Skip to main content
SpringerLink
Log in

A Conductivity Approach to Measuring Fixed Charge Density in Intervertebral Disc Tissue

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

Abstract

A new method for measuring the fixed charge density (FCD) in intervertebral disc (IVD) tissues employing a two-point electrical conductivity approach was developed. In this technique, the tissue is first confined and equilibrated in a potassium chloride (KCl) solution, and the tissue conductivity is then measured. This is then repeated with a second concentration of KCl solution. The FCD can be determined from the conductivity measurements. Using this method, the FCD values of bovine annulus fibrosus (AF) and nucleus pulposus (NP) tissues were determined to be 0.060 ± 0.027 mEq/g wet tissue and 0.19 ± 0.039 mEq/g wet tissue, respectively. The FCD of AF was significantly lower than that of NP tissue, similar to results in the literature for human IVD tissues. In order to verify the accuracy of the new method, the glycosaminoglycan (GAG) contents of the tissues were measured and used to estimate the tissue FCD. A strong correlation (R 2 = 0.84–0.87) was found to exist between FCD values measured and those estimated from GAG contents, indicating that the conductivity approach is a reliable technique for measuring the FCD of IVD tissues.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

FIGURE 1
FIGURE 2
FIGURE 3
FIGURE 4

Similar content being viewed by others

References

  1. Bashir, A., M. L. Gray, J. Hartke, et al. Nondestructive imaging of human cartilage glycosaminoglycan concentration by MRI. Magn. Reson. Med. 41:857–865, 1999.

    Article  CAS  PubMed  Google Scholar 

  2. Beckstein, J. C., S. Sen, T. P. Schaer, et al. Comparison of animal discs used in disc research to human lumbar disc. Spine 33:E166–E173, 2008.

    Article  PubMed  Google Scholar 

  3. Berkenblit, S. I., E. H. Frank, E. P. Salant, et al. Nondestructive detection of cartilage degeneration using electromechanical surface spectroscopy. J. Biomech. Eng. 116:384–392, 1994.

    Article  CAS  PubMed  Google Scholar 

  4. Buckwalter, J. A. Aging and degeneration of the human intervertebral disc. Spine 20:1307–1314, 1995.

    CAS  PubMed  Google Scholar 

  5. Burstein, D., M. L. Gray, A. L. Hartman, et al. Diffusion of small solutes in cartilage as measured by nuclear magnetic resonance (NMR) spectroscopy and imaging. J. Orthop. Res. 11:465–478, 1993.

    Article  CAS  PubMed  Google Scholar 

  6. Chen, S. S., Y. H. Falcovitz, R. Schneiderman, et al. Depth-dependent compressive properties of normal aged human femoral head articular cartilage: relationship to fixed charge density. Osteoarthr. Cartil. 9:561–569, 2001.

    Article  CAS  PubMed  Google Scholar 

  7. Chen, C. T., K. W. Fishbein, P. A. Torzilli, et al. Matrix fixed-charge density as determined by magnetic resonance microscopy of bioreactor-derived hyaline cartilage correlates with biochemical and biomechanical properties. Arthr. Rheum. 48:1047–1056, 2003.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  9. Eyre, D. R., P. Benya, and J. Buckwalter. Intervertebral disk: basic science perspectives. In: New Perspectives on Low Back Pain, edited by J. W. Frymoyer, S. L. Gordon, et al. Park Ridge, IL: American Academy of Orthopaedic Surgeons, 1989, pp. 147–207.

    Google Scholar 

  10. Farndale, R. W., C. A. Sayers, and A. J. Barrett. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect. Tissue Res. 9:247–248, 1982.

    Article  CAS  PubMed  Google Scholar 

  11. Frank, E. H., A. J. Grodzinsky, T. J. Koob, et al. Streaming potentials: a sensitive index of enzymatic degradation in articular cartilage. J. Orthop. Res. 5:497–508, 1987.

    Article  CAS  PubMed  Google Scholar 

  12. Gu, W. Y., and M. A. Justiz. Apparatus for measuring the swelling dependent electrical conductivity of charged hydrated soft tissues. J. Biomech. Eng. 124:790–793, 2002.

    Article  CAS  PubMed  Google Scholar 

  13. Gu, W. Y., M. A. Justiz, and H. Yao. Electrical conductivity of lumbar annulus fibrosis: effects of porosity and fixed charge density. Spine 27:2390–2395, 2002.

    Article  PubMed  Google Scholar 

  14. Gu, W. Y., W. M. Lai, and V. C. Mow. Theoretical basis for measurements of cartilage fixed-charge density using streaming current and electro-osmosis effects. ASME Adv. Bioeng. BED 26:55–58, 1993.

    Google Scholar 

  15. Gu, W. Y., B. Lewis, W. M. Lai, et al. A technique for measuring volume and true density of the solid matrix of cartilaginous tissues. Adv. Bioeng. ASME BED 33:89–90, 1996.

    Google Scholar 

  16. Gu, W. Y., B. Lewis, F. Saed-Nejad, et al. Hydration and true density of normal and PG-depleted bovine articular cartilage. Trans. Orthop. Res. Soc. 22:826, 1997.

    Google Scholar 

  17. Gu, W. Y., X. G. Mao, R. J. Foster, et al. The anisotropic hydraulic permeability of human lumbar anulus fibrosus. Influence of age, degeneration, direction, and water content. Spine 24:2449–2455, 1999.

    Article  CAS  PubMed  Google Scholar 

  18. Gu, W. Y., X. G. Mao, B. A. Rawlins, et al. Streaming potential of human lumbar anulus fibrosus is anisotropic and affected by disc degeneration. J. Biomech. 32:1177–1182, 1999.

    Article  CAS  PubMed  Google Scholar 

  19. Gu, W. Y., and H. Yao. Effects of hydration and fixed charge density on fluid transport in charged hydrated soft tissue. Ann. Biomed. Eng. 31:1162–1170, 2003.

    Article  PubMed  Google Scholar 

  20. Gu, W. Y., H. Yao, A. L. Vega, et al. Diffusivity of ions in agarose gels and intervertebral disc: Effect of porosity. Ann. Biomed. Eng. 32:1710–1717, 2004.

    Article  PubMed  Google Scholar 

  21. Guiot, B. H., and R. G. Fessler. Molecular biology of degenerative disc disease. Neurosurgery 47:1034–1040, 2000.

    Article  CAS  PubMed  Google Scholar 

  22. Hasegawa, I., S. Kuriki, S. Matsuno, et al. Dependence of electrical conductivity on fixed charge density in articular cartilage. Clin. Orthop. 177:283–288, 1983.

    PubMed  Google Scholar 

  23. Helfferich, F. Ion Exchange. New York: McGraw Hill Book Company, Inc., 1962.

    Google Scholar 

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

    Google Scholar 

  25. Hickey, D. S., and D. W. L. Hukins. Relation between the structure of the annulus fibrosus and the function and failure of the intervertebral disc. Spine 5:106–116, 1980.

    Article  CAS  PubMed  Google Scholar 

  26. Iatridis, J. C., J. J. MacLean, M. O’Brien, et al. Measurement of proteoglycan and water content distribution in human lumbar intervertebral discs. Spine 32:1493–1497, 2007.

    Article  PubMed  Google Scholar 

  27. Insko, E. K., D. B. Clayton, and M. A. Elliott. In vivo sodium MR imaging of the intervertebral disk at 4 T. Acad. Radiol. 9:800–804, 2002.

    Article  PubMed  Google Scholar 

  28. Jackson, A. R., F. Travascio, and W. Y. Gu. Effect of mechanical loading on electrical conductivity in human intervertebral disk. J. Biomech. Eng. 131:054505, 2009.

    Article  PubMed  Google Scholar 

  29. Jackson, A. R., H. Yao, M. D. Brown, et al. Anisotropic ion diffusivity in intervertebral disc: an electrical conductivity approach. Spine 31:2783–2789, 2006.

    Article  PubMed  Google Scholar 

  30. Jackson, A. R., T. Y. Yuan, C. Y. Huang, et al. Effect of compression and anisotropy on the diffusion of glucose in annulus fibrosus. Spine 33:1–7, 2008.

    Article  PubMed  Google Scholar 

  31. Johnstone, B., J. P. Urban, S. Roberts, et al. The fluid content of the human intervertebral disc. Comparison between fluid content and swelling pressure profiles of discs removed at surgery and those taken postmortem. Spine 17:412–416, 1992.

    Article  CAS  PubMed  Google Scholar 

  32. Katchalsky, A., and P. F. Curran. Nonequilibrium Thermodynamics in Biophysics, Vol. 4. Cambridge, MA: Harvard University Press, 1975.

    Google Scholar 

  33. Kelsey, J. L., D. F. Mundt, and A. L. Golden. Epidemiology of low back pain. In: The Lumbar Spine and Back Pain, edited by J. I. V. Malcolm. New York: Churchill Livingstone, 1992, pp. 537–549.

    Google Scholar 

  34. Koneshan, S., J. C. Rasaiah, R. M. Lynden-Bell, et al. Solvent structure, dynamics, and ion mobility in aqueous solution at 25 C. J. Phys. Chem. 102:4193–4204, 1998.

    CAS  Google Scholar 

  35. Kraemer, J., D. Kolditz, and R. Gowin. Water and electrolyte content of human intervertebral discs under variable load. Spine 10:69–71, 1985.

    Article  CAS  PubMed  Google Scholar 

  36. 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. 113:245–258, 1991.

    Article  CAS  PubMed  Google Scholar 

  37. Le, N. A., and B. C. Fleming. Measuring fixed charge density of goat articular cartilage using indentation methods and biochemical analysis. J. Biomech. 41:715–720, 2008.

    Article  PubMed  Google Scholar 

  38. Lesperance, L. M., M. L. Gray, and D. Burstein. Determination of fixed charge density in cartilage using nuclear magnetic resonance. J. Orthop. Res. 10:1–13, 1992.

    Article  CAS  PubMed  Google Scholar 

  39. Lu, X. L., C. Miller, F. H. Chen, et al. The generalized triphasic correspondence principle for simultaneous determination of the mechanical properties and proteoglycan content of articular cartilage by indentation. J. Biomech. 40:2434–2441, 2007.

    Article  PubMed  Google Scholar 

  40. Lu, X. L., D. D. Sun, X. E. Guo, et al. Indentation determined mechanoelectrochemical properties and fixed charge density of articular cartilage. Ann. Biomed. Eng. 32:370–379, 2004.

    Article  PubMed  Google Scholar 

  41. Lundon, K., and K. Bolton. Structure and function of the lumbar intervertebral disk in health, aging, and pathologic conditions. J. Orthop. Sports Phys. Ther. 31:291–303, 2001.

    CAS  PubMed  Google Scholar 

  42. Marchand, F., and A. M. Ahmed. Investigation of the laminate structure of lumbar disc annulus fibrosus. Spine 15:402–410, 1990.

    Article  CAS  PubMed  Google Scholar 

  43. Maroudas, A. Physicochemical properties of cartilage in the light of ion exchange theory. Biophys. J. 8:575–595, 1968.

    Article  CAS  PubMed  Google Scholar 

  44. Maroudas, A. Biophysical chemistry of cartilaginous tissues with special reference to solute and fluid transport. Biorheology 12:233–248, 1975.

    CAS  PubMed  Google Scholar 

  45. Maroudas, A. Physicochemical properties of articular cartilage. In: Adult Articular Cartilage, edited by Freeman MAR, Pitman Medical, London, 1979, pp. 215–290.

  46. Maroudas, A., H. Muir, and J. Wingham. The correlation of fixed negative charge with glycosaminoglycan content of human articular cartilage. Biochim. Biophys. Acta 177:492–500, 1969.

    CAS  PubMed  Google Scholar 

  47. Maroudas, A., and H. Thomas. A simple physicochemical micromethod for determining fixed anionic groups in connective tissue. Biochim. Biophys. Acta 215:214–216, 1975.

    Google Scholar 

  48. Maroudas, A., R. A. Stockwell, A. Nachemson, et al. Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. J. Anat. 120:113–130, 1975.

    CAS  PubMed  Google Scholar 

  49. Minassian, A., D. O’Hare, K. H. Parker, et al. Measurement of the charge properties of articular cartilage by an electrokinetic method. J. Orthop. Res. 16:720–725, 1998.

    Article  CAS  PubMed  Google Scholar 

  50. Narmoneva, D. A., J. Y. Wang, and L. A. Setton. A noncontacting method for material property determination for articular cartilage from osmotic loading. Biophys. J. 81:3066–3076, 2001.

    Article  CAS  PubMed  Google Scholar 

  51. NIH. Research on low back pain and common spinal disorders. NIH Guide 26, 1997.

  52. Palmer, A. W., R. E. Guldberg, and M. E. Levenston. Analysis of cartilage matrix fixed charge density and three-dimensional morphology via contrast-enhanced microcomputed tomography. Proc. Natl. Acad. Sci. USA 103:19255–19260, 2006.

    Article  CAS  PubMed  Google Scholar 

  53. Panagiotacopulos, N. D., M. H. Pope, R. Bloch, et al. Water content in human intervertebral discs. Part II. Viscoelastic behavior. Spine 12:918–924, 1987.

    Article  CAS  PubMed  Google Scholar 

  54. Panagiotacopulos, N. D., M. H. Pope, M. H. Krag, et al. Water content in human intervertebral discs. Part I. Measurement by magnetic resonance imaging. Spine 12:912–917, 1987.

    CAS  PubMed  Google Scholar 

  55. Perie, D., J. C. Iatridis, C. N. Demers, et al. Assessment of compressive modulus, hydraulic permeability and matrix content of trypsin-treated nucleus pulposus using quantitative MRI. J. Biomech. 39:1392–1400, 2006.

    Article  CAS  PubMed  Google Scholar 

  56. Shapiro, E. M., A. Borthakur, A. Gougoutas, et al. 23Na MRI accurately measures fixed charge density in articular cartilage. Magn. Reson. Med. 47:284–291, 2002.

    Article  PubMed  Google Scholar 

  57. Stevens, R. L., R. J. Ewins, P. A. Revell, et al. Proteoglycans of the intervertebral disc. Homology of structure with laryngeal proteoglycans. Biochem. J. 179:561–572, 1979.

    CAS  PubMed  Google Scholar 

  58. Urban JPG. Fluid and solute transport in the intervertebral disc. PhD dissertation, London University, London, UK, 1977.

  59. Urban, J. P. G., and A. Maroudas. The chemistry of the intervertebral disc in relation to its physiological function and requirements. Clin. Rheum. Dis. 6:51–77, 1980.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  61. Urban, J. P., and J. F. McMullin. Swelling pressure of the intervertebral disc: influence of proteoglycan and collagen contents. Biorheology 22:145–157, 1985.

    CAS  PubMed  Google Scholar 

  62. Wheaton, A. J., F. L. Casey, A. J. Gougoutas, et al. Correlation of T1rho with fixed charge density in cartilage. J. Magn. Reson. Imaging 20:519–525, 2004.

    Article  PubMed  Google Scholar 

  63. White, A. A. Biomechanics of lumbar spine and sacroiliac articulation: relevance to idiopathic low back pain. In: Symposium on Idiopathic Low Back Pain, edited by A.A. White and S.L. Gordon. St. Louis: CV Mosby Co., 1981, pp. 296–322.

Download references

Acknowledgment

This study was supported by the grant number AR050609 from NIH NIAMS.

Author information

Authors and Affiliations

  1. Tissue Biomechanics Laboratory, Department of Biomedical Engineering, College of Engineering, University of Miami, P.O. Box 248294, Coral Gables, FL, 33124-0621, USA

    Alicia R. Jackson, Tai-Yi Yuan & Wei Yong Gu

  2. Stem Cell and Mechanobiology Laboratory, Department of Biomedical Engineering, University of Miami, Coral Gables, FL, 33146, USA

    Chun-Yuh Huang

Authors
  1. Alicia R. Jackson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tai-Yi Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chun-Yuh Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wei Yong Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Yong Gu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jackson, A.R., Yuan, TY., Huang, CY. et al. A Conductivity Approach to Measuring Fixed Charge Density in Intervertebral Disc Tissue. Ann Biomed Eng 37, 2566–2573 (2009). https://doi.org/10.1007/s10439-009-9792-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-009-9792-0

Keywords

Search

Navigation