Abstract
The objective of this study was to determine the viscoelastic properties present within the intermediate zone of the porcine temporomandibular joint (TMJ) disc using nanoindentation. A 50-μm conospherical indenter tip using a displacement-controlled ramp function with a 600 nm/s loading and unloading rate, a 3000-nm peak displacement with a holding period of 30 s was used to indent the samples. Experimental load-relaxation tests were performed on the TMJ disc to determine the response in three different directions; the mediolateral, anteroposterior, and articular surface directions. The experimental data were analyzed using a generalized Maxwell model to obtain values for short- and long-time relaxation modulus and of material time constants. The short time relaxation modulus E I values were 180.92, 64.99, and 487.77 kPa for testing done on the articular surface, mediolateral, and anteroposterior directions, respectively. Corresponding values for the long-time relaxation modulus E ∞ were 45.9, 14.97, and 133.5 kPa. The method confirmed anisotropy present within the central intermediate zone of the porcine TMJ disc due to the directional orientation of the collagen fibers.
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References
Allen, K. D., and K. A. Athanasiou. Viscoelastic characterization of the porcine temporomandibular joint disc under unconfined compression. J. Biomech. 39:312–322, 2006.
Almarza, A., and K. Athanasiou. Evaluation of three growth factors in combinations of two for temporomandibular joint disc tissue engineering. Arch. Oral Biol. 51:215–221, 2006
Asif, S. A. S., K. J. Wahl, and R. J. Colton. Nanoindentation and contact stiffness measurement using force modulation with a capacitive load–displacement transducer. Rev. Sci. Instrum. 70(5):2408–2413, 1999
Beatty, M. W., M. J. Bruno, L. R. Iwasaki, and J. C. Nickel. Strain rate dependent orthotropic properties of pristine and impulsively loaded porcine temporomandibular joint disk. J. Biomed. Res. 57:25–34, 2001
Beek, M., M. Aarnts, J. Koolstra, A. Feilzer, and T. VanEijden. Dynamic properties of the human temporomandibular joint disc. J. Dent. Res. 80(3):876–880, 2001.
Briscoe, B. J., L. Fiori, and E. Pelillo. Nano-indentation of polymeric surfaces. J. Phys. D Appl. Phys. 31:2395–2405, 1998.
Cheng, L., X. Xi, L. E. Scriven, and W. W. Gerberich. Spherical-tip indentation of viscoelastic material. Mech. Mater. 37:213–226, 2005
Chin, L. P. Y., F. D. Aker, and K. Zarrinnia. The viscoelastic properties of the human temporomandibular joint disc. J. Oral Maxillofac. Surg. 54(3):315–318, 1996
Colombo, V., S. Palla, and L. M. Gallo. Temporomandibular joint loading patterns related to joint morphology: a theoretical study. Cells Tissues Organs 187:295–306, 2008
Constantinides, G., Z. I. Kalcioglu, F. J. Smith, M. McFarland, and K. J. VanVliet. Probing mechanical properties of fully hydrated gels and biological tissues. J. Biomech. 41:3285–3289, 2008.
de Bont, L. G., R. S. Liem, P. Havinga, and G. Boering. Fibrous component of the temporomandibular joint disc. Cranio 3:368, 1985
Detamore, M. S., and K. A. Athanasiou. Structure and function of the temporomandibular joint disc: implications for tissue engineering. J. Oral Maxillofac. Surg. 61(4):494–506, 2003
Detamore, M. S., and K. A. Athanasiou. Tensile properties of the porcine temporomandibular joint disc. J. Biomech. Eng. 125:558–565, 2003
Detamore, M. S., and K. A. Athanasiou. Motivation, characterization, and strategy for tissue engineering the temporomandibular joint disc. Tissue Eng. 9(6):1065–1087, 2004
Donzellia, P. S., L. M. Gallob, R. L. Spilker, and S. Palla. Biphasic finite element simulation of the TMJ disc from in vivo kinematic and geometric measurements. J. Biomech. 37:1787–1791, 2004.
Ebenstein, D. M., D. Coughlin, J. Chapman, C. Li, and L. A. Pruitt. Nanomechanical properties of calcification, fibrous tissue, and hematoma from atherosclerotic plaques. J. Biomed. Mater. Res. A 91A:1028–1037, 2008
Ebenstein, D. M., A. Kuo, J. J. Rodrigo, A. H. Reddi, M. Ries, and L. Pruitt. A nanoindentation technique for functional evaluation of cartilage repair tissue. J. Mater. Res. 19:273–281, 2004.
Ebenstein, D. M., and L. A. Pruitt. Nanoindentation of soft hydrated materials for application to vascular tissues. J. Biomed. Mater. Res. A 69A:222–232, 2004.
Fischer-Cripps, A. C. Nanoindentation. New York: Springer, 2002
Gallo, L. M., J. C. Nickel, L. R. Iwasaki, and S. Palla. Stress-field translation in the healthy human temporomandibular joint. J. Dent. Res. 79:1740–1746, 2000.
Hebbache, M. Nanoindentation of silicon: hardness and semiconductor–metal phase transition. Mater. Res. Soc. Symp. Proc. 791:177–182, 2004
Herring, S. W. TMJ anatomy and animal models. J. Musculosk. Neuronal Interact. 3:391–394, 2003
Herring, S. W., J. D. Decker, Z. J. Liu, and T. Ma. The temporomandibular joint in miniature pigs: anatomy, cell replication, and relation to loading. Anat. Rec. 266:152–166, 2002
Herring, S. W., K. L. Rafferty, Z. J. Liu, and C. D. Marshall. Jaw muscles and the skull in mammals: the biomechanics of mastication. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 131:207–219, 2001
Hoffler, C. E., X. E. Guo, P. K. Zysset, and S. A. Goldstein. An application of nanoindentation technique to measure bone tissue lamellae properties. J. Biomech. Eng. 125:1046–1053, 2005
Hongo, M., R. E. Gay, J. T. Hsu, K. D. Zhao, B. Ilharreborde, L. J. Berglund, and K. N. An. Effect of multiple freeze–thaw cycles on intervertebral dynamic motion characteristics in the porcine lumbar spine. J. Biomech. 41(4):916–920, 2008
Johnson, K. L. Contact Mechanics. Cambridge: Cambridge University Press, 1985
Kaufman, J. D., G. J. Miller, E. F. Morgan, and C. M. Klapperich. Time-dependent mechanical characterization of poly(2-hydroxyethyl methacrylate) hydrogels using nanoindentation and unconfined compression. J. Mater. Res. 23(5):1472–1481, 2008.
Khanna, S. K., P. Ranganathan, S. Yedla, R. Winter, and K. Puruchuri. Investigation of nanomechanical properties of the interphase in a glass fiber reinforced polyester composites using nanoindentation. Trans. ASME 125:90–96, 2003
Kiefer, G. N., K. Sundby, D. McAllister, N.G. Shrive, C. B. Frank, T. Lam, and N. S. Schachar. The effect of cryopreservation on the biomechanical behavior of bovine articular cartilage. J. Orthop. Res. 7(4):494–501, 1989
Kim, K. W., M. E. Wong, J. F. Helfrick, J. B. Thomas, and K. A. Athanasiou. Biomechanical tissue characterization of the superior joint space of the porcine temporomandibular joint. Ann. Biomed. Eng. 31:924–930, 2003
Koolstra, J. H., E. Tanaka, and T. M. G. J. V. Eijden. Viscoelastic material model for the temporomandibular joint disc derived from dynamic shear tests or strain-relaxation tests. J. Biomech., 40:2330–2334, 2007.
Kuboki, T., M. Shinoda, M. Orsini, and A. Yamashita. Viscoelastic properties of the pig temporomandibular joint articular soft tissues of the condyle and disc. J. Dent. Res. 76(11):1760–1769, 1997
Li, C., L. A. Pruitt, and K. B. King. Nanoindentation differentiates tissue-scale functional properties of native articular cartilage. J. Biomed. Mater. Res. A 78A:729–738, 2006.
Liu, Z. J., and S. W. Herring. Masticatory strains on osseous and ligamentous components of the jaw joint in miniature pigs. J. Orofac. Pain 14:265–278, 2000.
Milam, S. B., R. J. Klebe, R. G. Triplett, and D. Herbert. Characterization of the extracellular matrix of the primate temporomandibular joint. J. Oral Maxillofac. Surg. 49:381–391, 1991.
Mills, D. K., D. J. Fiandaca, and R. P. Scapino. Histological features and in-vitro proteoglycan synthesis in the rabbit craniomandibular joint disc. Arch. Oral Biol. 33:195–202, 1988
Mills, D. K., D. J. Fiandaca, and R. P. Scapino. Morphologic, microscopic, and immunohistochemical investigations into the function of the primate TMJ disc. J. Orofac. Pain 8:136–154, 1994.
Minarelli, A. M., M. Delsanto, and E. A. Liberti. The structure of the human temporomandibular joint disc: a scanning electron microscopy study. J. Orofac. Pain 11(2):95–100, 1997
Minarelli, A. M., and E. A. Liberti. A microscopic survey of the human temporomandibular joint disc. J. Oral Rehabil. 24:835, 1997
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
Nickel, J. C., R. Spilker, L. R. Iwasaki, Y. Gonzalez, W. D. McCall, R. Ohrbach, M. W. Beatty, and D. Marx. Static and dynamic mechanics of the temporomandibular joint: plowing forces, joint load and tissue stress. Orthod. Craniofac. Res. 12:159–167, 2009
Oliver, W., and G. Pharr. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7:1564–1583, 1992
Pozo, R. D., E. Tanaka, M. Tanaka, M. Okazaki, and K. Tanne. The Regional difference of viscoelastic property of bovine temporomandibular joint disc in compressive stress–relaxation. Med. Eng. Phys. 24:165–171, 2002
Scapino, R. P., P. B. Canham, H. M. Finlay, and D. K. Mills. The behavior of collagen fibres in stress relaxation and stress distribution in the jaw-joint disc of rabbits. Arch. Oral Biol. 41:1039–1052, 1996.
Scapino, R. P., A. Obrez, and D. Greising. Organization and function of the collagen fiber system in the human temporomandibular joint disk and its attachments. Cells Tissues Organs 182:201–225, 2006
Shengyi, T., and X. Yinghua. Biochemical properties and collagen fiber orientation of TMJ disc in dogs: part 1. Gross anatomy and collagen fiber orientation of the disc. J. Craniomandib. Disord. 5:28, 1991
Sindelar, B. J., and S. W. Herring. Soft tissue mechanics of the temporomandibular joint. Cells Tissues Organs 180:36–43, 2005.
Snider, G., J. Lomakin, M. Singh, S. Gehrke, and M. Detamore. Regional dynamic tensile properties of the TMJ disc. J. Dent. Res. 87(11):1053–1057, 2008
Stolz, M., R. Raiteri, A. U. Daniels, M. R. Van Landingham, W. Baschong, and U. Aebi. Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. Biophys. J. 86:3269–3283, 2004.
Sun, Z., Z. J. Liu, and S.W. Herring. Movement of temporomandibular tissues during mastication and passive manipulation in miniature pigs. Arch. Oral Biol. 47:293–305, 2002.
Tanaka, E., K. Hanaoka, T. VanEijden, M. Tanaka, M. Watanabe, M. Nishi, N. Kawai, H. Murata, T. Hamada, and K. Tanne. Dynamic shear properties of the temporomandibular joint disc. J. Dent. Res. 82(3):228–231, 2003.
Tanaka, E., N. Kawai, K. Hanaoka, T. V. Eijden, A. Sasaki, J. Aoyama, M. Tanaka, and K. Tanne. Shear properties of the temporomandibular joint disc in relation to compressive and shear strain. J. Dent. Res. 83(6):476–479, 2004
Tanaka, E., and Van Eijden, T. Biomechanical behavior of the temporomandibular joint disc. Crit. Rev. Oral Biol. Med. 14(2):138–150, 2003
Acknowledgments
This work was supported in part by the National Science Foundation and the UCARE (Undergraduate Creative Activities and Research Experiences) program at UNL. The authors are grateful for the thoughtful (and thought-provoking) reviewer comments and suggestions.
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Associate Editor Eiji Tanaka oversaw the review of this article.
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Yuya, P.A., Amborn, E.K., Beatty, M.W. et al. Evaluating Anisotropic Properties in the Porcine Temporomandibular Joint Disc Using Nanoindentation. Ann Biomed Eng 38, 2428–2437 (2010). https://doi.org/10.1007/s10439-010-9967-8
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DOI: https://doi.org/10.1007/s10439-010-9967-8