European Spine Journal

, Volume 18, Issue 4, pp 439–448 | Cite as

The elastic fibre network of the human lumbar anulus fibrosus: architecture, mechanical function and potential role in the progression of intervertebral disc degeneration

Review Article
First Online:
Received:
Revised:
Accepted:

Abstract

Elastic fibres are critical constituents of dynamic biological structures that functionally require elasticity and resilience. The network of elastic fibres in the anulus fibrosus of the intervertebral disc is extensive, however until recently, the majority of histological, biochemical and biomechanical studies have focussed on the roles of other extracellular matrix constituents such as collagens and proteoglycans. The resulting lack of detailed descriptions of elastic fibre network architecture and mechanical function has limited understanding of the potentially important contribution made by elastic fibres to healthy disc function and their possible roles in the progression of disc degeneration. In addition, it has made it difficult to postulate what the consequences of elastic fibre related disorders would be for intervertebral disc behaviour, and to develop treatments accordingly. In this paper, we review recent and historical studies which have examined both the structure and the function of the human lumbar anulus fibrosus elastic fibre network, provide a synergistic discussion in an attempt to clarify its potentially critical contribution both to normal intervertebral disc behaviour and the processes relating to its degeneration, and recommend critical areas for future research.

Keywords

Intervertebral disc Anulus fibrosus Elastic fibres Elastin Structure–function 
This is a preview of subscription content, log in to check access.

Notes

Conflict of interest statement

None.

References

  1. 1.
    Acaroglu ER, Iatridis JC, Setton LA, Foster RJ, Mow VC, Weidenbaum M (1995) Degeneration and aging affect the tensile behavior of human lumbar anulus fibrosus. Spine 20:2690–2701. doi: 10.1097/00007632-199512150-00010 PubMedCrossRefGoogle Scholar
  2. 2.
    Akhtar S, Davies JR, Caterson B (2005) Ultrastructural immunolocalization of alpha-elastin and keratan sulfate proteoglycan in normal and scoliotic lumbar disc. Spine 30:1762–1769. doi: 10.1097/01.brs.0000171912.44625.29 PubMedCrossRefGoogle Scholar
  3. 3.
    Armeniades CD, Lake LW, Missirlis YF (1973) Histologic origin of aortic tissue mechanics: the role of collagenous and elastic structures. Appl Polym Symp 22:319–339Google Scholar
  4. 4.
    Ashworth JL, Murphy G, Rock MJ, Sherratt MJ, Shapiro SD, Shuttleworth CA, Kielty CM (1999) Fibrillin degradation by matrix metalloproteinases: implications for connective tissue remodelling. Biochem J 340(Pt 1):171–181. doi: 10.1042/0264-6021:3400171 PubMedCrossRefGoogle Scholar
  5. 5.
    Bruehlmann SB, Hulme PA, Duncan NA (2004) In situ intercellular mechanics of the bovine outer annulus fibrosus subjected to biaxial strains. J Biomech 37:223–231. doi: 10.1016/S0021-9290(03)00244-6 PubMedCrossRefGoogle Scholar
  6. 6.
    Bruehlmann SB, Matyas JR, Duncan NA (2004) ISSLS prize winner: collagen fibril sliding governs cell mechanics in the anulus fibrosus: an in situ confocal microscopy study of bovine discs. Spine 29:2612–2620. doi: 10.1097/01.brs.0000146465.05972.56 PubMedCrossRefGoogle Scholar
  7. 7.
    Buckwalter JA, Cooper RR, Maynard JA (1976) Elastic fibers in human intervertebral discs. J Bone Joint Surg Am 58:73–76PubMedGoogle Scholar
  8. 8.
    Cassidy JJ, Hiltner A, Baer E (1989) Hierarchical structure of the intervertebral disc. Connect Tissue Res 23:75–88. doi: 10.3109/03008208909103905 PubMedCrossRefGoogle Scholar
  9. 9.
    Chrzanowski P, Keller S, Cerreta J, Mandl I, Turino GM (1980) Elastin content of normal and emphysematous lung parenchyma. Am J Med 69:351–359. doi: 10.1016/0002-9343(80)90004-2 PubMedCrossRefGoogle Scholar
  10. 10.
    Cloyd JM, Elliott DM (2007) Elastin content correlates with human disc degeneration in the anulus fibrosus and nucleus pulposus. Spine 32:1826–1831. doi: 10.1097/BRS.0b013e3181132a9d PubMedCrossRefGoogle Scholar
  11. 11.
    Debelle L, Tamburro AM (1999) Elastin: molecular description and function. Int J Biochem Cell Biol 31:261–272. doi: 10.1016/S1357-2725(98)00098-3 PubMedCrossRefGoogle Scholar
  12. 12.
    Eyre DR (1979) Biochemistry of the intervertebral disc. Int Rev Connect Tissue Res 8:227–291PubMedGoogle Scholar
  13. 13.
    Eyre DR, Muir H (1976) Types I and II collagens in intervertebral disc. Interchanging radial distributions in annulus fibrosus. Biochem J 157:267–270PubMedGoogle Scholar
  14. 14.
    Franchi M, Fini M, Quaranta M, De Pasquale V, Raspanti M, Giavaresi G, Ottani V, Ruggeri A (2007) Crimp morphology in relaxed and stretched rat Achilles tendon. J Anat 210:1–7. doi: 10.1111/j.1469-7580.2006.00666.x PubMedCrossRefGoogle Scholar
  15. 15.
    Fujita Y, Duncan NA, Lotz JC (1997) Radial tensile properties of the lumbar annulus fibrosus are site and degeneration dependent. J Orthop Res 15:814–819. doi: 10.1002/jor.1100150605 PubMedCrossRefGoogle Scholar
  16. 16.
    Fung YC (1981) Biomechanics: mechanical properties of living tissues. Springer, New YorkGoogle Scholar
  17. 17.
    Gosline JM (1976) The physical properties of elastic tissue. Int Rev Connect Tissue Res 7:211–249PubMedGoogle Scholar
  18. 18.
    Guerin HA, Elliott DM (2006) Degeneration affects the fiber reorientation of human annulus fibrosus under tensile load. J Biomech 39:1410–1418. doi: 10.1016/j.jbiomech.2005.04.007 PubMedCrossRefGoogle Scholar
  19. 19.
    Guerin HL, Elliott DM (2007) Quantifying the contributions of structure to annulus fibrosus mechanical function using a nonlinear, anisotropic, hyperelastic model. J Orthop Res 25:508–516. doi: 10.1002/jor.20324 PubMedCrossRefGoogle Scholar
  20. 20.
    Hickey DS, Hukins DW (1981) Collagen fibril diameters and elastic fibres in the annulus fibrosus of human fetal intervertebral disc. J Anat 133:351–357PubMedGoogle Scholar
  21. 21.
    Holm S (1996) Nutrition and pathophysiologic aspects of the lumbar intervertebral disc. In: Wiesel SW, Weinstein JN, Herkowitz HN, Dvorak J, Bell G (eds) The lumbar spine. Saunders, Philadelphia, pp 285–309Google Scholar
  22. 22.
    Iatridis JC, ap Gwynn I (2004) Mechanisms for mechanical damage in the intervertebral disc annulus fibrosus. J Biomech 37:1165–1175. doi: 10.1016/j.jbiomech.2003.12.026 PubMedCrossRefGoogle Scholar
  23. 23.
    Iatridis JC, MacLean JJ, Ryan DA (2005) Mechanical damage to the intervertebral disc annulus fibrosus subjected to tensile loading. J Biomech 38:557–565. doi: 10.1016/j.jbiomech.2004.03.038 PubMedCrossRefGoogle Scholar
  24. 24.
    Ishii T, Asuwa N (2000) Collagen and elastin degradation by matrix metalloproteinases and tissue inhibitors of matrix metalloproteinase in aortic dissection. Hum Pathol 31:640–646. doi: 10.1053/hupa.2000.7642 PubMedCrossRefGoogle Scholar
  25. 25.
    Johnson EF, Berryman H, Mitchell R, Wood WB (1985) Elastic fibres in the anulus fibrosus of the adult human lumbar intervertebral disc. A preliminary report. J Anat 143:57–63PubMedGoogle Scholar
  26. 26.
    Johnson EF, Caldwell RW, Berryman HE, Miller A, Chetty K (1984) Elastic fibers in the anulus fibrosus of the dog intervertebral disc. Acta Anat (Basel) 118:238–242. doi: 10.1159/000145851 CrossRefGoogle Scholar
  27. 27.
    Johnson EF, Chetty K, Moore IM, Stewart A, Jones W (1982) The distribution and arrangement of elastic fibres in the intervertebral disc of the adult human. J Anat 135:301–309PubMedGoogle Scholar
  28. 28.
    Kakivaya SR, Hoeve CA (1975) The glass point of elastin. Proc Natl Acad Sci USA 72:3505–3507. doi: 10.1073/pnas.72.9.3505 PubMedCrossRefGoogle Scholar
  29. 29.
    Kielty CM (2006) Elastic fibres in health and disease. Expert Rev Mol Med 8:1–23. doi: 10.1017/S146239940600007X PubMedCrossRefGoogle Scholar
  30. 30.
    Kielty CM, Sherratt MJ, Shuttleworth CA (2002) Elastic fibres. J Cell Sci 115:2817–2828PubMedGoogle Scholar
  31. 31.
    Klein JA, Hukins DW (1982) X-ray diffraction demonstrates reorientation of collagen fibres in the annulus fibrosus during compression of the intervertebral disc. Biochim Biophys Acta 717:61–64PubMedGoogle Scholar
  32. 32.
    Klein JA, Hukins DW (1982) Collagen fibre orientation in the annulus fibrosus of intervertebral disc during bending and torsion measured by X-ray diffraction. Biochim Biophys Acta 719:98–101PubMedGoogle Scholar
  33. 33.
    Korecki CL, MacLean JJ, Iatridis JC (2007) Characterization of an in vitro intervertebral disc organ culture system. Eur Spine J 16:1029–1037. doi: 10.1007/s00586-007-0327-9 PubMedCrossRefGoogle Scholar
  34. 34.
    Kozaci LD, Guner A, Oktay G, Guner G (2006) Alterations in biochemical components of extracellular matrix in intervertebral disc herniation: role of MMP-2 and TIMP-2 in type II collagen loss. Cell Biochem Funct 24:431–436. doi: 10.1002/cbf.1250 PubMedCrossRefGoogle Scholar
  35. 35.
    Le Maitre CL, Freemont AJ, Hoyland JA (2006) Human disc degeneration is associated with increased MMP 7 expression. Biotech Histochem 81:125–131. doi: 10.1080/10520290601005298 PubMedCrossRefGoogle Scholar
  36. 36.
    Le Maitre CL, Pockert A, Buttle DJ, Freemont AJ, Hoyland JA (2007) Matrix synthesis and degradation in human intervertebral disc degeneration. Biochem Soc Trans 35:652–655. doi: 10.1042/BST0350652 PubMedCrossRefGoogle Scholar
  37. 37.
    Lee TC, Midura RJ, Hascall VC, Vesely I (2001) The effect of elastin damage on the mechanics of the aortic valve. J Biomech 34:203–210. doi: 10.1016/S0021-9290(00)00187-1 PubMedCrossRefGoogle Scholar
  38. 38.
    Marchand F, Ahmed AM (1990) Investigation of the laminate structure of lumbar disc anulus fibrosus. Spine 15:402–410. doi: 10.1097/00007632-199005000-00011 PubMedCrossRefGoogle Scholar
  39. 39.
    Mecham RP, Broekelmann TJ, Fliszar CJ, Shapiro SD, Welgus HG, Senior RM (1997) Elastin degradation by matrix metalloproteinases. Cleavage site specificity and mechanisms of elastolysis. J Biol Chem 272:18071–18076. doi: 10.1074/jbc.272.29.18071 PubMedCrossRefGoogle Scholar
  40. 40.
    Melrose J, Smith SM, Appleyard RC, Little CB (2008) Aggrecan, versican and type VI collagen are components of annular translamellar crossbridges in the intervertebral disc. Eur Spine J 17:314–324. doi: 10.1007/s00586-007-0538-0 PubMedCrossRefGoogle Scholar
  41. 41.
    Mikawa Y, Hamagami H, Shikata J, Yamamuro T (1986) Elastin in the human intervertebral disk. A histological and biochemical study comparing it with elastin in the human yellow ligament. Arch Orthop Trauma Surg 105:343–349. doi: 10.1007/BF00449940 PubMedCrossRefGoogle Scholar
  42. 42.
    Missirlis YF (1977) Use of enzymolysis techniques in studying the mechanical properties of connective tissue components. J Bioeng 1:215–222PubMedGoogle Scholar
  43. 43.
    Mizuno H, Roy AK, Zaporojan V, Vacanti CA, Ueda M, Bonassar LJ (2006) Biomechanical and biochemical characterization of composite tissue-engineered intervertebral discs. Biomaterials 27:362–370. doi: 10.1016/j.biomaterials.2005.06.042 PubMedCrossRefGoogle Scholar
  44. 44.
    Montes GS (1996) Structural biology of the fibres of the collagenous and elastic systems. Cell Biol Int 20:15–27. doi: 10.1006/cbir.1996.0004 PubMedCrossRefGoogle Scholar
  45. 45.
    Nerurkar NL, Elliott DM, Mauck RL (2007) Mechanics of oriented electrospun nanofibrous scaffolds for annulus fibrosus tissue engineering. J Orthop Res 25:1018–1028. doi: 10.1002/jor.20384 PubMedCrossRefGoogle Scholar
  46. 46.
    Oakes BW, Bialkower B (1977) Biomechanical and ultrastructural studies on the elastic wing tendon from the domestic fowl. J Anat 123:369–387PubMedGoogle Scholar
  47. 47.
    O’Halloran DM, Pandit AS (2007) Tissue-engineering approach to regenerating the intervertebral disc. Tissue Eng 13:1927–1954. doi: 10.1089/ten.2005.0608 PubMedCrossRefGoogle Scholar
  48. 48.
    Olczyk K (1994) Age-related changes of elastin content in human intervertebral discs. Folia Histochem Cytobiol 32:41–44PubMedGoogle Scholar
  49. 49.
    Oxlund H, Manschot J, Viidik A (1988) The role of elastin in the mechanical properties of skin. J Biomech 21:213–218. doi: 10.1016/0021-9290(88)90172-8 PubMedCrossRefGoogle Scholar
  50. 50.
    Pearcy MJ, Tibrewal SB (1984) Lumbar intervertebral disc and ligament deformations measured in vivo. Clin Orthop Relat Res 191:281–286PubMedGoogle Scholar
  51. 51.
    Pezowicz CA, Robertson PA, Broom ND (2005) Intralamellar relationships within the collagenous architecture of the annulus fibrosus imaged in its fully hydrated state. J Anat 207:299–312. doi: 10.1111/j.1469-7580.2005.00467.x PubMedCrossRefGoogle Scholar
  52. 52.
    Pezowicz CA, Robertson PA, Broom ND (2006) The structural basis of interlamellar cohesion in the intervertebral disc wall. J Anat 208:317–330. doi: 10.1111/j.1469-7580.2006.00536.x PubMedCrossRefGoogle Scholar
  53. 53.
    Pezowicz CA, Schechtman HP, Robertson PA, Broom ND (2006) Mechanisms of anular failure resulting from excessive intradiscal pressure: a microstructural-micromechanical investigation. Spine 31:2891–2903. doi: 10.1097/01.brs.0000248412.82700.8b PubMedCrossRefGoogle Scholar
  54. 54.
    Postacchini F, Bellocci M, Massobrio M (1984) Morphologic changes in annulus fibrosus during aging. An ultrastructural study in rats. Spine 9:596–603. doi: 10.1097/00007632-198409000-00010 PubMedCrossRefGoogle Scholar
  55. 55.
    Raspanti M, Manelli A, Franchi M, Ruggeri A (2005) The 3D structure of crimps in the rat Achilles tendon. Matrix Biol 24:503–507. doi: 10.1016/j.matbio.2005.07.006 PubMedCrossRefGoogle Scholar
  56. 56.
    Scarselli V (1961) Increase in elastin content of the human aorta during growth. Nature 191:710–711. doi: 10.1038/191710a0 PubMedCrossRefGoogle Scholar
  57. 57.
    Schollum ML, Robertson PA, Broom ND (2008) ISSLS prize winner: microstructure and mechanical disruption of the lumbar disc annulus: part I: a microscopic investigation of the translamellar bridging network. Spine 33:2702–2710PubMedCrossRefGoogle Scholar
  58. 58.
    Sedowofia KA, Tomlinson IW, Weiss JB, Hilton RC, Jayson MI (1982) Collagenolytic enzyme systems in human intervertebral disc: their control, mechanism, and their possible role in the initiation of biomechanical failure. Spine 7:213–222. doi: 10.1097/00007632-198205000-00005 PubMedCrossRefGoogle Scholar
  59. 59.
    Shah JS, Hampson WG, Jayson MI (1978) The distribution of surface strain in the cadaveric lumbar spine. J Bone Joint Surg Br 60:246–251PubMedGoogle Scholar
  60. 60.
    Sherratt MJ, Baldock C, Haston JL, Holmes DF, Jones CJ, Shuttleworth CA, Wess TJ, Kielty CM (2003) Fibrillin microfibrils are stiff reinforcing fibres in compliant tissues. J Mol Biol 332:183–193. doi: 10.1016/S0022-2836(03)00829-5 PubMedCrossRefGoogle Scholar
  61. 61.
    Smith LJ, Byers S, Costi JJ, Fazzalari NL (2008) Elastic fibers enhance the mechanical integrity of the human lumbar anulus fibrosus in the radial direction. Ann Biomed Eng 36:214–223. doi: 10.1007/s10439-007-9421-8 PubMedCrossRefGoogle Scholar
  62. 62.
    Smith LJ, Fazzalari NL (2006) Regional variations in the density and arrangement of elastic fibres in the anulus fibrosus of the human lumbar disc. J Anat 209:359–367. doi: 10.1111/j.1469-7580.2006.00610.x PubMedCrossRefGoogle Scholar
  63. 63.
    Smith LJ, Fazzalari NL (2008) Structural changes to the human lumbar anulus fibrosus elastic fibre network following radial tensile deformation. 54th Annual Meeting of the Orthopaedic Research Society. San Francisco, CAGoogle Scholar
  64. 64.
    Stokes IA (1987) Surface strain on human intervertebral discs. J Orthop Res 5:348–355. doi: 10.1002/jor.1100050306 PubMedCrossRefGoogle Scholar
  65. 65.
    Toshima M, Ohtani Y, Ohtani O (2004) Three-dimensional architecture of elastin and collagen fiber networks in the human and rat lung. Arch Histol Cytol 67:31–40. doi: 10.1679/aohc.67.31 PubMedCrossRefGoogle Scholar
  66. 66.
    Tsantrizos A, Ito K, Aebi M, Steffen T (2005) Internal strains in healthy and degenerated lumbar intervertebral discs. Spine 30:2129–2137. doi: 10.1097/01.brs.0000181052.56604.30 PubMedCrossRefGoogle Scholar
  67. 67.
    Urban J (1996). Disc biochemistry in relation to function. In: Wiesel SW, Weinstein JN, Herkowitz HN, Dvorak J, Bell G (eds) The lumbar spine. Saunders, Philadelphia, pp 271–280Google Scholar
  68. 68.
    Vesely I (1998) The role of elastin in aortic valve mechanics. J Biomech 31:115–123. doi: 10.1016/S0021-9290(97)00122-X PubMedCrossRefGoogle Scholar
  69. 69.
    Wagner DR, Reiser KM, Lotz JC (2006) Glycation increases human annulus fibrosus stiffness in both experimental measurements and theoretical predictions. J Biomech 39:1021–1029. doi: 10.1016/j.jbiomech.2005.02.013 PubMedCrossRefGoogle Scholar
  70. 70.
    Weiler WC, Nerlich NA, Zipperer ZJ, Bachmeier BB, Boos BN (2002) Expression of major matrix metalloproteinases is associated with intervertebral disc degradation and resorption. Eur Spine J 11:308–320. doi: 10.1007/s00586-002-0472-0 PubMedCrossRefGoogle Scholar
  71. 71.
    Wilda H, Gough JE (2006) In vitro studies of annulus fibrosus disc cell attachment, differentiation and matrix production on PDLLA/45S5 Bioglass composite films. Biomaterials 27:5220–5229. doi: 10.1016/j.biomaterials.2006.06.008 PubMedCrossRefGoogle Scholar
  72. 72.
    Yu J, Fairbank JC, Roberts S, Urban JP (2005) The elastic fiber network of the anulus fibrosus of the normal and scoliotic human intervertebral disc. Spine 30:1815–1820. doi: 10.1097/01.brs.0000173899.97415.5b PubMedCrossRefGoogle Scholar
  73. 73.
    Yu J, Tirlapur U, Fairbank J, Handford P, Roberts S, Winlove CP, Cui Z, Urban JP (2007) Microfibrils, elastin fibres and collagen fibres in the human intervertebral disc and bovine tail disc. J Anat 210:460–471. doi: 10.1111/j.1469-7580.2007.00707.x PubMedCrossRefGoogle Scholar
  74. 74.
    Yu J, Winlove PC, Roberts S, Urban JP (2002) Elastic fibre organization in the intervertebral discs of the bovine tail. J Anat 201:465–475. doi: 10.1046/j.1469-7580.2002.00111.x PubMedCrossRefGoogle Scholar
  75. 75.
    Yuan H, Kononov S, Cavalcante FS, Lutchen KR, Ingenito EP, Suki B (2000) Effects of collagenase and elastase on the mechanical properties of lung tissue strips. J Appl Physiol 89:3–14PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Bone and Joint Research Laboratory, Division of Tissue PathologyInstitute of Medical and Veterinary Science and Hanson InstituteAdelaideAustralia
  2. 2.Discipline of PathologyThe University of AdelaideAdelaideAustralia

Personalised recommendations