Advertisement

Correlating Material Properties with Tissue Composition in Enzymatically Digested Bovine Annulus Fibrosus and Nucleus Pulposus Tissue

  • Delphine S. PerieEmail author
  • Jeff J. Maclean
  • Julia P. Owen
  • James C. Iatridis
Article

Abstract

Aging and degeneration of the intervertebral disk are accompanied by decreases in water and proteoglycan contents, and structural alterations. The aim of this study was to determine the impact of compositional changes on the material properties of intervertebral disk tissues. Confined compression stress-relaxation experiments were applied to bovine caudal annulus fibrosus and nucleus pulposus tissue specimens that were separated into three experimental groups: in situ, free-swelling control (PBS), and digestion (chondroitinase-ABC). Measurements of glycosaminoglycan (GAG) and water content, as well as nonlinear finite deformation biphasic theory and multiple linear regression analyses were performed. The compressive modulus H A0 and permeability k 0 of in situ specimens were 0.37±0.06 MPa and 0.49±0.08×10−15 m4 N−1 s−1 for nucleus, and 0.74±0.13 MPa and 0.42±0.05×10−15 m4 N−1 s−1 for annulus, respectively. There was a larger effect of swelling and digestion on the material properties and biochemical composition of nucleus pulposus than for annulus fibrosus. Alterations in proteoglycan and water content affected the compressive modulus and permeability, although the permeability was somewhat more strongly affected by water content than by proteoglycan content. Correlation coefficients r≤0.75 for the multiple regression indicated water and GAG content can moderately predict material properties, however other compositional and structural factors must be considered.

Keywords

Confined compression Intervertebral disk Annulus fibrosus Nucleus pulposus Hydration Proteolytic digestion Compressive modulus Hydraulic permeability 

Notes

ACKNOWLEDGMENTS

Supported by NIH grant 1K01AR02078 and Whitaker Foundation grant RG-03-0030.

REFERENCES

  1. 1.
    Acaroglu, E. R., J. C. Iatridis, L. A. Setton, R. J. Foster, V. C. Mow, and M. Weidenbaum. Degeneration and aging affect the tensile behavior of human lumbar anulus fibrosus. Spine 20:2690–2701, 1995.PubMedCrossRefGoogle Scholar
  2. 2.
    Antoniou, J., T. Steffen, F. Nelson, N. Winterbottom, A. P. Hollander, R. A. Poole, M. Aebi, and M. Alini. The human lumbar intervertebral disc: Evidence for changes in the biosynthesis and denaturation of the extracellular matrix with growth, maturation, ageing, and degeneration. J. Clin. Invest. 98:996–1003, 1996.PubMedCrossRefGoogle Scholar
  3. 3.
    Ateshian, G. A., W. H. Warden, J. J. Kim, R. P. Grelsamer, and V. C. Mow. Finite deformation biphasic material properties of bovine articular cartilage from confined compression experiments. J. Biomech. 30:1157–1164, 1997.PubMedCrossRefGoogle Scholar
  4. 4.
    Bernick, S., J. M. Walker, and W. J. Paule. Age changes to the annulus fibrosus in human intervertebral discs. Spine 16:520–524, 1991.PubMedCrossRefGoogle Scholar
  5. 5.
    Best, B. A., F. Guilak, L. A. Setton, W. Zhu, F. Saed-Nejad, A. Ratcliffe, M. Weidenbaum, and V. C. Mow. Compressive mechanical properties of the human anulus fibrosus and their relationship to biochemical composition. Spine 19:212–221, 1994.PubMedCrossRefGoogle Scholar
  6. 6.
    Brickley-Parsons, D., and M. J. Glimcher. Is the chemistry of collagen in intervertebral discs an expression of Wolff's Law? A study of the human lumbar spine. Spine 9(2):148–163, 1984.PubMedCrossRefGoogle Scholar
  7. 7.
    Buckwalter, J. A.. Aging and degeneration of the human intervertebral disc. Spine 20(11):1307–1314, 1995.PubMedGoogle Scholar
  8. 8.
    Buschmann, M. D., J. Soulhat, A. Shirazi-Adl, J. S. Jurvelin, and E. B. Hunziker. Confined compression of articular cartilage: Linearity in ramp and sinusoidal tests and the importance of interdigitation and incomplete confinement. J. Biomech. 31:171–178, 1998.PubMedCrossRefGoogle Scholar
  9. 9.
    Cassidy, J. J., A. Hiltner, and E. Baer. Hierarchical structure of the intervertebral disc. Connect. Tissue Res. 23(1):75–88, 1989.PubMedCrossRefGoogle Scholar
  10. 10.
    Demers, C. N., J. Antoniou, and F. Mwale. Value and limitations of using the bovine tail as a model for the human lumbar spine. Spine 29(24):2793–2799, 2004.PubMedCrossRefGoogle Scholar
  11. 11.
    Elliott, D. M., and J. J. Sarver. Young investigator award: Validation of the mouse and rat disc as mechanical models of the human lumbar disc. Spine 29(7):713–722, 2004.PubMedCrossRefGoogle Scholar
  12. 12.
    Eyre, D. R., and H. Muir. Quantitative analysis of types I and II collagens in human intervertebral discs at various ages. Biochim. Biophys. Acta 492:29–42, 1977.PubMedGoogle Scholar
  13. 13.
    Farndale, R. W., D. J. Buttle, and A. J. Barrett. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim. Biophys. Acta 883:173–177, 1986.PubMedGoogle Scholar
  14. 14.
    Gu, W. Y., X. G. Mao, R. J. Foster, M. Weidenbaum, V. C. Mow, and B. A. Rawlins. The anisotropic hydraulic permeability of human lumbar annulus fibrosus. Influence of age, degeneration, direction, and water content. Spine 24:2449–2455, 1999.PubMedCrossRefGoogle Scholar
  15. 15.
    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.PubMedCrossRefGoogle Scholar
  16. 16.
    Happey, F., C. H. Pearson, A. Naylor, and R. L. Turner. The ageing of the human intervertebral disc. Gerontologia 15:174–188, 1969.PubMedGoogle Scholar
  17. 17.
    Holmes, M. H., and V. C. Mow. The nonlinear characteristic of soft gels and hydrated connective tissues in ultrafiltration. J. Biomech. 23:1145–1156, 1990.PubMedCrossRefGoogle Scholar
  18. 18.
    Iatridis, J. C., L. A. Setton, M. Weidenbaum, and V. C. Mow. Alterations in the mechanical behavior of the human lumbar nucleus pulposus with degeneration and aging. J. Orthop. Res. 15:318–322, 1997.PubMedCrossRefGoogle Scholar
  19. 19.
    Iatridis, J. C., L. A. Setton, R. J. Foster, B. A. Rawlins, M. Weidenbaum, and V. C. Mow. Degeneration affects the anisotropic and nonlinear behaviors of human annulus fibrosus in compression. J. Biomech.31(6):535–544, 1998.PubMedCrossRefGoogle Scholar
  20. 20.
    Klisch, S. M., and J. C. Lotz. A special theory of biphasic mixtures and experimental results for human annulus fibrosus tested in confined compression. J. Biomech. Eng. 122:180–188, 2000.PubMedCrossRefGoogle Scholar
  21. 21.
    Lyons, G., S. M. Eisenstein, and M. B. Sweet. Biochemical changes in intervertebral disc degeneration. Biochim. Biophys. Acta 673(4):443–453, 1981.PubMedGoogle Scholar
  22. 22.
    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.PubMedCrossRefGoogle Scholar
  23. 23.
    Natarajan, R. N., J. R. Williams, and G. B. Andersson. Recent advances in analytical modeling of lumbar disc degeneration. Spine 29(23):2733–2741, 2004.PubMedCrossRefGoogle Scholar
  24. 24.
    Oshima, H., H. Ishihara, J. P. Urban, and H. Tsuji. The use of coccygeal discs to study intervertebral disc metabolism. J. Orthop. Res. 11(3):332–338, 1993.PubMedCrossRefGoogle Scholar
  25. 25.
    Pearce, R. H., B. J. Grimmer, and M. E. Adams. Degeneration and the chemical composition of the human lumbar intervertebral disc. J. Orthop. Res. 5(2):198–205, 1987.PubMedCrossRefGoogle Scholar
  26. 26.
    Roughley, P. J., R. J. White, M. C. Magny, J. Liu, R. H. Pearce, and J. S. Mort. Non-proteoglycan forms of biglycan increase with age in human articular cartilage. Biochem. J. 295:421–426, 1993.PubMedGoogle Scholar
  27. 27.
    Takahashi, T., H. Kurihara, S. Nakajima, T. Kato, S. Matsuzaka, T. Sekiguchi, M. Onaya, S. Miyauchi, S. Mizuno, and K. Horie. Chemonucleolytic effects of chondroitinase ABC on normal rabbit intervertebral discs. Course of action up to 10 days postinjection and minimum effective dose. Spine 21:2405–2411, 1996.PubMedCrossRefGoogle Scholar
  28. 28.
    Thompson, J. P., R. H. Pearce, M. T. Schechter, M. E. Adams, I. K. Tsang, and P. B. Bishop. Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 15(5):411–415, 1990.PubMedCrossRefGoogle Scholar
  29. 29.
    Umehara, S., S. Tadano, K. Abumi, K. Katagiri, K. Kaneda, and T. Ukai. Effects of degeneration on the elastic modulus distribution in the lumbar intervertebral disc. Spine 21(7):811–819, 1996.PubMedCrossRefGoogle Scholar
  30. 30.
    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(10):1234–1241, 2002.PubMedCrossRefGoogle Scholar

Copyright information

© Biomedical Engineering Society 2006

Authors and Affiliations

  • Delphine S. Perie
    • 1
    • 2
    Email author
  • Jeff J. Maclean
    • 1
  • Julia P. Owen
    • 1
  • James C. Iatridis
    • 1
  1. 1.Department of Mechanical EngineeringUniversity of VermontBurlingtonUSA
  2. 2.Laboratoire de Biomécanique de ToulouseUniversity Toulouse IIIToulouse cedexFrance

Personalised recommendations