Development of a Rat Model of Mechanically Induced Tunable Pain and Associated Temporomandibular Joint Responses

J Oral Maxillofac Surg. 2016 Jan;74(1):54.e1-10. doi: 10.1016/j.joms.2015.09.005. Epub 2015 Sep 21.

Abstract

Purpose: Although mechanical overloading of the temporomandibular joint (TMJ) is implicated in TMJ osteoarthritis (OA) and orofacial pain, most experimental models of TMJ-OA induce only acute and resolving pain, which do not meaningfully simulate the pathomechanisms of TMJ-OA in patients with chronic pain. The aim of this study was to adapt an existing rat model of mechanically induced TMJ-OA, to induce persistent orofacial pain by altering only the jaw-opening force, and to measure the expression of common proxies of TMJ-OA, including degradation and inflammatory proteins, in the joint.

Materials and methods: TMJ-OA was mechanically induced in a randomized, prospective study using 2 magnitudes of opening loads in separate groups (ie.,. 2-N, 3.5-N and sham control [no load]). Steady mouth opening was imposed daily (60 minutes/day for 7 days) in female Holtzman rats, followed by 7 days of rest, and orofacial sensitivity was measured throughout the loading and rest periods. Joint structure and extent of degeneration were assessed at day 14 and expression of matrix metalloproteinase-13 (MMP-13), hypoxia-inducible factor-1α (HIF-1α), and tumor necrosis factor-α (TNF-α) in articular cartilage was evaluated by immunohistochemistry and quantitative densitometry methods at day 7 between the 2 loading and control groups. Statistical differences of orofacial sensitivity and chondrocyte expression between loading groups were computed and significance was set at a P value less than .05.

Results: Head-withdrawal thresholds for the 2 loading groups were significantly decreased during loading (P < .0001), but that decrease remained through day 14 only for the 3.5-N group (P < .00001). At day 14, TMJs from the 2-N and 3.5-N groups exhibited truncation of the condylar cartilage, typical of TMJ-OA. In addition, a 3.5-N loading force significantly upregulated MMP-13 (P < .0074), with nearly a 2-fold increase in HIF-1α (P < .001) and TNF-α (P < .0001) at day 7, in 3.5-N loaded joints over those loaded by 2 N.

Conclusion: Unlike a 2-N loading force, mechanical overloading of the TMJ using a 3.5-N loading force induced constant and nonresolving pain and the upregulation of inflammatory markers only in the 3.5-N group, suggesting that these markers could predict the maintenance of persistent orofacial pain. As such, the development of a tunable experimental TMJ-OA model that can separately induce acute or persistent orofacial pain using similar approaches provides a platform to better understand the pathomechanisms involved and possibly to evaluate potential treatment strategies for patients with painful TMJ-OA.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomechanical Phenomena
  • Cartilage, Articular / chemistry
  • Cartilage, Articular / pathology
  • Chondrocytes / chemistry
  • Chondrocytes / pathology
  • Chronic Pain / etiology*
  • Chronic Pain / metabolism
  • Disease Models, Animal*
  • Facial Pain / etiology*
  • Facial Pain / metabolism
  • Female
  • Hypoxia-Inducible Factor 1, alpha Subunit / analysis
  • Mandibular Condyle / chemistry
  • Mandibular Condyle / pathology
  • Matrix Metalloproteinase 13 / analysis
  • Osteoarthritis / etiology*
  • Osteoarthritis / metabolism
  • Random Allocation
  • Range of Motion, Articular / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Sensation / physiology
  • Stress, Mechanical
  • Temporomandibular Joint Disorders / etiology*
  • Temporomandibular Joint Disorders / metabolism
  • Time Factors
  • Tumor Necrosis Factor-alpha / analysis

Substances

  • Hif1a protein, rat
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Tumor Necrosis Factor-alpha
  • Matrix Metalloproteinase 13
  • Mmp13 protein, rat