0
Research Papers

Effect of Pre-Stress on the Dynamic Tensile Behavior of the TMJ Disc

[+] Author and Article Information
J. Lomakin

Department of Chemical and
Petroleum Engineering,
University of Kansas,
Lawrence, KS 66045

P. A. Sprouse

Bioengineering Program,
University of Kansas,
1530 West 15th Street,
Lawrence, KS 66045

S. H. Gehrke

e-mail: shgehrke@ku.edu
Department of Chemical and
Petroleum Engineering,
University of Kansas,
Lawrence, KS 66045
Bioengineering Program,
University of Kansas,
1530 West 15th Street,
Lawrence, KS 66045

1Present address: Arsenal Medical, 480 Arsenal Street, Watertown, MA 02472.

2Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the JOURNAL OF BIOMECHANICAL ENGINEERING. Manuscript received February 9, 2013; final manuscript received September 16, 2013; accepted manuscript posted October 19, 2013; published online November 26, 2013. Assoc. Editor: Tammy Haut Donahue.

J Biomech Eng 136(1), 011001 (Nov 26, 2013) (8 pages) Paper No: BIO-13-1069; doi: 10.1115/1.4025775 History: Received February 09, 2013; Revised September 16, 2013; Accepted October 19, 2013

Previous dynamic analyses of the temporomandibular joint (TMJ) disc have not included a true preload, i.e., a step stress or strain beyond the initial tare load. However, due to the highly nonlinear stress-strain response of the TMJ disc, we hypothesized that the dynamic mechanical properties would greatly depend on the preload, which could then, in part, account for the large variation in the tensile stiffnesses reported for the TMJ disc in the literature. This study is the first to report the dynamic mechanical properties as a function of prestress. As hypothesized, the storage modulus (E′) of the disc varied by a factor of 25 in the mediolateral direction and a factor of 200 in the anteroposterior direction, depending on the prestress. Multiple constant strain rate sweeps were extracted and superimposed via strain-rate frequency superposition (SRFS), which demonstrated that the strain rate amplitude and strain rate were both important factors in determining the TMJ disc material properties, which is an effect not typically seen with synthetic materials. The presented analysis demonstrated, for the first time, the applicability of viscoelastic models, previously applied to synthetic polymer materials, to a complex hierarchical biomaterial such as the TMJ disc, providing a uniquely comprehensive way to capture the viscoelastic response of biological materials. Finally, we emphasize that the use of a preload, preferably which falls within the linear region of the stress-strain curve, is critical to provide reproducible results for tensile analysis of musculoskeletal tissues. Therefore, we recommend that future dynamic mechanical analyses of the TMJ disc be performed at a controlled prestress corresponding to a strain range of 5–10%.

FIGURES IN THIS ARTICLE
<>
Copyright © 2014 by ASME
Topics: Stress , Disks , Storage
Your Session has timed out. Please sign back in to continue.

References

Kuboki, T., Shinoda, M., Orsini, M. G., and Yamashita, A., 1997, “Viscoelastic Properties of the Pig Temporomandibular Joint Articular Soft Tissues of the Condyle and Disc,” J. Dent. Res., 76(11), pp. 1760–1769. [CrossRef] [PubMed]
Beatty, M. W., Bruno, M. J., Iwasaki, L. R., and Nickel, J. C., 2001, “Strain Rate Dependent Orthotropic Properties of Pristine and Impulsively Loaded Porcine Temporomandibular Joint Disk,” J. Biomed. Mater. Res., 57(1), pp. 25–34. [CrossRef] [PubMed]
Tanaka, E., and van Eijden, T., 2003, “Biomechanical Behavior of the Temporomandibular Joint Disc,” Crit. Rev. Oral. Biol. Med., 14(2), pp. 138–150. [CrossRef] [PubMed]
Detamore, M. S., and Athanasiou, K. A., 2003, “Motivation, Characterization, and Strategy for Tissue Engineering the Temporomandibular Joint Disc,” Tissue Eng., 9(6), pp. 1065–1087. [CrossRef] [PubMed]
Detamore, M. S., and Athanasiou, K. A., 2003, “Structure and Function of the Temporomandibular Joint Disc: Implications for Tissue Engineering,” J. Oral Maxillofac. Surg., 61(4), pp. 494–506. [CrossRef] [PubMed]
Beek, M., Koolstra, J. H., van Ruijven, L. J., and van Eijden, T. M., 2000, “Three-Dimensional Finite Element Analysis of the Human Temporomandibular Joint Disc,” J. Biomech., 33(3), pp. 307–316. [CrossRef] [PubMed]
Donzelli, P. S., Gallo, L. M., Spilker, R. L., and Palla, S., 2004, “Biphasic Finite Element Simulation of the TMJ Disc From In Vivo Kinematic and Geometric Measurements,” J. Biomech., 37(11), pp. 1787–1791. [CrossRef] [PubMed]
Tanaka, E., del Pozo, R., Tanaka, M., Asai, D., Hirose, M., Iwabe, T., and Tanne, K., 2004, “Three-Dimensional Finite Element Analysis of Human Temporomandibular Joint With and Without Disc Displacement During Jaw Opening,” Med. Eng. Phys., 26(6), pp. 503–511. [CrossRef] [PubMed]
Koolstra, J. H., 2003, “Number Crunching With the Human Masticatory System,” J. Dent. Res., 82(9), pp. 672–676. [CrossRef] [PubMed]
Detamore, M. S., and Athanasiou, K. A., 2003, “Tensile Properties of the Porcine Temporomandibular Joint Disc,” ASME J. Biomech. Eng., 125(4), pp. 558–565. [CrossRef]
Rees, L. A., 1954, “The Structure and Function of the Mandibular Joint,” Br. Dent. J., 96(6), pp. 125–133.
Athanasiou, K. A., Almarza, A. J., Detamore, M. S., and Kalpacki, K. N., 2009, Tissue Engineering of Temporomandibular Joint Cartilage, Morgan and Claypool, San Rafael, CA.
Teng, S., Xu, Y., Cheng, M., and Li, Y., 1991, “Biomechanical Properties and Collagen Fiber Orientation of TMJ Discs in Dogs: Part 2. Tensile Mechanical Properties of the Discs,” J. Craniomandib. Disord., 5(2), pp. 107–114. [PubMed]
Scapino, R. P., Obrez, A., and Greising, D., 2006, “Organization and Function of the Collagen Fiber System in the Human Temporomandibular Joint Disk and Its Attachments,” Cells Tissues Organs, 182(3–4), pp. 201–225. [CrossRef] [PubMed]
Tanne, K., Tanaka, E., and Sakuda, M., 1991, “The Elastic Modulus of the Temporomandibular Joint Disc From Adult Dogs,” J. Dent. Res., 70(12), pp. 1545–1548. [CrossRef] [PubMed]
Beek, M., Aarnts, M. P., Koolstra, J. H., Feilzer, A. J., and van Eijden, T. M., 2001, “Dynamic Properties of the Human Temporomandibular Joint Disc,” J. Dent. Res., 80(3), pp. 876–880. [CrossRef] [PubMed]
Tanaka, E., Kawai, N., Hanaoka, K., Van Eijden, T., Sasaki, A., Aoyama, J., Tanaka, M., and Tanne, K., 2004, “Shear Properties of the Temporomandibular Joint Disc in Relation to Compressive and Shear Strain,” J. Dent. Res., 83(6), pp. 476–479. [CrossRef] [PubMed]
Tanaka, E., Kikuzaki, M., Hanaoka, K., Tanaka, M., Sasaki, A., Kawai, N., Ishino, Y., Takeuchi, M., and Tanne, K., 2003, “Dynamic Compressive Properties of Porcine Temporomandibular Joint Disc,” Eur. J. Oral Sci., 111(5), pp. 434–439. [CrossRef] [PubMed]
Tanaka, E., Aoyama, J., Tanaka, M., Van Eijden, T., Sugiyama, M., Hanaoka, K., Watanabe, M., and Tanne, K., 2003, “The Proteoglycan Contents of the Temporomandibular Joint Disc Influence Its Dynamic Viscoelastic Properties,” J. Biomed. Mater. Res. Part A, 65(3), pp. 386–392. [CrossRef]
Tanaka, E., Aoyama, J., Tanaka, M., Murata, H., Hamada, T., and Tanne, K., 2002, “Dynamic Properties of Bovine Temporomandibular Joint Disks Change With Age,” J. Dent. Res., 81(9), pp. 618–622. [CrossRef] [PubMed]
Koolstra, J. H., Tanaka, E., and Van Eijden, T. M., 2007, “Viscoelastic Material Model for the Temporomandibular Joint Disc Derived From Dynamic Shear Tests or Strain–Relaxation Tests,” J. Biomech., 40(10), pp. 2330–2334. [CrossRef] [PubMed]
Beatty, M. W., Nickel, J. C., Iwasaki, L. R., and Leiker, M., 2003, “Mechanical Response of the Porcine Temporomandibular Joint Disc to an Impact Event and Repeated Tensile Loading,” J. Orofac. Pain, 17(2), pp. 160–166. [PubMed]
Snider, G. R., Lomakin, J., Singh, M., Gehrke, S. H., and Detamore, M. S., 2008, “Regional Dynamic Tensile Properties of the TMJ Disc,” J. Dent. Res., 87(11), pp. 1053–1057. [CrossRef] [PubMed]
Fernandez, P., Rey, M. J. L., and Canteli, A. F., 2011, “Viscoelastic Characterisation of the Temporomandibular Joint Disc in Bovines,” Strain, 47(2), pp. 188–193. [CrossRef]
Lamela, M. J., Fernández, P., Ramos, A., Fernández-Canteli, A., and Tanaka, E., 2013, “Dynamic Compressive Properties of Articular Cartilages in the Porcine Temporomandibular Joint,” J. Mech. Behav. Biomed. Mater., 23, pp. 62–70. [CrossRef] [PubMed]
Tanaka, E., Kawai, N., Van Eijden, T., Watanabe, M., Hanaoka, K., Nishi, M., Iwabe, T., and Tanne, K., 2003, “Impulsive Compression Influences the Viscous Behavior of Porcine Temporomandibular Joint Disc,” Eur. J. Oral Sci., 111(4), pp. 353–358. [CrossRef] [PubMed]
Herring, S. W., 2003, “TMJ Anatomy and Animal Models,” J. Musculoskeletal and Neuronal Interact., 3(4), pp. 391–394.
Herring, S. W., 2003, “TMJ Anatomy and Animal Models,” J. Musculoskeletal and Neuronal Interact., 3(4), pp. 406–397.
Oloyede, A., Flachsmann, R., and Broom, N. D., 1992, “The Dramatic Influence of Loading Velocity on the Compressive Response of Articular-Cartilage,” Connect. Tissue Res., 27(4), pp. 211–224. [CrossRef] [PubMed]
Tanaka, E., Tanaka, M., Aoyama, J., Watanabe, M., Hattori, Y., Asai, D., Iwabe, T., Sasaki, A., Sugiyama, M., and Tanne, K., 2002, “Viscoelastic Properties and Residual Strain in a Tensile Creep Test on Bovine Temporomandibular Articular Discs,” Arch. Oral Biol., 47(2), pp. 139–146. [CrossRef] [PubMed]
Chin, L. P. Y., Aker, F. D., and Zarrinnia, K., 1996, “The Viscoelastic Properties of the Human Temporomandibular Joint Disc,” J. Oral Maxillofac. Surg., 54(3), pp. 315–318. [CrossRef] [PubMed]
Tanaka, E., Hanaoka, K., van Eijden, T., Tanaka, M., Watanabe, M., Nishi, M., Kawai, N., Murata, H., Hamada, T., and Tanne, K., 2003, “Dynamic Shear Properties of the Temporomandibular Joint Disc,” Int. Am. Assoc. Dent.Res., 82, pp. 228–231. [CrossRef]
Singh, M., and Detamore, M. S., 2008, “Tensile Properties of the Mandibular Condylar Cartilage,” ASME J. Biomech. Eng., 130(1), p. 011009. [CrossRef]
Allen, K. D., and Athanasiou, K. A., 2005, “A Surface-Regional and Freeze-Thaw Characterization of the Porcine Temporomandibular Joint Disc,” Ann. Biomed. Eng., 33(7), pp. 951–962. [CrossRef] [PubMed]
Ferry, J. D., 1980, Viscoelastic Properties of Polymers, Wiley, New York.
Inman, D. J., 2000, Engineering Vibration, Prentice-Hall, Englewood Cliffs, NJ.
Klemuk, S. A., and Titze, I. R., 2004, “Viscoelastic Properties of Three Vocal-Fold Injectable Biomaterials at Low Audio Frequencies,” Laryngoscope, 114(9), pp. 1597–1603. [CrossRef] [PubMed]
Mavrilas, D., Sinouris, E. A., Vynios, D. H., and Papageorgakopoulou, N., 2005, “Dynamic Mechanical Characteristics of Intact and Structurally Modified Bovine Pericardial Tissues,” J. Biomech., 38(4), pp. 761–768. [CrossRef] [PubMed]
Menard, K. P., 1999, Dynamic Mechanical Analysis: A Practical Introduction, CRC, Boca Raton.
Meredith, N., Alleyne, D., and Cawley, P., 1996, “Quantitative Determination of the Stability of the Implant-Tissue Interface Using Resonance Frequency Analysis,” Clin. Oral Implants Res., 7(3), pp. 261–267. [CrossRef] [PubMed]
Wang, T. G., Hsiao, T. Y., Wang, C. L., and Shau, Y. W., 2007, “Resonance Frequency in Patellar Tendon,” Scand. J. Med. Sci. Sports, 17(5), pp. 535–538. [CrossRef] [PubMed]
Park, S., and Ateshian, G. A., 2006, “Dynamic Response of Immature Bovine Articular Cartilage in Tension and Compression, and Nonlinear Viscoelastic Modeling of the Tensile Response,” ASME J. Biomech. Eng., 128(4), pp. 623–630. [CrossRef]
Wyss, H. M., Miyazaki, K., Mattsson, J.Hu, Z. B., Reichman, D. R., and Weitz, D. A., 2007, “Strain-Rate Frequency Superposition: A Rheological Probe of Structural Relaxation in Soft Materials,” Phys. Rev. Lett., 98(23), p. 4. [CrossRef]
Koenderink, G. H., Atakhorrami, M., MacKintosh, F. C., and Schmidt, C. F., 2006, “High-Frequency Stress Relaxation in Semiflexible Polymer Solutions and Networks,” Phys. Rev. Lett., 96(13), p. 138307. [CrossRef] [PubMed]
Gardel, M. L., Shin, J. H., MacKintosh, F. C., Mahadevan, L., Matsudaira, P. A., and Weitz, D. A., 2004, “Scaling of F-Actin Network Rheology to Probe Single Filament Elasticity and Dynamics,” Phys. Rev. Lett., 93(18), p. 188102. [CrossRef] [PubMed]
Hoffman, B. D., Massiera, G., and Crocker, J. C., 2005, “Forced Unfolding of Protein Domains Determines Cytoskeletal Rheology,” Bull. Am. Phys. Soc., 1, p. 31003.
Kong, H. J., Wong, E., and Mooney, D. J., 2003, “Independent Control of Rigidity and Toughness of Polymeric Hydrogels,” Macromolecules, 36(12), pp. 4582–4588. [CrossRef]
Schwartz, M. H., Leo, P. H., and Lewis, J. L., 1994, “A Microstructural Model for the Elastic Response of Articular-Cartilage,” J. Biomech., 27(7), pp. 865–873. [CrossRef] [PubMed]
Stokes, J. R., and Frith, W. J., 2008, “Rheology of Gelling and Yielding Soft Matter Systems,” Soft Matter, 4(6), pp. 1133–1140. [CrossRef]
Mohan, P. H., and Bandyopadhyay, R., 2008, “Phase Behavior and Dynamics of a Micelle-Forming Triblock Copolymer System,” Phys. Rev. E, 77(4), p. 7. [CrossRef]
Tanaka, E., Detamore, M. S., and Mercuri, L. G., 2008, “Degenerative Disorders of the Temporomandibular Joint: Etiology, Diagnosis, and Treatment,” J. Dent. Res., 87(4), pp. 296–307. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

The nonlinear stress-strain response causes variation in dynamic moduli, depending on the magnitude of the prestress applied before cyclic loading. Dynamic tests using a small prestress measures the properties within the “toe region” of the stress-strain curve, whereas tests using sufficiently larger prestresses measure properties in the linear region. We hypothesized that incorporating larger prestresses up to the linear region would result in larger storage moduli.

Grahic Jump Location
Fig. 2

Representative frequency sweeps of the TMJ disc in the mediolateral direction at 0.1% dynamic strain. (a) The storage modulus increased 2 orders of magnitude with greater prestress and was also a weak function of oscillation frequency. (b) The tan δ decreased as a function of sample prestress. The approximate range of prestrains corresponding to the prestresses was 0–15%.

Grahic Jump Location
Fig. 3

Representative strain sweeps of the TMJ disc in the mediolateral direction at 1 rad/s. (a) The storage modulus was constant, indicating linear viscoelastic behavior, up to 0.1% strain. At greater strains, the storage modulus dipped slightly and then rose. The rise was a consequence of the nonlinear stress-strain response. (b) The tan δ as a function of strain. The approximate range of prestrains corresponding to the prestresses was 0–15%.

Grahic Jump Location
Fig. 4

(a) The storage modulus (E′) at 10 rad/s and 0.1% strain with 95% confidence intervals of the TMJ disc in the mediolateral and anteroposterior directions as a function of the prestress. The modulus appeared directly proportional to the sample prestress. (b) Frequency exponents (n) with 95% confidence intervals. Here, n was calculated from a power law fit of frequency sweeps of the TMJ disc in the mediolateral direction and n appeared to reach a plateau at higher prestresses. The approximate range of prestrains corresponding to the prestresses was 0–15%.

Grahic Jump Location
Fig. 5

Representative frequency sweeps of the TMJ disc in the anteroposterior direction at 0.1% strain. (a) The storage modulus increased 2 orders of magnitude with greater prestress and was also a weak function of the oscillation frequency. (b) The tan δ decreased as a function of the sample prestress. The approximate range of prestrains corresponding to the prestresses was 0–10%.

Grahic Jump Location
Fig. 6

Representative strain sweeps of the TMJ disc in the anteroposterior direction at 10 rad/s. (a) The storage modulus was constant, indicating stable linear viscoelastic behavior, up to 0.1% strain. At greater strains, the storage modulus dipped slightly and then rose. The rise was a consequence of the nonlinear stress-strain response. (b) The tan δ as a function of strain. The approximate range of prestrains corresponding to the prestresses was 0–10%.

Grahic Jump Location
Fig. 7

A representative series of constant rate sweeps at different strain rates for the TMJ disc mediolateral sections at 80 g preload. During each sweep, the applied strain amplitude was inversely proportional to the oscillation frequency.

Grahic Jump Location
Fig. 8

Master curves for the TMJ disc sections. (a) Mediolateral section prestressed with 17.1 Pa. (b) Mediolateral section prestressed with 51.3 Pa. (c) Anteroposterior section prestressed with 308.0 Pa. (d) Anteroposterior section prestressed with 513.3 Pa. The value of the correction factor b was ω−1 and the value of a was experimentally determined to be ω−0.03.

Tables

Errata

Discussions

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging and repositioning the boxes below.

Related Journal Articles
Related eBook Content
Topic Collections

Sorry! You do not have access to this content. For assistance or to subscribe, please contact us:

  • TELEPHONE: 1-800-843-2763 (Toll-free in the USA)
  • EMAIL: asmedigitalcollection@asme.org
Sign In