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Evaluating Anisotropic Properties in the Porcine Temporomandibular Joint Disc Using Nanoindentation

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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

  1. Allen, K. D., and K. A. Athanasiou. Viscoelastic characterization of the porcine temporomandibular joint disc under unconfined compression. J. Biomech. 39:312–322, 2006.

    Article  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  Google Scholar 

  4. 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

    Article  CAS  Google Scholar 

  5. 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.

    Article  CAS  PubMed  Google Scholar 

  6. Briscoe, B. J., L. Fiori, and E. Pelillo. Nano-indentation of polymeric surfaces. J. Phys. D Appl. Phys. 31:2395–2405, 1998.

    Article  CAS  Google Scholar 

  7. Cheng, L., X. Xi, L. E. Scriven, and W. W. Gerberich. Spherical-tip indentation of viscoelastic material. Mech. Mater. 37:213–226, 2005

    Article  Google Scholar 

  8. 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

    Article  CAS  PubMed  Google Scholar 

  9. 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

    Article  PubMed  Google Scholar 

  10. 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.

    Article  PubMed  Google Scholar 

  11. de Bont, L. G., R. S. Liem, P. Havinga, and G. Boering. Fibrous component of the temporomandibular joint disc. Cranio 3:368, 1985

    CAS  PubMed  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. Detamore, M. S., and K. A. Athanasiou. Tensile properties of the porcine temporomandibular joint disc. J. Biomech. Eng. 125:558–565, 2003

    Article  PubMed  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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.

    Article  Google Scholar 

  16. 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

    Google Scholar 

  17. 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.

    CAS  Google Scholar 

  18. 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.

    Article  CAS  PubMed  Google Scholar 

  19. Fischer-Cripps, A. C. Nanoindentation. New York: Springer, 2002

    Google Scholar 

  20. 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.

    Article  CAS  PubMed  Google Scholar 

  21. Hebbache, M. Nanoindentation of silicon: hardness and semiconductor–metal phase transition. Mater. Res. Soc. Symp. Proc. 791:177–182, 2004

    CAS  Google Scholar 

  22. Herring, S. W. TMJ anatomy and animal models. J. Musculosk. Neuronal Interact. 3:391–394, 2003

    CAS  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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

    Article  PubMed  Google Scholar 

  27. Johnson, K. L. Contact Mechanics. Cambridge: Cambridge University Press, 1985

    Google Scholar 

  28. 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.

    Article  CAS  PubMed  Google Scholar 

  29. 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

    CAS  Google Scholar 

  30. 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

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  CAS  PubMed  Google Scholar 

  34. 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.

    PubMed  Google Scholar 

  35. 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.

    CAS  PubMed  Google Scholar 

  36. 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.

    Article  CAS  PubMed  Google Scholar 

  37. 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

    Article  CAS  PubMed  Google Scholar 

  38. 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.

    CAS  PubMed  Google Scholar 

  39. 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

    CAS  PubMed  Google Scholar 

  40. Minarelli, A. M., and E. A. Liberti. A microscopic survey of the human temporomandibular joint disc. J. Oral Rehabil. 24:835, 1997

    Article  Google Scholar 

  41. 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

    Article  CAS  PubMed  Google Scholar 

  42. 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

    Article  CAS  PubMed  Google Scholar 

  43. 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

    Article  CAS  Google Scholar 

  44. 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

    Article  PubMed  Google Scholar 

  45. 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.

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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

    CAS  PubMed  Google Scholar 

  48. Sindelar, B. J., and S. W. Herring. Soft tissue mechanics of the temporomandibular joint. Cells Tissues Organs 180:36–43, 2005.

    Article  PubMed  Google Scholar 

  49. 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

    Article  CAS  PubMed  Google Scholar 

  50. 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.

    Article  CAS  PubMed  Google Scholar 

  51. 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.

    Article  PubMed  Google Scholar 

  52. 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.

    Article  CAS  PubMed  Google Scholar 

  53. 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

    Article  CAS  PubMed  Google Scholar 

  54. Tanaka, E., and Van Eijden, T. Biomechanical behavior of the temporomandibular joint disc. Crit. Rev. Oral Biol. Med. 14(2):138–150, 2003

    Article  Google Scholar 

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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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Correspondence to J. A. Turner.

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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

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