An interspecies comparison of the temporomandibular joint disc

Abstract

The temporomandibular joint (TMJ) disc plays a critical role in normal function of the joint, and many disorders of the TMJ are a result of disc dysfunction. Previous quantitative TMJ characterization studies examined either the human or a specific animal model, but no single study has compared different species, in the belief that differences in joint morphology, function, and diet would be reflected in the material properties of the disc. In this study, we examined topographical biochemical (collagen, glycosaminoglycan, and DNA content) and biomechanical (tensile and compressive) properties of the human TMJ disc, and also discs from the cow, goat, pig, and rabbit. Regional and interspecies variations were identified in all parameters measured, and certain disc characteristics were observed across all species, such as a weak intermediate zone under mediolateral tension. While human discs possessed properties distinct from those of the other species, pig discs were most similar to the human, suggesting that the pig may be a suitable animal model for TMJ bioengineering efforts.

Figure 1.

Description of the TMJ disc regions tested in this investigation and gross morphology of the collected discs. (A) Regions of the TMJ disc used for biochemical, histological, and compression testing: posterior band central (PBC), intermediate zone (IZ), medial (IZM), IZ central (IZC), IZ lateral (IZL), and anterior band central (ABC). (B) Regions of the TMJ disc used for tensile testing: mediolateral (ML), posterior (ML P), ML central (ML C), ML anterior (ML A), anteroposterior (AP), medial (AP M), AP central (AP C), AP lateral (AP L). (C) Scaled figure showing the gross morphology of TMJ discs collected from the 5 different species tested. (D) Dimensions of discs collected from each species measured in the mediolateral (M-L) and anteroposterior (A-P) directions. Data are presented as mean ± SD. A one-way ANOVA was conducted on the data from each direction, and animals not connected by the same letter were statistically different from one another. The pig was the only animal with dimensions not significantly different from those of the human in both the A-P and M-L directions.

Figure 2.

Biochemical and histological analysis. (A-C) Interspecies comparison of the quantitative biochemical content of the TMJ disc. Data were normalized to wet weight and are presented as mean ± SD. A two-way ANOVA is presented with the factors of species and region. Samples not connected by the same letter are statistically different from each other. (A) Total collagen content of human samples was not statistically different from that in pig or rabbit discs. (B) Human discs contained significantly less DNA content than the other species, likely because of age. (C) Sulfated GAG content of human samples fell in between those of the pig and rabbit samples. (D) Safranin-O/fast green staining of sections from the TMJ disc. Positive Safranin-O staining (red to purple) is clear in all samples except human ABC and all regions of the pig disc. Images were taken on a Nikon E600 microscope with a 20X objective. (Note: The complete biochemical dataset is presented online in Appendix Table 3.)

Figure 3.

Biomechanical properties under tension. Data are presented as mean ± SD. Data were analyzed by a two-way ANOVA with Tukey’s HSD test post hoc where appropriate, and groups not connected by the same letter are significantly different (p < 0.05). Peak (A) and relaxed (B) Young’s moduli under tensile loading. Human tissue was the stiffest among the species, and the central region under mediolateral strain was the most compliant among the regions under both loading conditions. (Note: The complete tensile dataset is presented online in Appendix Table 1.)

Figure 4.

Biomechanical properties under compression at 20% strain. Data are presented as mean ± SD. Data were analyzed by a two-way ANOVA with Tukey’s HSD test post hoc where appropriate, and groups not connected by the same letter are significantly different (p < 0.05). (A) Compressive moduli under instantaneous loading. The porcine, leporine, and bovine tissue yielded values statistically similar to those of the human, while the caprine tissue was stiffer than the human tissue. (B) Compressive moduli at equilibrium. Human and pig discs were significantly more compliant than rabbit, goat, and cow discs. The band regions were significantly stiffer than the intermediate zone regions under both instantaneous and relaxed conditions. (Note: The complete compressive dataset is presented online in Appendix Table 2.)