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Biaxial Testing of Human Annulus Fibrosus and Its Implications for a Constitutive Formulation

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Abstract

Internal pressure in the healthy human annulus fibrosus leads to multiaxial stress in vivo, yet uniaxial tests have been used exclusively to characterize its in vitro mechanical response and to determine its elastic strain energy function (W). We expected that biaxial tension tests would provide unique and necessary data for characterizing the annular material response, and thereby, for determining W. We performed uniaxial and biaxial tests on specimens of annulus, then developed an objective methodology for defining an appropriate form for W that considers data from multiple experiments simultaneously and allows the data to dictate more directly the form and the number of parameters needed. We found that the stresses attained in the biaxial tests were higher, while the strains were considerably lower, than those observed in the uniaxial tests. A comparison of strain energy functions determined from the different data sets demonstrated that constitutive models derived from uniaxial data could not predict annulus behavior in biaxial tension and vice versa. Since the annulus is in a state of multaxial stress in vivo, we conclude that uniaxial tests alone are insufficient to prescribe a physiologically relevant W for this tissue.

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REFERENCES

  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.

    Google Scholar 

  2. Bass, E. C. Biaxial Nonlinear Elastic Response of the Human Lumbar Annulus Fibrosus and Its Role in the Determination of a Physiologically Relevant Constitutive Relation. PhD Thesis, Mechanical Engineering, University of California at Berkeley, 1999.

    Google Scholar 

  3. Best, B. A., F. Guilak, L. A. Setton, W. Zhu, N. F. Saed, 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.

    Google Scholar 

  4. Best, B. A., L. A. Setton, F. Guilak, A. Ratcliffe, M. Weidenbaum, and V. C. Mow. Permeability and compressive stiffness of annulus fibrosus: Variation with site and composition. Trans***. ORS 14:354, 1989.

    Google Scholar 

  5. Brinckmann, P. Injury of the annulus fibrosus and disc protrusions***. An in vitro investigation on human lumbar discsq. Spine11:149–153, 1986.

    Google Scholar 

  6. Debes, J. C., and Y. C. Fung. Effect of temperature on the biaxial mechanics of excised lung parenchyma of the dog. J. Appl. Physiol.73:1171–1180, 1992.

    Google Scholar 

  7. Debes, J.C., andY.C. Fung. Biaxialmechanics of excised canine pulmonary arteries. Am. J. Physiol. 269:H433–H442, 1995.

    Google Scholar 

  8. Duncan, N. A., and J. C. Lotz. Experimental validation of a porohyperelastic finite element model of the annulus fibrosus. In: Computer Methods in Biomechanics & Biomedical Engineering-2, edited by J. Middleton, M. L. Jones, and G. N. Pande. New York: Gordon and Breach, 1998, pp. 527–534.

    Google Scholar 

  9. Ebara, S., J. C. Iatridis, L. A. Setton, R. J. Foster, V. C. Mow, and M. Weidenbaum. Tensile properties of nondegenerate human lumbar anulus fibrosus. Spine 21:452–461, 1996.

    Google Scholar 

  10. Elliott, D. M., M. A. LeRoux, T. A. Laursen, and L. A. Setton. Formulation of a continuum anisotropic model for the anulus fibrosus in tension. Adv. Bioeng.43:165–166, 1997.

    Google Scholar 

  11. Elliott, D. M., and L. A. Setton. Anisotropic and inhomogeneous tensile behavior of the human anulus fibrosus: Experimental measurement and material model predictions. J. Biomech. Eng. 123:256–263, 2001.

    Google Scholar 

  12. Flynn, D. M., G. D. Peura, P. Grigg, and A. H. Hoffman. A finite element based method to determine the properties of planar soft tissue. J. Biomech. Eng. 120:202–210, 1998.

    Google Scholar 

  13. Fujita, Y., N. A. Duncan, and J. C. Lotz. Radial tensile properties of the lumbar annulus fibrosus are site and degeneration dependent. J. Orthop. Res. 15:814–819, 1997.

    Google Scholar 

  14. Fung, Y. C., K. Fronek, and P. Patitucci. Pseudoelasticity of arteries and the choice of its mathematical expression. Am. J. Physiol. 237:H620–H631, 1979.

    Google Scholar 

  15. Galante, J. O. Tensile properties of the human lumbar annulus fibrosus. Acta Orthop. Scand. Suppl.100:1–91, 1967.

    Google Scholar 

  16. Green, A. E., and J. E. Adkins. Large Elastic Deformations. Oxford: Clarendon Press, 1970, 324 pp.

    Google Scholar 

  17. Green, T. P., M. A. Adams, and P. Dolan. Tensile properties of the annulus fibrosus. Ii: Ultimate tensile strength and fatigue life. Eur. Spine J. 2:209–214, 1993.

    Google Scholar 

  18. Humphrey, J. D., R. K. Strumpf, and F. C. Yin. Biaxial mechanical behavior of excised ventricular epicardium. Am. J. Physiol. 259:H101–H108, 1990.

    Google Scholar 

  19. Humphrey, J. D., R. K. Strumpf, and F. C. Yin. Determination of a constitutive relation for passive myocardium: I. A new functional form. J. Biomech. Eng. 112:333–339, 1990.

    Google Scholar 

  20. Humphrey, J. D., R. K. Strumpf, and F. C. Yin. Determination of a constitutive relation for passive myocardium: II. Parameter estimation. J. Biomech. Eng. 112:340–346, 1990.

    Google Scholar 

  21. Humphrey, J. D., R. K. Strumpf, and F. C. Yin. A constitutive theory for biomembranes: Application to epicardial mechanics. J. Biomech. Eng. 114:461–466, 1992.

    Google Scholar 

  22. Humphrey, J. D., D. L. Vawter, and R. P. Vito. Quantification of strains in biaxially tested soft tissues. J. Biomech. 20:59–65, 1987.

    Google Scholar 

  23. James, A. G., A. Green, and G. M. Simpson. Strain-energy functions of rubber i: Characterization of gum vulcanates. J. Appl. Poly. Sci. 19:2033–2058, 1975.

    Google Scholar 

  24. Jones, D. F., and L. R. G. Treloar. The properties of rubber in pure homogeneous strain. J. Phys. D 8:1285–1304, 1975.

    Google Scholar 

  25. Kang, T., J. D. Humphrey, and F. C. Yin. Comparison of biaxial mechanical properties of excised endocardium and epicardium. Am. J. Physiol. 270:H2169–H2176, 1996.

    Google Scholar 

  26. Klisch, S. M., and J. C. Lotz. Application of a fiber-reinforced continuum theory to multiple deformations of the annulus fibrosus. J. Biomech. 32:1027–1036, 1999.

    Google Scholar 

  27. Lanir, Y., and Y. C. Fung. Two-dimensional mechanical properties of rabbit skin. Ii. Experimental results. J. Biomech. 7:171–182, 1974.

    Google Scholar 

  28. Mansour, J. M., and V. C. Mow. The permeability of articular cartilage under compressive strain and at high pressures. J. Bone Joint Surg. [Am.] 58:509–516, 1976.

    Google Scholar 

  29. Marchand, F., and A. M. Ahmed. Mechanical properties and failure mechanisms of the lumbar disc annulus. Trans. ORS 14:355, 1989.

    Google Scholar 

  30. Markolf, K. L., and J. M. Morris. The structural components of the intervertebral disc. A study of their contributions to the ability of the disc to withstand compressive forces. J. Bone Joint Surg. [Am.] 56:675–687, 1974.

    Google Scholar 

  31. Ogden, R. W. Biaxial deformation of rubber-like solids: Comparison of theory and experiment. J. Phys. D 12:1463–1472, 1979.

    Google Scholar 

  32. Ogden, R. W. Non-Linear Elastic Deformations. Chichester, UK: Ellis Horwood, 1984, 532 pp.

    Google Scholar 

  33. Rivlin, R. S., and D. W. Saunders. Large elastic deformations of isotropic materials: Vii. Experiments on the deformation of rubber. In: Collected Papers of R.S. Rivlin, edited by G. I. Barenblatt and D. D. Joseph. New York: Springer, 1997, 1997, pp. 157–194.

    Google Scholar 

  34. Sacks, M. S., and C. J. Chuong. Orthotropic mechanical properties of chemically treated bovine pericardium. Ann. Biomed. Eng. 26:892–902, 1998.

    Google Scholar 

  35. Shirazi-Adl, A., S. C. Shrivastava, and A. M. Ahmed. Stress analysis of the lumbar disc-body unit in compression. A threedimensional nonlinear finite element study. Spine 9:120–134, 1984.

    Google Scholar 

  36. Skaggs, D. L., M. Weidenbaum, J. C. Iatridis, A. Ratcliffe, and V. C. Mow. Regional variation in tensile properties and biochemical composition of the human lumbar anulus fibrosus. Spine 19:1310–1319, 1994.

    Google Scholar 

  37. Stokes, I. A. Surface strain on human intervertebral discs. J. Orthop. Res.5:348–355, 1987.

    Google Scholar 

  38. 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 15:411–415, 1990.

    Google Scholar 

  39. Tong, P., and Y. C. Fung. The stress-strain relationship for the skin. J. Biomech. 9:649–657, 1976.

    Google Scholar 

  40. Vaishnav, R. N., J. T. Young, J. S. Janicki, and D. J. Patel. Nonlinear anisotropic elastic properties of the canine aorta. Biophys. J. 12:1008–1027, 1972.

    Google Scholar 

  41. Vangerko, H., and L. R. G. Treloar. The inflation and extension of rubber tube for biaxial strain studies. J. Phys. D 11:1969–1978, 1978.

    Google Scholar 

  42. Vawter, D. L., Y. C. Fung, and J. B. West. Constitutive equation of lung elasticity. J. Biomech. Eng. 101:38–45, 1979.

    Google Scholar 

  43. Vorp, D.A., K. R. Rajagopal, P. J. Smolinski, and H. S. Borovetz. Identification of elastic properties of homogeneous, orthotropic vascular segments in distension. J. Biomech.28:501–512, 1995.

    Google Scholar 

  44. Wagner, D. R., and J. C. Lotz. Theoretical model and experimental results for the nonlinear elastic behavior of human annulus fibrosus. J. Orthop. Res., 22:901–909, 2004.

    Google Scholar 

  45. Waldman, S. D., and M. J. Lee. Boundary conditions during biaxial testing of planar connective tissues. Part 1: Dynamic behaviour. J. Mater. Sci. 13:933–938, 2002.

    Google Scholar 

  46. Wu, H. C., and R. F. Yao. Mechanical behavior of the human annulus fibrosus. J. Biomech. 9:1–7, 1976.

    Google Scholar 

  47. Yin, F. C., R. K. Strumpf, P. H. Hew, and S. L. Zeger. Quantification of the mechanical properties of noncontracting canine myocardium under simultaneous biaxial loading. J. Biomech. 20:577–589, 1987.

    Google Scholar 

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Bass, E.C., Ashford, F.A., Segal, M.R. et al. Biaxial Testing of Human Annulus Fibrosus and Its Implications for a Constitutive Formulation. Annals of Biomedical Engineering 32, 1231–1242 (2004). https://doi.org/10.1114/B:ABME.0000039357.70905.94

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  • DOI: https://doi.org/10.1114/B:ABME.0000039357.70905.94

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