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European Spine Journal

, Volume 26, Issue 1, pp 248–258 | Cite as

Staying connected: structural integration at the intervertebral disc–vertebra interface of human lumbar spines

  • Sharon BrownEmail author
  • Samantha Rodrigues
  • Christopher Sharp
  • Kelly Wade
  • Neil Broom
  • Iain W. McCall
  • Sally Roberts
Original Article

Abstract

Purpose

To investigate the microscopic fibrous integration between the intervertebral disc, cartilage endplates and vertebral endplates in human lumbar spines of varying degrees of degeneration using differential interference contrast (DIC) optics. Weakness at these junctions is considered to be an important factor in the aetiology of disc herniations.

Methods

Magnetic resonance images (MRIs) of cadaveric lumbar spines were graded for degeneration and motion segments from a range of degenerative grades isolated and bisected sagittally. Following fixation and decalcification, these were cut into segments containing anterior or posterior annulus fibrosus or nucleus pulposus. The segments were cryo-sectioned and sections visualised using both standard light and DIC microscopy.

Results

Detachment at the interface between the disc and vertebrae increased with greater degenerative grade (from 1.9 % in Grade I to 28 % in Grade V), especially at the boundary between the cartilage and vertebral endplates. DIC microscopy revealed the fibrous organisation at the IVD–cartilage endplate interface with structural features, such as annular lamellae branching and nodal insertions in the nucleus pulposus region; these have been previously observed in ovine spines, but were less uniform in humans. Structural integrity of the IVD and cartilage endplate was also lost with increasing degeneration.

Conclusions

This preliminary study shows that microscopic structural features may act to maintain attachment between the IVD and CEP in the human spine. Loss of structural integrity in this region may destabilise the spine, possibly altering the mechanical environment of the cells in the disc and so potentially contribute to the aetiopathogenesis of IVD degeneration.

Keywords

Differential interference contrast (DIC) microscopy Lamellae branching Nodal insertions Collagen Degeneration 

Notes

Acknowledgments

This study was supported by the Orthopaedic Institute Ltd, Robert Jones and Agnes Hunt Orthopaedic Hospital, Oswestry and a Travelling Fellowship from the Winston Churchill Memorial Trust [Sharon Owen (nee Brown)]. We are grateful to Mike Haddaway and Dr Victor Cassar-Pullicino and members of the Imaging Department for their support.

Compliance with ethical standards

Conflict of interest

All the authors declare that no competing interests exist.

References

  1. 1.
    Alini M, Eisenstein SM, Ito K, Little C, Kettler AA, Masuda K, Melrose J, Ralphs J, Stokes I, Wilke HJ (2008) Are animal models useful for studying human disc disorders/degeneration? Eur Spine J 17:2–19CrossRefPubMedGoogle Scholar
  2. 2.
    Aoki J, Yamamoto I, Kitamura N, Sone T, Itoh H, Torizuka K, Takasu K (1987) End plate of the discovertebral joint: degenerative change in the elderly adult. Radiology 164:411–414CrossRefPubMedGoogle Scholar
  3. 3.
    Balkovec C, Adams MA, Dolan P, McGill SM (2015) Annulus fibrosus can strip hyaline cartilage end plate from subchondral bone: a study of the intervertebral disk in tension. Global Spine J 5:360–365CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Battie MC, Lazary A, Fairbank J, Eisenstein S, Heywood C, Brayda-Bruno M, Varga PP, McCall I (2014) Disc degeneration-related clinical phenotypes. Eur Spine J 23(Suppl 3):S305–S314CrossRefPubMedGoogle Scholar
  5. 5.
    Benneker LM, Heini PF, Alini M, Anderson SE, Ito K (2005) 2004 young investigator award winner: vertebral endplate marrow contact channel occlusions and intervertebral disc degeneration. Spine (Phila Pa 1976) 30:167–173CrossRefGoogle Scholar
  6. 6.
    Boos N, Weissbach S, Rohrbach H, Weiler C, Spratt KF, Nerlich AG (2002) Classification of age-related changes in lumbar intervertebral discs: 2002 Volvo Award in basic science. Spine 27:2631–2644CrossRefPubMedGoogle Scholar
  7. 7.
    Broberg KB (1983) On the mechanical behaviour of intervertebral discs. Spine (Phila Pa 1976) 8:151–165CrossRefGoogle Scholar
  8. 8.
    Corsi A, De Maio F, Mancini F, Ippolito E, Riminucci M, Bianco P (2008) Notochordal inclusions in the vertebral bone marrow. J Bone Miner Res 23:572–575CrossRefPubMedGoogle Scholar
  9. 9.
    Detiger SE, Holewijn RM, Hoogendoorn RJ, van Royen BJ, Helder MN, Berger FH, Kuijer JP, Smit TH (2015) MRI T2* mapping correlates with biochemistry and histology in intervertebral disc degeneration in a large animal model. Eur Spine J 24:1935–1943CrossRefPubMedGoogle Scholar
  10. 10.
    Ferguson SJ, Steffen T (2003) Biomechanics of the aging spine. Eur Spine J 12(Suppl 2):S97–S103CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Herrero CF, Garcia SB, Garcia LV, Aparecido Defino HL (2014) Endplates changes related to age and vertebral segment. Biomed Res Int 2014:545017CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Humzah MD, Soames RW (1988) Human intervertebral disc: structure and function. Anat Rec 220:337–356CrossRefPubMedGoogle Scholar
  13. 13.
    Inoue H (1981) Three-dimensional architecture of lumbar intervertebral discs. Spine (Phila Pa 1976) 6:139–146CrossRefGoogle Scholar
  14. 14.
    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 135:301–309PubMedPubMedCentralGoogle Scholar
  15. 15.
    Junhui L, Zhengfeng M, Zhi S, Mamuti M, Lu H, Shunwu F, Fengdong Z (2015) Anchorage of annulus fibrosus within the vertebral endplate with reference to disc herniation. Microsc Res Tech 78:754–760CrossRefPubMedGoogle Scholar
  16. 16.
    Lama P, Zehra U, Balkovec C, Claireaux HA, Flower L, Harding IJ, Dolan P, Adams MA (2014) Significance of cartilage endplate within herniated disc tissue. Eur Spine J 23:1869–1877CrossRefPubMedGoogle Scholar
  17. 17.
    Maroudas A, Stockwell RA, Nachemson A, Urban J (1975) Factors involved in the nutrition of the human lumbar intervertebral disc: cellularity and diffusion of glucose in vitro. J Anat 120:113–130PubMedPubMedCentralGoogle Scholar
  18. 18.
    McFadden KD, Taylor JR (1989) End-plate lesions of the lumbar spine. Spine (Phila Pa 1976) 14:867–869CrossRefGoogle Scholar
  19. 19.
    Moon SM, Yoder JH, Wright AC, Smith LJ, Vresilovic EJ, Elliott DM (2013) Evaluation of intervertebral disc cartilaginous endplate structure using magnetic resonance imaging. Eur Spine J 22:1820–1828CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Moore RJ, Vernon-Roberts B, Fraser RD, Osti OL, Schembri M (1996) The origin and fate of herniated lumbar intervertebral disc tissue. Spine 21:2149–2155CrossRefPubMedGoogle Scholar
  21. 21.
    Nosikova YS, Santerre JP, Grynpas M, Gibson G, Kandel RA (2012) Characterization of the annulus fibrosus-vertebral body interface: identification of new structural features. J Anat 221:577–589CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Paietta RC, Burger EL, Ferguson VL (2013) Mineralization and collagen orientation throughout aging at the vertebral endplate in the human lumbar spine. J Struct Biol 184:310–320CrossRefPubMedGoogle Scholar
  23. 23.
    Pezowicz CA, Robertson PA, Broom ND (2006) The structural basis of interlamellar cohesion in the intervertebral disc wall. J Anat 208:317–330CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Pfirrmann CW, Metzdorf A, Zanetti M, Hodler J, Boos N (2001) Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine (Phila Pa 1976) 26:1873–1878CrossRefGoogle Scholar
  25. 25.
    Rajasekaran S, Bajaj N, Tubaki V, Kanna RM, Shetty AP (2013) ISSLS Prize winner: the anatomy of failure in lumbar disc herniation: an in vivo, multimodal, prospective study of 181 subjects. Spine (Phila Pa 1976) 38:1491–1500CrossRefGoogle Scholar
  26. 26.
    Roberts S, Menage J, Eisenstein SM (1993) The cartilage end-plate and intervertebral disc in scoliosis: calcification and other sequelae. J Orthop Res 11:747–757CrossRefPubMedGoogle Scholar
  27. 27.
    Roberts S, Menage J, Urban JP (1989) Biochemical and structural properties of the cartilage end-plate and its relation to the intervertebral disc. Spine (Phila Pa 1976) 14:166–174CrossRefGoogle Scholar
  28. 28.
    Rodrigues SA, Thambyah A, Broom ND (2015) A multiscale structural investigation of the annulus-endplate anchorage system and its mechanisms of failure. Spine J 15:405–416CrossRefPubMedGoogle Scholar
  29. 29.
    Rodrigues SA, Wade KR, Thambyah A, Broom ND (2012) Micromechanics of annulus-end plate integration in the intervertebral disc. Spine J 12:143–150CrossRefPubMedGoogle Scholar
  30. 30.
    Schollum ML, Robertson PA, Broom ND (2009) A microstructural investigation of intervertebral disc lamellar connectivity: detailed analysis of the translamellar bridges. J Anat 214:805–816CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Tanaka M, Nakahara S, Inoue H (1993) A pathologic study of discs in the elderly. Separation between the cartilaginous endplate and the vertebral body. Spine (Phila Pa 1976) 18:1456–1462CrossRefGoogle Scholar
  32. 32.
    Taylor JR (1975) Growth of human intervertebral discs and vertebral bodies. J Anat 120:49–68PubMedPubMedCentralGoogle Scholar
  33. 33.
    Veres SP, Robertson PA, Broom ND (2009) The morphology of acute disc herniation: a clinically relevant model defining the role of flexion. Spine (Phila Pa 1976) 34:2288–2296CrossRefGoogle Scholar
  34. 34.
    Wade KR, Robertson PA, Broom ND (2011) A fresh look at the nucleus-endplate region: new evidence for significant structural integration. Eur Spine J 20:1225–1232CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Wade KR, Robertson PA, Broom ND (2012) On how nucleus-endplate integration is achieved at the fibrillar level in the ovine lumbar disc. J Anat 221:39–46CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Wade KR, Robertson PA, Broom ND (2012) On the extent and nature of nucleus-annulus integration. Spine (Phila Pa 1976) 37:1826–1833CrossRefGoogle Scholar
  37. 37.
    Wade KR, Robertson PA, Broom ND (2014) Influence of maturity on nucleus-endplate integration in the ovine lumbar spine. Eur Spine J 23:732–744CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Wade KR, Robertson PA, Thambyah A, Broom ND (2015) “Surprise” loading in flexion increases the risk of disc herniation due to annulus-endplate junction failure: a mechanical and microstructural investigation. Spine (Phila Pa 1976) 40:891–901CrossRefGoogle Scholar
  39. 39.
    Wang Y, Battie MC, Videman T (2012) A morphological study of lumbar vertebral endplates: radiographic, visual and digital measurements. Eur Spine J 21:2316–2323CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Wang Y, Videman T, Battie MC (2013) Morphometrics and lesions of vertebral end plates are associated with lumbar disc degeneration: evidence from cadaveric spines. J Bone Joint Surg Am 95:e26CrossRefPubMedGoogle Scholar
  41. 41.
    Yu J, Schollum ML, Wade KR, Broom ND, Urban JP (2015) A detailed examination of the elastic network leads to a new understanding of annulus fibrosus organisation. Spine (Phila Pa 1976) 40:1149–1157CrossRefGoogle Scholar
  42. 42.
    Yu J, Winlove PC, Roberts S, Urban JP (2002) Elastic fibre organization in the intervertebral discs of the bovine tail. J Anat 201:465–475CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Zehra U, Robson-Brown K, Adams MA, Dolan P (2015) Porosity and thickness of the vertebral endplate depend on local mechanical loading. Spine (Phila Pa 1976) 40:1173–1180CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Sharon Brown
    • 1
    Email author
  • Samantha Rodrigues
    • 2
  • Christopher Sharp
    • 3
  • Kelly Wade
    • 2
  • Neil Broom
    • 2
  • Iain W. McCall
    • 1
  • Sally Roberts
    • 1
  1. 1.Spinal StudiesRJAH Orthopaedic Hospital Foundation Trust and ISTM (Keele University)OswestryUK
  2. 2.Department of Chemical and Materials EngineeringUniversity of AucklandAucklandNew Zealand
  3. 3.University Centre Shrewsbury, Institute of MedicineUniversity of ChesterShrewsburyUK

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