Abstract
To investigate potential mechanisms associated with the increased prevalence of temporomandibular joint (TMJ) disorders among women, the study objective was to determine sex-dependent and region-dependent differences in fixed charge density (FCD) using an electrical conductivity method. Seventeen TMJ discs were harvested from nine males (77 ± 4 years) and eight females (86 ± 4 years). Specimens were prepared from the anterior band, posterior band, intermediate zone, medial disc and lateral disc. FCD was determined using an electrical conductivity method, assessing differences among disc regions and between sexes. Statistical modeling showed significant effects for donor sex (p = 0.002), with cross-region FCD for male discs 0.051 ± 0.018 milliequivalent moles per gram (mEq/g) wet tissue and 0.043 ± 0.020 mEq/g wet tissue for female discs. FCD was significantly higher for male discs compared to female discs in the posterior band, with FCD 0.063 ± 0.015 mEq/g wet tissue for male discs and 0.032 ± 0.020 mEq/g wet tissue for female discs (p = 0.050). These results indicate FCD contributes approximately 20% towards TMJ disc compressive modulus, through osmotic swelling pressure regulation. Additionally, FCD regulates critical extracellular ionic/osmotic and nutrient environments. Sexual dimorphisms in TMJ disc FCD, and resulting differences in extracellular ionic/osmotic and nutrient environments, could result in altered mechano–electro-chemical environments between males and females and requires further study.
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Bibby, S. R., D. A. Jones, R. M. Ripley, and J. P. Urban. Metabolism of the intervertebral disc: effects of low levels of oxygen, glucose, and pH on rates of energy metabolism of bovine nucleus pulposus cells. Spine (Phila. Pa 1976) 30:487–496, 2005.
Chen, C. T., K. W. Fishbein, P. A. Torzilli, A. Hilger, R. G. Spencer, and W. E. Horton, Jr. Matrix fixed-charge density as determined by magnetic resonance microscopy of bioreactor-derived hyaline cartilage correlates with biochemical and biomechanical properties. Arthritis Rheum. 48:1047–1056, 2003.
Cisewski, S. E., L. Zhang, J. Kuo, G. J. Wright, Y. Wu, M. J. Kern, and H. Yao. The effects of oxygen level and glucose concentration on the metabolism of porcine TMJ disc cells. Osteoarthr. Cartil. 23:1790–1796, 2015.
Comper, W. D., and T. C. Laurent. Physiological function of connective tissue polysaccharides. Physiol. Rev. 58:255–315, 1978.
Cortes, D. H., N. T. Jacobs, J. F. DeLucca, and D. M. Elliott. Elastic, permeability and swelling properties of human intervertebral disc tissues: a benchmark for tissue engineering. J. Biomech. 47:2088–2094, 2014.
Detamore, M. S., J. G. Orfanos, A. J. Almarza, M. M. French, M. E. Wong, and K. A. Athanasiou. Quantitative analysis and comparative regional investigation of the extracellular matrix of the porcine temporomandibular joint disc. Matrix Biol. 24:45–57, 2005.
Grodzinsky, A. J. Electromechanical and physicochemical properties of connective tissue. Crit. Rev. Biomed. Eng. 9:133–199, 1983.
Gu, W. Y., W. M. Lai, and V. C. Mow. A mixture theory for charged-hydrated soft tissues containing multi-electrolytes: passive transport and swelling behaviors. J. Biomech. Eng. 120:169–180, 1998.
Gu, W. Y., and H. Yao. Effects of hydration and fixed charge density on fluid transport in charged hydrated soft tissues. Ann. Biomed. Eng. 31:1162–1170, 2003.
Hansson, T., T. Oberg, G. E. Carlsson, and S. Kopp. Thickness of the soft tissue layers and the articular disk in the temporomandibular joint. Acta Odontol. Scand. 35:77–83, 1977.
Hasegawa, I., S. Kuriki, S. Matsuno, and G. Matsumoto. Dependence of electrical conductivity on fixed charge density in articular cartilage. Clin. Orthop. Relat. Res. 177:283–288, 1983.
Haskin, C. L., S. B. Milam, and I. L. Cameron. Pathogenesis of degenerative joint disease in the human temporomandibular joint. Crit. Rev. Oral Biol. Med. 6:248–277, 1995.
Jackson, A. R., F. Travascio, and W. Y. Gu. Effect of mechanical loading on electrical conductivity in human intervertebral disk. J. Biomech. Eng. 131:054505, 2009.
Jackson, A. R., T. Y. Yuan, C. Y. Huang, and W. Y. Gu. A conductivity approach to measuring fixed charge density in intervertebral disc tissue. Ann. Biomed. Eng. 37:2566–2573, 2009.
Kuo, J., L. Zhang, T. Bacro, and H. Yao. The region-dependent biphasic viscoelastic properties of human temporomandibular joint discs under confined compression. J. Biomech. 43:1316–1321, 2010.
Lai, W. M., J. S. Hou, and V. C. Mow. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J. Biomech. Eng. 113:245–258, 1991.
LeResche, L. Epidemiology of temporomandibular disorders: implications for the investigation of etiologic factors. Crit. Rev. Oral Biol. Med. 8:291–305, 1997.
Lu, X. L., and V. C. Mow. Biomechanics of articular cartilage and determination of material properties. Med. Sci. Sports Exerc. 40:193–199, 2008.
Lu, X. L., V. C. Mow, and X. E. Guo. Proteoglycans and mechanical behavior of condylar cartilage. J. Dent. Res. 88:244–248, 2009.
Lu, X. L., D. D. Sun, X. E. Guo, F. H. Chen, W. M. Lai, and V. C. Mow. Indentation determined mechanoelectrochemical properties and fixed charge density of articular cartilage. Ann. Biomed. Eng. 32:370–379, 2004.
Maroudas, A. Physicochemical properties of cartilage in the light of ion exchange theory. Biophys. J. 8:575–595, 1968.
Maroudas, A., and H. Thomas. A simple physicochemical micromethod for determining fixed anionic groups in connective tissue. Biochim. Biophys. Acta 215:214–216, 1970.
Morrow, D., R. H. Tallents, R. W. Katzberg, W. C. Murphy, and T. C. Hart. Relationship of other joint problems and anterior disc position in symptomatic TMD patients and in asymptomatic volunteers. J. Orofac. Pain 10:15–20, 1996.
Mow, V. C., S. C. Kuei, W. M. Lai, and C. G. Armstrong. Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. J. Biomech. Eng. 102:73–84, 1980.
Mow, V. C., and A. Ratcliffe. Structure and function of articular cartilage and meniscus. In: Basic Orthopaedic Biomechanics, edited by V. C. Mow, and W. C. Hayes. New York: Lippincott-Raven, 1997, pp. 113–177.
Perie, D., D. Korda, and J. C. Iatridis. Confined compression experiments on bovine nucleus pulposus and annulus fibrosus: sensitivity of the experiment in the determination of compressive modulus and hydraulic permeability. J. Biomech. 38:2164–2171, 2005.
Pritchard, S., and F. Guilak. The role of F-actin in hypo-osmotically induced cell volume change and calcium signaling in anulus fibrosus cells. Ann. Biomed. Eng. 32:103–111, 2004.
Ribeiro, R. F., R. H. Tallents, R. W. Katzberg, W. C. Murphy, M. E. Moss, A. C. Magalhaes, and O. Tavano. The prevalence of disc displacement in symptomatic and asymptomatic volunteers aged 6 to 25 years. J. Orofac. Pain 11:37–47, 1997.
Roberts, S., J. Menage, and J. P. Urban. Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine (Phila. Pa 1976) 14:166–174, 1989.
Sun, D. D., X. E. Guo, M. Likhitpanichkul, W. M. Lai, and V. C. Mow. The influence of the fixed negative charges on mechanical and electrical behaviors of articular cartilage under unconfined compression. J. Biomech. Eng. 126:6–16, 2004.
Urban, J. P. G., and A. Maroudas. The measurement of fixed charged density in the intervertebral disc. Biochim. Biophys. Acta Gen. Subj. 586:166–178, 1979.
Urban, J. P., and J. F. McMullin. Swelling pressure of the lumbar intervertebral discs: influence of age, spinal level, composition, and degeneration. Spine (Phila. Pa 1976) 13:179–187, 1988.
Wan, L. Q., C. Miller, X. E. Guo, and V. C. Mow. Fixed electrical charges and mobile ions affect the measurable mechano-electrochemical properties of charged-hydrated biological tissues: the articular cartilage paradigm. Mech. Chem. Biosyst. 1:81–99, 2004.
Wright, G. J., J. Kuo, C. Shi, T. R. Bacro, E. H. Slate, and H. Yao. Effect of mechanical strain on solute diffusion in human TMJ discs: an electrical conductivity study. Ann. Biomed. Eng. 41:2349–2357, 2013.
Wu, Y., S. E. Cisewski, Y. Sun, B. J. Damon, B. L. Sachs, V. D. Pellegrini, E. H. Slate, and H. Yao. Quantifying baseline fixed charge density in healthy human cartilage endplate. Spine 2017. https://doi.org/10.1097/BRS.0000000000002061.
Wuertz, K., J. P. Urban, J. Klasen, A. Ignatius, H. J. Wilke, L. Claes, and C. Neidlinger-Wilke. Influence of extracellular osmolarity and mechanical stimulation on gene expression of intervertebral disc cells. J. Orthop. Res. 25:1513–1522, 2007.
Yao, H., M. A. Justiz, D. Flagler, and W. Y. Gu. Effects of swelling pressure and hydraulic permeability on dynamic compressive behavior of lumbar annulus fibrosus. Ann. Biomed. Eng. 30:1234–1241, 2002.
Acknowledgments
This Project was supported by NIH Grants DE018741 and DE021134, a NIH F31 Pre-doctoral Fellowship DE023482 to GJW, and a NIH T32 Post-doctoral Fellowship DE017551 to MCC.
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None of the authors of this paper have a conflict of interest that might be construed as affecting the conduct or reporting of the work presented.
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Associate Editor Michael S. Detamore oversaw the review of this article.
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Wright, G.J., Coombs, M.C., Wu, Y. et al. Electrical Conductivity Method to Determine Sexual Dimorphisms in Human Temporomandibular Disc Fixed Charge Density. Ann Biomed Eng 46, 310–317 (2018). https://doi.org/10.1007/s10439-017-1963-9
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DOI: https://doi.org/10.1007/s10439-017-1963-9