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Research Papers

The Regional Contribution of Glycosaminoglycans to Temporomandibular Joint Disc Compressive Properties

[+] Author and Article Information
Vincent P. Willard, Kerem N. Kalpakci

Department of Bioengineering,  Rice University, Houston, TX 77005

Andrew J. Reimer

Department of Biomedical Engineering,  University of California Davis, Davis, CA 95616

Kyriacos A. Athanasiou1

Department of Biomedical Engineering,  University of California Davis, Davis, CA 95616athanasiou@ucdavis.edu

1

Corresponding Author. Department of Biomedical Engineering, University of California Davis, One Shields Avenue, Davis, CA 95616.

J Biomech Eng 134(1), 011011 (Feb 10, 2012) (8 pages) doi:10.1115/1.4005763 History: Received October 07, 2011; Revised January 01, 2012; Posted January 24, 2012; Published February 10, 2012; Online February 10, 2012

Understanding structure-function relationships in the temporomandibular joint (TMJ) disc is a critical first step toward creating functional tissue replacements for the large population of patients suffering from TMJ disc disorders. While many of these relationships have been identified for the collagenous fraction of the disc, this same understanding is lacking for the next most abundant extracellular matrix component, sulfated glycosaminoglycans (GAGs). Though GAGs are known to play a major role in maintaining compressive integrity in GAG-rich tissues such as articular cartilage, their role in fibrocartilaginous tissues in which GAGs are much less abundant is not clearly defined. Therefore, this study investigates the contribution of GAGs to the regional viscoelastic compressive properties of the temporomandibular joint (TMJ) disc. Chondroitinase ABC (C-ABC) was used to deplete GAGs in five different disc regions, and the time course for >95% GAG removal was defined. The compressive properties of GAG depleted regional specimens were then compared to non-treated controls using an unconfined compression stress-relaxation test. Additionally, treated and non-treated specimens were assayed biochemically and histologically to confirm GAG removal. Compared to untreated controls, the only regions affected by GAG removal in terms of biomechanical properties were in the intermediate zone, the most GAG-rich portion of the disc. Without GAGs, all intermediate zone regions showed decreased tissue viscosity, and the intermediate zone lateral region also showed a 12.5% decrease in modulus of relaxation. However, in the anterior and posterior band regions, no change in compressive properties was observed following GAG depletion, though these regions showed the highest compressive properties overall. Although GAGs are not the major extracellular matrix molecule of the TMJ disc, they are responsible for some of the viscoelastic compressive properties of the tissue. Furthermore, the mechanical role of sulfated GAGs in the disc varies regionally in the tissue, and GAG abundance does not always correlate with higher compressive properties. Overall, this study found that sulfated GAGs are important to TMJ disc mechanics in the intermediate zone, an important finding for establishing design characteristics for future tissue engineering efforts.

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Copyright © 2012 by American Society of Mechanical Engineers
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Figure 3

Viscoelastic compressive properties of GAG depleted TMJ disc and hyaline cartilage samples. (a) GAG removal with C-ABC did not produce a significant difference in the instantaneous modulus of the TMJ disc. (b) C-ABC treatment also had no effect on the instantaneous modulus of the tibial cartilage, although it did trend lower. (c) Overall, C-ABC treatment did not produce a change in the relaxation modulus of TMJ disc samples. (d) GAG depletion in articular cartilage produced a ∼50% decrease in the tissue’s relaxation modulus. (e) GAG depletion produced an overall decrease in the coefficient of viscosity for TMJ disc samples. All regions of the intermediate zone (IZM, IZC, IZL) displayed a ∼30% decrease in viscosity. (f) C-ABC treatment of hyaline cartilage led to a ∼50% decrease in the coefficient of viscosity. Data is presented as mean ± SD. Letters in brackets represent the results of a two-way ANOVA for TMJ disc specimens and a student’s t-test for hyaline cartilage specimens. Groups not connected by the same letter are statistically different. (Note: TMJ disc regions and hyaline cartilage are plotted different scales to enhance readability).

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Figure 4

Sulfated GAG and collagen content of C-ABC treated samples. (a) C-ABC treatment produced extensive GAG depletion (≥96%) in all regions of the TMJ disc. (b) Using the same treatment, GAG depletion in tibial cartilage was only about 50%. (c) C-ABC treatment produced no change in collagen per dry weight within the TMJ disc. (d) Treatment of hyaline cartilage with C-ABC did increase the collagen per dry weight (∼10%). All data is presented as mean ± SD. Letters in brackets represent the results of a two-way ANOVA for the TMJ disc samples and a student’s t-test for the articular cartilage samples. Groups not connected by the same letter are statistically different. (Note: TMJ disc regions and hyaline cartilage are plotted on different scales to enhance readability).

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Figure 5

Safranin-O staining of C-ABC treated specimens to examine the distribution of sulfated GAGs. Some positive staining (red color) can be found in TMJ disc samples immediately surrounding cells, but very low overall staining was observed, and no staining was detected in the matrix. In contrast, intense positive staining can be seen throughout the matrix of articular cartilage. C-ABC treatment produced a small but visible difference in some TMJ disc samples. Treatment of hyaline cartage produced a very obvious depletion of GAGs starting at the edge of the tissue and proceeding toward the center. (Scale bar = 100 μm).

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Figure 1

Investigated regions of the TMJ disc and tibial cartilage. Because of the heterogeneous nature of the TMJ disc, the contribution of GAGs to the compressive properties of the tissue was tested regionally. (a) 3 mm discs were harvested from five regions of the disc: the posterior band (PB), anterior band (AB), intermediate zone medial (IZM), intermediate zone central (IZC), and intermediate zone lateral (IZL). Hyaline articular cartilage (AC) from the tibial plateau was as a benchmark control in this investigation. (b) A 3 mm disc has harvested from the center of the tibial plateau on the medial side of the joint. (not drawn to scale).

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Figure 2

Time course of GAG removal from the TMJ disc. Samples from the IZL region of the disc were treated with C-ABC or a control buffer for up to 12 h and their final sulfated GAG content was measured. A one-way ANOVA comparing time points within the treatment control and C-ABC treated groups is shown. Time points not connected by the same letter are statistically different from each other. C-ABC treatment produced a rapid decrease in the GAG content of the disc, which equilibrated after 3 h of treatment. A decrease in GAG content was also seen in the treatment control group, but was only statistically significant after 12 h. A 3 h incubation was chosen for all subsequent testing. Data is presented as mean ± SD.

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