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Nutrient Transport in Human Annulus Fibrosus is Affected by Compressive Strain and Anisotropy

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Abstract

The avascular intervertebral disc (IVD) receives nutrition via transport from surrounding vasculature; poor nutrition is believed to be a main cause of disc degeneration. In this study, we investigated the effects of mechanical deformation and anisotropy on the transport of two important nutrients—oxygen and glucose—in human annulus fibrosus (AF). The diffusivities of oxygen and glucose were measured under three levels of uniaxial confined compression—0, 10, and 20%—and in three directions—axial, circumferential, and radial. The glucose partition coefficient was also measured at three compression levels. Results for glucose and oxygen diffusivity in AF ranged from 4.46 × 10−7 to 9.77 × 10−6 cm2/s and were comparable to previous studies; the glucose partition coefficient ranged from 0.71 to 0.82 and was also similar to previous results. Transport properties were found to decrease with increasing deformation, likely caused by fluid exudation during tissue compression and reduction in pore size. Furthermore, diffusivity in the radial direction was lower than in the axial or circumferential directions, indicating that nutrient transport in human AF is anisotropic. This behavior is likely a consequence of the layered structure and unique collagen architecture of AF tissue. These findings are important for better understanding nutritional supply in IVD and related disc degeneration.

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References

  1. Adams, M. A., and W. C. Hutton. The effect of posture on the fluid content of lumbar intervertebral discs. Spine. 8(6):665–671, 1983.

    Article  PubMed  CAS  Google Scholar 

  2. Adams, M. A., and W. C. Hutton. The effect of posture on diffusion into lumbar intervertebral discs. J. Anat. 147:121–134, 1986.

    PubMed  CAS  Google Scholar 

  3. Arun, R., B. J. C. Freeman, B. E. Scammell, et al. 2009 ISSLS Prize Winner: what influence does sustained mechanical load have on diffusion in the human intervertebral disc?: an in vivo study using serial postcontrast magnetic resonance imaging. Spine. 34(21):2324–2337, 2009.

    Article  PubMed  Google Scholar 

  4. Beattie, P. F., P. S. Morgan, and D. Peters. Diffusion-weighted magnetic resonance imaging of normal and degenerative lumbar intervertebral discs: a new method to potentially quantify the physiological effect of physical therapy intervention. J. Orthop. Sports Phys. Therapy 38(2):42–49, 2008.

    Google Scholar 

  5. Bibby, S. R., J. C. Fairbank, M. R. Urban, et al. Cell viability in scoliotic discs in relation to disc deformity and nutrient levels. Spine. 27(20):2220–2228, 2002.

    Article  PubMed  Google Scholar 

  6. Brodin, H. Path of nutrition in articular cartilage and intervertebral disk. Acta Orthop. Scand. 24:177, 1955.

    PubMed  CAS  Google Scholar 

  7. Brown, M. D., and T. T. Tsaltas. Studies on the permeability of the intervertebral disc during skeletal maturation. Spine. 1:240–244, 1976.

    Article  Google Scholar 

  8. 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(4):465–478, 1993.

    Article  PubMed  CAS  Google Scholar 

  9. Chiu, E. J., D. C. Newitt, M. R. Segal, et al. Magnetic resonance imaging measurement of relaxation and water diffusion in the human lumbar intervertebral disc under compression in vitro. Spine. 26(19):E437–E444, 2001.

    Article  PubMed  CAS  Google Scholar 

  10. Drew, S. C., P. Silva, S. Crozier, et al. A diffusion and T2 relaxation MRI study of the ovine lumbar intervertebral disc under compression in vitro. Phys. Med. Biol. 49:3585–3592, 2004.

    Article  PubMed  Google Scholar 

  11. Fetter, N. L., H. A. Leddy, F. Guilak, et al. Composition and transport properties of human ankle and knee cartilage. J. Orthop. Res. 24(2):211–219, 2006.

    Article  PubMed  Google Scholar 

  12. Gilchrist, C. L., J. Q. Xia, L. A. Setton, et al. High-resolution determination of soft tissue deformations using MRI and first-order texture correlation. IEEE Trans. Med. Imaging 23(5):546–553, 2004.

    Article  PubMed  Google Scholar 

  13. 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. BED33:89–90, 1996.

    Google Scholar 

  14. 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  PubMed  CAS  Google Scholar 

  15. Holm, S., A. Maroudas, J. P. Urban, et al. Nutrition of the intervertebral disc: solute transport and metabolism. Connect Tissue Res. 8(2):101–119, 1981.

    Article  PubMed  CAS  Google Scholar 

  16. Holm, S., and A. Nachemson. Nutritional changes in the canine intervertebral disc after spinal fusion. Clin. Orthop. 169:243–258, 1982.

    PubMed  Google Scholar 

  17. Horner, H. A., and J. P. Urban. 2001 Volvo Award Winner in Basic Science Studies: effect of nutrient supply on the viability of cells from the nucleus pulposus of the intervertebral disc. Spine. 26(23):2543–2549, 2001.

    Article  PubMed  CAS  Google Scholar 

  18. Iatridis, J. C., and I. ap Gwynn. Mechanisms for mechanical damage in the intervertebral disc annulus fibrosus. J. Biomech. 37:1165–1175, 2004.

    Article  PubMed  Google Scholar 

  19. Jackson, A. R., and W. Y. Gu. Transport properties of cartilaginous tissues. Curr. Rheumatol. Rev. 5:40–50, 2009.

    Article  PubMed  CAS  Google Scholar 

  20. 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):1–7, 2008.

    Article  PubMed  Google Scholar 

  21. Kealey, S. M., T. Aho, D. Delong, et al. Assessment of apparent diffusion coefficient in normal and degenerated intervertebral lumbar disks: initial experience. Radiology 235(2):569–574, 2005.

    Article  PubMed  Google Scholar 

  22. Kraemer, J., D. Kolditz, and R. Gowin. Water and electrolyte content of human intervertebral discs under variable load. Spine. 10(1):69–71, 1985.

    Article  PubMed  CAS  Google Scholar 

  23. Kurunlahti, M., L. Kerttula, J. Jauhiainen, et al. Correlation of diffusion in lumbar intervertebral disks with occlusion of lumbar arteries: a study in adult volunteers. Radiology 221(3):779–786, 2001.

    Article  PubMed  CAS  Google Scholar 

  24. 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  PubMed  CAS  Google Scholar 

  25. Malda, J., J. Rouwkema, D. E. Martens, et al. Oxygen gradients in tissue-engineered PEGT/PBT cartilaginous constructs: measurement and modeling. Biotechnol. Bioeng. 86(1):9–18, 2004.

    Article  PubMed  CAS  Google Scholar 

  26. Marchand, F., and A. M. Ahmed. Investigation of the laminate structure of lumbar disc annulus fibrosus. Spine. 15(5):402–410, 1990.

    Article  PubMed  CAS  Google Scholar 

  27. Maroudas, A. Transport of solutes through cartilage: permeability to large molecules. J. Anat. 122(2):335–347, 1976.

    PubMed  CAS  Google Scholar 

  28. Maroudas, A., P. Bullough, S. A. Swanson, et al. The permeability of articular cartilage. J. Bone Joint. Surg. Br. 50(1):166–177, 1968.

    PubMed  CAS  Google Scholar 

  29. 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(1):113–130, 1975.

    PubMed  CAS  Google Scholar 

  30. Nachemson, A., T. Lewin, A. Maroudas, et al. In vitro diffusion of dye through the end-plates and the annulus fibrosus of human lumbar inter-vertebral discs. Acta Orthop. Scand. 41(6):589–607, 1970.

    Article  PubMed  CAS  Google Scholar 

  31. NIH. Research on Low Back Pain and Common Spinal Disorders. NIH Guide, Vol. 26, No. 16. Bethesda, MD: National Institutes of Health, 1997.

  32. Niinimäki, J., A. Korkiakoski, O. Ojala, et al. Association between visual degeneration of intervertebral discs and the apparent diffusion coefficient. Magn. Reson. Imaging 27:641–647, 2009.

    Article  PubMed  Google Scholar 

  33. O’Connell, G. D., W. Johannessen, E. J. Vresilovic, et al. Human internal disc strains in axial compression measured noninvasively using magnetic resonance imaging. Spine (Phila Pa 1976) 32(25):2860–2868, 2007.

    Google Scholar 

  34. O’Hare, D., C. P. Winlove, and K. H. Parker. Electrochemical method for direct measurement of oxygen concentration and diffusivity in the intervertebral disc: electrochemical characterization and tissue–sensor interactions. J. Biomed. Eng. 13(4):304–312, 1991.

    Article  PubMed  Google Scholar 

  35. Ogata, K., and L. A. Whiteside. Volvo award winner in basic science. Nutritional pathways of the intervertebral disc. An experimental study using hydrogen washout technique. Spine. 6(3):211–216, 1981.

    Article  PubMed  CAS  Google Scholar 

  36. Ohshima, H., H. Tsuji, N. Hiarano, et al. Water diffusion pathway, swelling pressure, and biomechanical properties of the intervertebral disc during compression load. Spine. 14:1234–1244, 1989.

    Article  PubMed  CAS  Google Scholar 

  37. Quinn, T. M., V. Morel, and J. J. Meister. Static compression of articular cartilage can reduce solute diffusivity and partitioning: implications for the chondrocyte biological response. J. Biomech. 34(11):1463–1469, 2001.

    Article  PubMed  CAS  Google Scholar 

  38. Rodriguez, A. G., A. E. Rodriguez-Soto, A. J. Burghardt, et al. Morphology of the human vertebral endplate. J. Orthop. Res. 30(2):280–287, 2012.

    Article  PubMed  Google Scholar 

  39. Thompson, J. P., R. H. Pearce, M. T. Schechter, et al. Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine. 15:411–415, 1990.

    Article  PubMed  CAS  Google Scholar 

  40. Torzilli, P. A., D. A. Grande, and J. M. Arduino. Diffusive properties of immature articular cartilage. J. Biomed. Mater. Res. 40(1):132–138, 1998.

    Article  PubMed  CAS  Google Scholar 

  41. Travascio, F., A. R. Jackson, M. D. Brown, et al. Relationship between solute transport properties and tissue morphology in human annulus fibrosus. J. Orthop. Res. 27:1625–1630, 2009.

    Article  PubMed  Google Scholar 

  42. Urban, J. P. The role of the physicochemical environment in determining disc cell behaviour. Biochem. Soc. Trans. 30(6):858–864, 2001.

    Article  Google Scholar 

  43. Urban, J. P., S. Holm, A. Maroudas, et al. Nutrition of the intervertebral disc: effect of fluid flow on solute transport. Clin. Orthop. 170:296–302, 1982.

    PubMed  CAS  Google Scholar 

  44. Urban, J. P., and S. Roberts. Development and degeneration of the intervertebral discs. Mol. Med. Today. 1(7):329–335, 1995.

    Article  PubMed  CAS  Google Scholar 

  45. Wang, S., Q. Xia, P. Passias, et al. Measurement of geometric deformation of lumbar intervertebral discs under in vivo weightbearing condition. J. Biomech. 42(6):705–711, 2009.

    Article  PubMed  Google Scholar 

  46. Yuan, T. Y., A. R. Jackson, C. Y. Huang, et al. Strain-dependent oxygen diffusivity in bovine annulus fibrosus. J. Biomech. Eng. 131:074503, 2009.

    Google Scholar 

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Acknowledgments

This study was supported by grants from NIH (AR050609, AR056101 and EB008653) and an NRSA Fellowship from NIH NIA (AG030921). The authors wish to thank Mr. Andre Castillo, BSBE, for his help in apparatus development.

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Authors and Affiliations

  1. Orthopaedic Biomechanics Lab, Department of Biomedical Engineering, University of Miami, Coral Gables, FL, USA

    Alicia R. Jackson

  2. Tissue Biomechanics Lab, Department of Mechanical and Aerospace Engineering, University of Miami, Coral Gables, FL, USA

    Tai-Yi Yuan & Wei Yong Gu

  3. Stem Cell and Mechanobiology Lab, Department of Biomedical Engineering, University of Miami, Coral Gables, FL, USA

    Tai-Yi Yuan & Chun-Yuh Huang

  4. Department of Orthopaedics, Miller School of Medicine, University of Miami, Miami, FL, USA

    Mark D. Brown

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  1. Alicia R. Jackson
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Correspondence to Wei Yong Gu.

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Associate Editor Daniel Elson oversaw the review of this article.

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Jackson, A.R., Yuan, TY., Huang, CY. et al. Nutrient Transport in Human Annulus Fibrosus is Affected by Compressive Strain and Anisotropy. Ann Biomed Eng 40, 2551–2558 (2012). https://doi.org/10.1007/s10439-012-0606-4

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  • DOI: https://doi.org/10.1007/s10439-012-0606-4

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