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Role of load history in intervertebral disc mechanics and intradiscal pressure generation

  • David Hwang
  • Adam S. Gabai
  • Miao Yu
  • Alvin G. Yew
  • Adam H. HsiehEmail author
Original Paper

Abstract

Solid–fluid interactions play an important role in mediating viscoelastic behaviour of biological tissues. In the intervertebral disc, water content is governed by a number of factors, including age, disease and mechanical loads, leading to changes in stiffness characteristics. We hypothesized that zonal stress distributions depend on load history, or the prior stresses experienced by the disc. To investigate these effects, rat caudal motion segments were subjected to compressive creep biomechanical testing in vitro using a protocol that consisted of two phases: a Prestress Phase (varied to represent different histories of load) followed immediately by an Exertion Phase, identical across all Prestress groups. Three analytical models were used to fit the experimental data in order to evaluate load history effects on gross and zonal disc mechanics. Model results indicated that while gross transient response was insensitive to load history, there may be changes in the internal mechanics of the disc. In particular, a fluid transport model suggested that the role of the nucleus pulposus in resisting creep during Exertion depended on Prestress conditions. Separate experiments using similarly defined load history regimens were performed to verify these predictions by measuring intradiscal pressure with a fibre optic sensor. We found that the ability for intradiscal pressure generation was load history-dependent and exhibited even greater sensitivity than predicted by analytical models. A 0.5 MPa Exertion load resulted in 537.2 kPa IDP for low magnitude Prestress compared with 373.7 kPa for high magnitude Prestress. Based on these measurements, we developed a simple model that may describe the pressure-shear environment in the nucleus pulposus. These findings may have important implications on our understanding of how mechanical stress contributes to disc health and disease etiology.

Keywords

Intervertebral disc Intradiscal pressure Nucleus pulposus Biomechanics Mechanobiology 

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References

  1. Adams MA, Hutton WC (1983) The effect of posture on the fluid content of lumbar intervertebral discs. Spine 8(6): 665–671CrossRefGoogle Scholar
  2. Adams MA, McMillan DW et al (1996a) Sustained loading generates stress concentrations in lumbar intervertebral discs. Spine 21(4): 434–438CrossRefGoogle Scholar
  3. Adams MA, McNally DS et al (1996b) Stress’ distributions inside intervertebral discs. The effects of age and degeneration. J Bone Joint Surg Br Vol 78(6): 965–972CrossRefGoogle Scholar
  4. Antolic A, Harrison R et al (2007) Effect of extracellular osmolality on cell volume and resting metabolism in mammalian skeletal muscle. Am J Physiol Regul Integr Comp Physiol 292(5): R1994–R2000CrossRefGoogle Scholar
  5. Barbir A, Michalek AJ et al (2010) Effects of enzymatic digestion on compressive properties of rat intervertebral discs. J Biomech 43(6): 1067–1073CrossRefGoogle Scholar
  6. Beckstein JC, Sen S et al (2008) Comparison of animal discs used in disc research to human lumbar disc: axial compression mechanics and glycosaminoglycan content. Spine (Phila Pa 1976) 33(6): E166–E173CrossRefGoogle Scholar
  7. Bush PG, Hall AC (2001) The osmotic sensitivity of isolated and in situ bovine articular chondrocytes. J Orthop Res 19(5): 768–778CrossRefGoogle Scholar
  8. Bush PG, Hall AC (2005) Passive osmotic properties of in situ human articular chondrocytes within non-degenerate and degenerate cartilage. J Cell Physiol 204(1): 309–319CrossRefGoogle Scholar
  9. Carter DR, Wong M (2003) Modelling cartilage mechanobiology. Philos Trans R Soc Lond B Biol Sci 358(1437): 1461–1471CrossRefGoogle Scholar
  10. Cassidy JJ, Silverstein MS et al (1990) A water transport model for the creep response of the intervertebral disc. J Mater Sci Mater Med 1(2): 81–89CrossRefGoogle Scholar
  11. Ching CT, Chow DH et al (2004) Changes in nuclear composition following cyclic compression of the intervertebral disc in an in vivo rat-tail model. Med Eng Phys 26(7): 587–594CrossRefGoogle Scholar
  12. Costi JJ, Hearn TC et al (2002) The effect of hydration on the stiffness of intervertebral discs in an ovine model. Clin Biomech (Bristol, Avon) 17(6): 446–455CrossRefGoogle Scholar
  13. Dennison CR, Wild PM et al (2008) Ex vivo measurement of lumbar intervertebral disc pressure using fibre-Bragg gratings. J Biomech 41(1): 221–225CrossRefGoogle Scholar
  14. Ekstrom L, Holm S et al (2004) In vivo porcine intradiscal pressure as a function of external loading. J Spinal Disord Tech 17(4): 312–316CrossRefGoogle Scholar
  15. Elliott DM, Sarver JJ (2004) Young investigator award winner: validation of the mouse and rat disc as mechanical models of the human lumbar disc. Spine (Phila Pa 1976) 29(7): 713–722CrossRefGoogle Scholar
  16. Elliott DM, Yerramalli CS et al (2008) The effect of relative needle diameter in puncture and sham injection animal models of degeneration. Spine (Phila Pa 1976) 33(6): 588–596CrossRefGoogle Scholar
  17. Gu WY, Yao H (2003) Effects of hydration and fixed charge density on fluid transport in charged hydrated soft tissues. Ann Biomed Eng 31(10): 1162–1170CrossRefGoogle Scholar
  18. Guo X, Lanir Y et al (2007) Effect of osmolarity on the zero-stress state and mechanical properties of aorta. Am J Physiol Heart Circ Physiol 293(4): H2328–H2334CrossRefGoogle Scholar
  19. Han SM, Lee SY et al (2001) Disc hydration measured by magnetic resonance imaging in relation to its compressive stiffness in rat models. Proc Inst Mech Eng H 215(5): 497–501CrossRefGoogle Scholar
  20. Handa T, Ishihara H et al (1997) Effects of hydrostatic pressure on matrix synthesis and matrix metalloproteinase production in the human lumbar intervertebral disc. Spine (Phila Pa 1976) 22(10): 1085–1091CrossRefGoogle Scholar
  21. Haut TL, Haut RC (1997) The state of tissue hydration determines the strain-rate-sensitive stiffness of human patellar tendon. J Biomech 30(1): 79–81CrossRefGoogle Scholar
  22. Hoffman AH, Robichaud DR II et al (2005) Determining the effect of hydration upon the properties of ligaments using pseudo Gaussian stress stimuli. J Biomech 38(8): 1636–1642CrossRefGoogle Scholar
  23. Hsieh AH, Walsh AL et al (2004) Apoptosis corresponds with disc strain environment during dynamic compression. In: Transactions of the 50th annual meeting of the orthopaedic research society, San FranciscoGoogle Scholar
  24. Hsieh AH, Wagner DR, Cheng LY, Lotz JC (2005) Dependence of mechanical behavior of the murine tail disc on regional material properties: a parametric finite element study. ASME J Biomech Eng 127(7): 1158–1167CrossRefGoogle Scholar
  25. Hsieh AH, Hwang D et al (2009) Degenerative anular changes induced by puncture are associated with insufficiency of disc biomechanical function. Spine (Phila Pa 1976) 34(10): 998–1005CrossRefGoogle Scholar
  26. Johannessen W, Vresilovic EJ et al (2004) Intervertebral disc mechanics are restored following cyclic loading and unloaded recovery. Ann Biomed Eng 32(1): 70–76CrossRefGoogle Scholar
  27. Kasra M, Goel V et al (2003) Effect of dynamic hydrostatic pressure on rabbit intervertebral disc cells. J Orthop Res 21(4): 597–603CrossRefGoogle Scholar
  28. Kumaresan S, Yoganandan N et al (1999) Finite element modeling of the cervical spine: role of intervertebral disc under axial and eccentric loads. Med Eng Phys 21(10): 689–700CrossRefGoogle Scholar
  29. Lacroix D, Prendergast PJ (2002) A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J Biomech 35(9): 1163–1171CrossRefGoogle Scholar
  30. Le Maitre CL, Frain J et al (2008) Human cells derived from degenerate intervertebral discs respond differently to those derived from non-degenerate intervertebral discs following application of dynamic hydrostatic pressure. Biorheology 45(5): 563–575Google Scholar
  31. Le Maitre CL, Fotheringham AP et al (2009) Development of an in vitro model to test the efficacy of novel therapies for IVD degeneration. J Tissue Eng Regen Med 3(6): 461–469CrossRefGoogle Scholar
  32. Lotz JC, Colliou OK et al (1998) Compression-induced degeneration of the intervertebral disc: an in vivo mouse model and finite-element study. Spine 23(23): 2493–2506CrossRefGoogle Scholar
  33. MacLean JJ, Lee CR et al (2004) Anabolic and catabolic mRNA levels of the intervertebral disc vary with the magnitude and frequency of in vivo dynamic compression. J Orthop Res 22(6): 1193–1200CrossRefGoogle Scholar
  34. MacLean JJ, Owen JP et al (2007) Role of endplates in contributing to compression behaviors of motion segments and intervertebral discs. J Biomech 40(1): 55–63CrossRefGoogle Scholar
  35. Masuoka K, Michalek AJ et al (2007) Different effects of static versus cyclic compressive loading on rat intervertebral disc height and water loss in vitro. Spine (Phila Pa 1976) 32(18): 1974–1979CrossRefGoogle Scholar
  36. McNally DS, Adams MA (1992) Internal intervertebral disc mechanics as revealed by stress profilometry. Spine (Phila Pa 1976) 17(1): 66–73CrossRefGoogle Scholar
  37. Meakin JR, Hukins DW (2000) Effect of removing the nucleus pulposus on the deformation of the annulus fibrosus during compression of the intervertebral disc. J Biomech 33(5): 575–580CrossRefGoogle Scholar
  38. Meakin JR, Redpath TW et al (2001) The effect of partial removal of the nucleus pulposus from the intervertebral disc on the response of the human annulus fibrosus to compression. Clin Biomech (Bristol, Avon) 16(2): 121–128CrossRefGoogle Scholar
  39. Michalek AJ, Funabashi KL et al (2010) Needle puncture injury of the rat intervertebral disc affects torsional and compressive biomechanics differently. Eur Spine JGoogle Scholar
  40. Nesson S, Yu M et al (2008) Miniature fiber optic pressure sensor with composite polymer-metal diaphragm for intradiscal pressure measurements. J Biomed Opt 13(4): 044040CrossRefGoogle Scholar
  41. Nimer E, Schneiderman R et al (2003) Diffusion and partition of solutes in cartilage under static load. Biophys Chem 106(2): 125–146CrossRefGoogle Scholar
  42. Pflaster DS, Krag MH et al (1997) Effect of test environment on intervertebral disc hydration. Spine (Phila Pa 1976) 22(2): 133–139CrossRefGoogle Scholar
  43. Race A, Broom ND et al (2000) Effect of loading rate and hydration on the mechanical properties of the disc. Spine 25(6): 662–669CrossRefGoogle Scholar
  44. Saxena T, Gilbert JL et al (2009) A versatile mesoindentation system to evaluate the micromechanical properties of soft, hydrated substrates on a cellular scale. J Biomed Mater Res A 90(4): 1206–1217Google Scholar
  45. Seroussi RE, Krag MH et al (1989) Internal deformations of intact and denucleated human lumbar discs subjected to compression, flexion, and extension loads. J Orthop Res 7(1): 122–131CrossRefGoogle Scholar
  46. Thornton GM, Shrive NG et al (2001) Altering ligament water content affects ligament pre-stress and creep behaviour. J Orthop Res 19(5): 845–851CrossRefGoogle Scholar
  47. Wachtel E, Maroudas A (1998) The effects of pH and ionic strength on intrafibrillar hydration in articular cartilage. Biochim Biophys Acta 1381(1): 37–48CrossRefGoogle Scholar
  48. Walsh AJ, Lotz JC (2004) Biological response of the intervertebral disc to dynamic loading. J Biomech 37(3): 329–337CrossRefGoogle Scholar
  49. Wuertz K, Godburn K et al (2009) In vivo remodeling of intervertebral discs in response to short- and long-term dynamic compression. J Orthop Res 27(9): 1235–1242CrossRefGoogle Scholar
  50. Zernia G, Huster D (2006) Collagen dynamics in articular cartilage under osmotic pressure. NMR Biomed 19(8): 1010–1019CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • David Hwang
    • 1
  • Adam S. Gabai
    • 2
  • Miao Yu
    • 2
  • Alvin G. Yew
    • 2
  • Adam H. Hsieh
    • 1
    • 3
    • 4
    Email author
  1. 1.Fischell Department of BioengineeringUniversity of MarylandCollege ParkUSA
  2. 2.Department of Mechanical EngineeringUniversity of MarylandCollege ParkUSA
  3. 3.Department of OrthopaedicsUniversity of MarylandBaltimoreUSA
  4. 4.Orthopaedic Mechanobiology LaboratoryCollege ParkUSA

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