoarthritis Research Society International histopathology scoring. Our data suggest reduced facet cartilage compressive and tensile moduli and increased permeability with increasing degenerative grade, particularly at the lower levels of the spine. µCT analyses revealed spinal level-dependent alterations to the subchondral bone, with an increase in trabecular bone at the L4-L5 level, but a decrease at the upper levels of the lumbar spine with increasing degenerative grade. Cortical bone volume fraction was generally decreased with increasing degenerative grade across spinal levels. Correlation analysis revealed several associations between quantitative measures of disc degeneration and facet OA. This study showed that alterations in the mechanical properties of facet cartilage and in the structural properties of facet subchondral bone correlated with aspects of disc degeneration and were highly dependent on spinal level.

Keywords: biomechanics; indentation; intervertebral disc degeneration; osteoarthritis; zygapophyseal joint.

Figure 1.

A). Donor Demographics and levels analyzed per donor. B). Number of facets evaluated corresponding to each lumbar spine level.

Figure 2.

A). Sample macroscopic images of individual facets for each grade from different donors. Graded according to prior study by Li et al; (Grade 1: surface fibrillation; Grade 2: fissuring; Grade 3: erosion of 30% or less of the articular surface; Grade 4: erosion of more than 30% of the articular surface). B). Distribution of number of facets from each macroscopic grade stratified by disc Pfirrmann grade. C). Distribution of number of facets from each macroscopic grade stratified by spinal level.

Figure 3.

A). Safranin-O and Fast Green-stained histological sections of human facets demonstrating the sample variation from different donors within the same OARSI score (Scale = 2 mm). The number of facets from each OARSI score was stratified by B). spinal level and C). disc Pfirrmann grade.

Figure 4.

A). Photograph of cartilage indentation testing setup with 1mm indenter and potted facet sample. B). “Diamond” configuration demonstrating the 4 individual points, each 3mm apart, where cartilage creep testing was performed. The dashed line delineates the articular surface.C). Mean (dark colored line) and standard deviation (shaded area) deformation versus time curves from the creep indentation testingfor OARSI grade 2 and 5 facets. D). Individual sample deformation versus time (on a logarithmic scale) showing the Hertzian biphasictheory model fit to the raw data from indentation testing to determine compressive modulus, tensile modulus,K₀,and M of the facet cartilage. E). Compressive modulus, F). tensile modulus and G). permeability stratified by OARSI grade and spinal level. Graphs depict mean plus the 95% confidence interval, and bars denote significant differences between groups.

Figure 5.

A). Example contours of facet cortical and trabecular bone for μCT analysis (scale = 3mm)of B). cortical bone volume fraction (BV/TV), C). trabecular bone volume fraction (BV/TV), D). trabecular number, E). trabecular thickness, and F). trabecular spacing, stratified by spinal level and macroscopic grade. Graphs depict mean plus the 95% confidence interval, and bars denote significant differences between groups.