Skip to main content

Advertisement

Log in

Refinement of Elastic, Poroelastic, and Osmotic Tissue Properties of Intervertebral Disks to Analyze Behavior in Compression

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Intervertebral disks support compressive forces because of their elastic stiffness as well as the fluid pressures resulting from poroelasticity and the osmotic (swelling) effects. Analytical methods can quantify the relative contributions, but only if correct material properties are used. To identify appropriate tissue properties, an experimental study and finite element analytical simulation of poroelastic and osmotic behavior of intervertebral disks were combined to refine published values of disk and endplate properties to optimize model fit to experimental data. Experimentally, nine human intervertebral disks with adjacent hemi-vertebrae were immersed sequentially in saline baths having concentrations of 0.015, 0.15, and 1.5 M and the loss of compressive force at constant height (force relaxation) was recorded over several hours after equilibration to a 300-N compressive force. Amplitude and time constant terms in exponential force–time curve-fits for experimental and finite element analytical simulations were compared. These experiments and finite element analyses provided data dependent on poroelastic and osmotic properties of the disk tissues. The sensitivities of the model to alterations in tissue material properties were used to obtain refined values of five key material parameters. The relaxation of the force in the three bath concentrations was exponential in form, expressed as mean compressive force loss of 48.7, 55.0, and 140 N, respectively, with time constants of 1.73, 2.78, and 3.40 h. This behavior was analytically well represented by a model having poroelastic and osmotic tissue properties with published tissue properties adjusted by multiplying factors between 0.55 and 2.6. Force relaxation and time constants from the analytical simulations were most sensitive to values of fixed charge density and endplate porosity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

FIGURE 1
FIGURE 2
FIGURE 3
FIGURE 4

Similar content being viewed by others

References

  1. 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(4):996–1003, 1996.

    Article  CAS  PubMed  Google Scholar 

  2. Ayotte, D. C., K. Ito, and S. Tepic. Direction-dependent resistance to flow in the endplate of the intervertebral disc: an ex vivo study. J. Orthop. Res. 19(6):1073–1077, 2001.

    Article  CAS  PubMed  Google Scholar 

  3. Broberg, K. B. On the mechanical behaviour of intervertebral discs. Spine 8(2):151–165, 1983.

    Article  CAS  PubMed  Google Scholar 

  4. Charnley, J. The imbibition of fluid as a cause of herniation of the nucleus pulposus. Lancet 1(6699):124–127, 1952.

    Article  CAS  PubMed  Google Scholar 

  5. Cowin, S. C. Bone poroelasticity. J. Biomech. 32(3):217–238, 1999.

    Article  CAS  PubMed  Google Scholar 

  6. Drost, M. R., P. Willems, H. Snijders, J. M. Huyghe, J. D. Janssen, and A. Huson. Confined compression of canine annulus fibrosus under chemical and mechanical loading. J. Biomech. Eng. 117(4):390–396, 1995.

    Article  CAS  PubMed  Google Scholar 

  7. Ehlers, W., N. Karajan, and B. Markert. An extended biphasic model for charged hydrated tissues with application to the intervertebral disc. Biomech. Model. Mechanobiol. 8(3):233–251, 2009.

    Article  CAS  PubMed  Google Scholar 

  8. Eisenberg, S. R., and A. J. Grodzinsky. Swelling of articular cartilage and other connective tissues: electromechanochemical forces. J. Orthop. Res. 3(2):148–159, 1985.

    Article  CAS  PubMed  Google Scholar 

  9. 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.

    Article  CAS  PubMed  Google Scholar 

  10. Frijns, A. J. H., J. M. Huyghe, and J. D. Janssen. A validation of the quadriphasic mixture theory for intervertebral disc tissue. Int. J. Eng. Sci. 35:1419–1429, 1997.

    Article  CAS  Google Scholar 

  11. Fujita, Y., D. R. Wagner, A. A. Biviji, N. A. Duncan, and J. C. Lotz. Anisotropic shear behavior of the annulus fibrosus: effect of harvest site and tissue prestrain. Med. Eng. Phys. 22:349–357, 2000.

    Article  CAS  PubMed  Google Scholar 

  12. Grodzinsky, A. J., V. Roth, E. Myers, W. D. Grossman, and V. C. Mow. The significance of electromechanical and osmotic forces in the nonequilibrium swelling behavior of articular cartilage in tension. J. Biomech. Eng. 103(4):221–231, 1981.

    Article  CAS  PubMed  Google Scholar 

  13. Gu, W. Y., W. M. Lai, and V. C. Mow. A mixture theory for charged-hydrated soft tissues containing multi-electrolytes: passive transport and swelling behaviors. J. Biomech. Eng. 120:169–180, 1998.

    Article  CAS  PubMed  Google Scholar 

  14. Gu, W. Y., W. M. Lai, and V. C. Mow. Transport of fluid and ions through a porous-permeable charged-hydrated tissue, and streaming potential data on normal bovine articular cartilage. J. Biomech. 26(6):709–723, 1993.

    Article  CAS  PubMed  Google Scholar 

  15. Gu, W. Y., V. C. Mao, R. J. Foster, M. Weidenbaum, V. C. Mow, and B. A. Rawlins. The anisotropic hydraulic permeability of human lumbar anulus fibrosus. Influence of age, degeneration, direction, and water content. Spine 24(23):2449–2455, 1999.

    Article  CAS  PubMed  Google Scholar 

  16. Hendry, N. G. C. The hydration of the nucleus pulposus and its relation to intervertebral disc derangement. J. Bone Joint Surg. 40B(1):132–144, 1958.

    Google Scholar 

  17. Heneghan, P., and P. E. Riches. Determination of the strain-dependent hydraulic permeability of the compressed bovine nucleus pulposus. J. Biomech. 41(4):903–906, 2008.

    Article  PubMed  Google Scholar 

  18. Holzapfel, G. A., C. A. Schulze-Bauer, G. Feigl, and P. Regitnig. Single lamellar mechanics of the human lumbar anulus fibrosus. Biomech. Model. Mechanobiol. 3(3):125–140, 2005.

    Article  CAS  PubMed  Google Scholar 

  19. Huyghe, J. M., and M. R. Drost. Uniaxial tensile testing of canine annulus fibrosus tissue under changing salt concentrations. Biorheology 41(3–4):255–261, 2004.

    CAS  PubMed  Google Scholar 

  20. Huyghe, J. M., G. B. Houben, M. R. Drost, and C. C. van Donkelaar. An ionised/non-ionised dual porosity model of intervertebral disc tissue. Biomech. Model. Mechanobiol. 2(1):3–19, 2003.

    Article  CAS  PubMed  Google Scholar 

  21. Huyghe, J. M., and J. D. Janssen. Quadriphasic mechanics of swelling incompressible porous media. Int. J. Eng. Sci. 35(8):793–802, 1997.

    Article  Google Scholar 

  22. Iatridis, J. C., J. P. Laible, and M. H. Krag. Influence of fixed charge density magnitude and distribution on the intervertebral disc: applications of a poroelastic and chemical electric (PEACE) model. J. Biomech. Eng. 125:12–24, 2003.

    Article  PubMed  Google Scholar 

  23. Iatridis, J. C., J. J. MacLean, M. O’Brien, and I. A. Stokes. Measurements of proteoglycan and water content distribution in human lumbar intervertebral discs. Spine 32(14):1493–1497, 2007.

    Article  PubMed  Google Scholar 

  24. 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(2):318–322, 1997.

    Article  CAS  PubMed  Google Scholar 

  25. Johannessen, W., and D. M. Elliott. Effects of degeneration on the biphasic material properties of human nucleus pulposus in confined compression. Spine 30(24):E724–E729, 2005.

    Article  PubMed  Google Scholar 

  26. Johannessen, W., E. J. Vresilovic, A. C. Wright, and D. M. Elliott. Intervertebral disc mechanics are restored following cyclic loading and unloaded recovery. Ann. Biomed. Eng. 32(1):70–76, 2004.

    Article  PubMed  Google Scholar 

  27. Lai, W. M., J. S. Hou, and V. C. Mow. A triphasic theory for the swelling and deformation behaviors of articular cartilage. J. Biomech. Eng. 113(3):245–258, 1991.

    Article  CAS  PubMed  Google Scholar 

  28. Laible, J. P., D. S. Pflaster, M. H. Krag, B. R. Simon, and L. D. Haugh. A poroelastic-swelling finite element model with application to the intervertebral disc. Spine 18(5):659–670, 1993.

    Article  CAS  PubMed  Google Scholar 

  29. Laible, J. P., D. Pflaster, B. R. Simon, M. H. Krag, M. Pope, and L. D. Haugh. A dynamic material parameter estimation procedure for soft tissue using a poroelastic finite element model. J. Biomech. Eng. 116(1):19–29, 1994.

    Article  CAS  PubMed  Google Scholar 

  30. Li, G. P., J. T. Bronk, K. N. An, and P. J. Kelly. Permeability of cortical bone of canine tibiae. Microvasc. Res. 34(3):302–310, 1987.

    Article  CAS  PubMed  Google Scholar 

  31. Lim, T. H., and J. H. Hong. Poroelastic properties of bovine vertebral trabecular bone. J. Orthop. Res. 18(4):671–677, 2000.

    Article  CAS  PubMed  Google Scholar 

  32. Malko, J. A., W. C. Hutton, and W. A. Fajman. An in vivo MRI study of the changes in volume (and fluid content) of the lumbar intervertebral disc after overnight bed rest and during an 8-hour walking protocol. J. Spinal Disord. Tech. 15(2):157–163, 2002.

    PubMed  Google Scholar 

  33. Mcmillan, D. W., G. Garbutt, and M. A. Adams. Effect of sustained loading on the water content of intervertebral discs: Implications for disc metabolism. Ann. Rheum. Dis. 55(12):880–887, 1996.

    Article  CAS  PubMed  Google Scholar 

  34. 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(1):73–84, 1980.

    Article  CAS  PubMed  Google Scholar 

  35. Natarajan, R. N., S. A. Lavender, H. A. An, and G. B. Andersson. Biomechanical response of a lumbar intervertebral disc to manual lifting activities: a poroelastic finite element model study. Spine 33(18):1958–1965, 2008.

    Article  PubMed  Google Scholar 

  36. 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.

    Article  PubMed  Google Scholar 

  37. Perié, D., D. Korda, and J. C. Iatridis. Confined compression experiments on bovine nucleus pulposus and annulus fibrosus: sensitivity of the experiment in the determination of compressive modulus and hydraulic permeability. J. Biomech. 38(11):2164–2171, 2005.

    Article  PubMed  Google Scholar 

  38. Riches, P. E., N. Dhillon, J. Lotz, A. W. Woods, and D. S. McNally. The internal mechanics of the intervertebral disc under cyclic loading. J. Biomech. 35:1263–1271, 2002.

    Article  CAS  PubMed  Google Scholar 

  39. Roughley, P. J. Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine 29(23):2691–2699, 2004.

    Article  PubMed  Google Scholar 

  40. Schroeder, Y., D. M. Elliott, W. Wilson, F. P. Baaijens, and J. M. Huyghe. Experimental and model determination of human intervertebral disc osmoviscoelasticity. J. Orthop. Res. 26(8):1141–1146, 2008.

    Article  CAS  PubMed  Google Scholar 

  41. Setton, L. A., W. Zhu, M. Weidenbaum, A. Ratcliffe, and V. C. Mow. Compressive properties of the cartilaginous end-plate of the baboon lumbar spine. J. Orthop. Res. 11(2):228–239, 1993.

    Article  CAS  PubMed  Google Scholar 

  42. Simon, B. R., J. P. Liable, D. Pflaster, Y. Yuan, and M. H. Krag. A poroelastic finite element formulation including transport and swelling in soft tissue structures. J. Biomech. Eng. 118(1):1–9, 1996.

    Article  CAS  PubMed  Google Scholar 

  43. Simon, B. R., J. S. Wu, M. W. Carlton, J. H. Evans, and L. E. Kazarian. Structural models for human spinal motion segments based on a poroelastic view of the intervertebral disk. J. Biomech. Eng. 107(4):327–335, 1985.

    Article  CAS  PubMed  Google Scholar 

  44. Simon, B. R., J. S. Wu, M. W. Carlton, L. E. Kazarian, E. P. France, J. H. Evans, and O. C. Zienkiewicz. Poroelastic dynamic structural models of rhesus spinal motion segments. Spine 10(6):494–507, 1985.

    Article  CAS  PubMed  Google Scholar 

  45. Stokes, I. A., M. Gardner-Morse, D. Churchill, and J. P. Laible. Measurement of a spinal motion segment stiffness matrix. J. Biomech. 35(4):517–521, 2002.

    Article  PubMed  Google Scholar 

  46. 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.

    Article  CAS  PubMed  Google Scholar 

  47. Urban, J. P., and A. Maroudas. Swelling of the intervertebral disc in vitro. Connect. Tissue Res. 9(1):1–10, 1981.

    Article  CAS  PubMed  Google Scholar 

  48. Urban, J. P., and J. F. Mcmullin. Swelling pressure of the intervertebral disc: influence of proteoglycan and collagen contents. Biorheology 22(2):145–157, 1985.

    CAS  PubMed  Google Scholar 

  49. van der Veen, A. J., M. G. Mullender, I. Kingma, J. H. van Dieen, and T. H. Smit. Contribution of vertebral bodies endplates and intervertebral discs to the compression creep of spinal motion segments. J. Biomech. 41(6):1260–1268, 2008.

    Article  PubMed  Google Scholar 

  50. van Loon, R., J. M. Huyghe, M. W. Wijlaars, and F. P. T. Baaijens. 3D FE implementation of an incompressible quadriphasic mixture model. Int. J. Numer. Methods Eng. 57:1243–1258, 2003.

    Article  Google Scholar 

  51. Wilson, W., C. C. van Donkelaarm, and J. M. Huyghe. A comparison between mechano-electrochemical and biphasic swelling theories for soft hydrated tissues. J. Biomech. Eng. 127(1):158–165, 2005.

    Article  CAS  PubMed  Google Scholar 

  52. Yao, H., and W. Y. Gu. Three-dimensional inhomogeneous triphasic finite-element analysis of physical signals and solute transport in human intervertebral disc under axial compression. J. Biomech. 40(9):2071–2077, 2007.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by NIH Grant R01 AR 049370. Lumbar spines were provided by the National Disease Research Interchange (NDRI). Jacob Lubinski assisted with a preliminary study. Richard Stanley provided technical support for experimental work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ian A. F. Stokes.

Additional information

Associate Editor Peter E. McHugh oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stokes, I.A.F., Laible, J.P., Gardner-Morse, M.G. et al. Refinement of Elastic, Poroelastic, and Osmotic Tissue Properties of Intervertebral Disks to Analyze Behavior in Compression. Ann Biomed Eng 39, 122–131 (2011). https://doi.org/10.1007/s10439-010-0140-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-010-0140-1

Keywords

Navigation