Advertisement

European Spine Journal

, Volume 21, Supplement 6, pp 810–818 | Cite as

Age-related changes in human cervical, thoracal and lumbar intervertebral disc exhibit a strong intra-individual correlation

  • C. Weiler
  • M. Schietzsch
  • T. Kirchner
  • A. G. Nerlich
  • N. Boos
  • K. Wuertz
Original Article

Abstract

Introduction

Intervertebral disc (IVD) degeneration is characterized as a multifactorial disease, in which the hereditary background is thought to be of high importance. Accordingly, one would expect all spinal levels (lumbar/cervical/thoracal) to be affected by above-average disc degeneration in genetically predisposed individuals. The aim of this study, therefore, was to analyze the amount of degenerative changes in different spine levels in humans from different ages.

Materials and methods

In detail, the presence, localization and abundance of histomorphological changes in the annulus fibrosus (AF) and nucleus pulposus (NP) in the cervical (C5/C6), thoracic (T2/T3) and lumbar (L2/L3) spine were investigated in complete autopsy IVD specimens (47 individuals) covering a complete age range (0–95 years).

Results

Results indicate that the highest degree of histo-degenerative changes were observed in the NP in all spine levels and showed an age-related expression pattern. With regard to the different spine levels, lumbar disc specimen showed significantly more degenerative changes compared to cervical and thoracic discs, whereas no statistical difference was observed between cervical and thoracic discs. In summary, highest grades of degeneration were observed in lumbar discs (especially in the NP). Intra-individual correlations between the degeneration score in the different levels showed a significant individual concordance.

Conclusions

The intra-individual correlation of degenerative changes in all three examined spine regions further supports the notion that individual, i.e. genetic factors are strong predisposing factor for the development of age-related disc alterations.

Keywords

Disc degeneration Histological degeneration score (HDS) Cervical, thoracic and lumbar spine Aging Intra-individual correlation 

Notes

Acknowledgments

This study was made possible by grants from AOSpine (SRN 02/103 and AOSBRC-07-03). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of AOSpine. The investigation was undertaken in accordance with the local ethic committee guidelines.

Conflict of interest

None.

References

  1. 1.
    Adams MA, Roughley PJ (2006) What is intervertebral disc degeneration, and what causes it? Spine 31:2151–2161PubMedCrossRefGoogle Scholar
  2. 2.
    Baba H, Maezawa Y, Furusawa N, Fukuda M, Uchida K, Kokubo Y, Imura S (1997) Herniated cervical intervertebral discs: histological and immunohistochemical characteristics. Eur J Histochem 41:261–270PubMedGoogle Scholar
  3. 3.
    Battie MC, Videman T (2006) Lumbar disc degeneration: epidemiology and genetics. J Bone Joint Surg Am 88(Suppl 2):3–9PubMedCrossRefGoogle Scholar
  4. 4.
    Battie MC, Videman T, Kaprio J, Gibbons LE, Gill K, Manninen H, Saarela J, Peltonen L (2009) The Twin Spine Study: contributions to a changing view of disc degeneration. Spine J 9:47–59PubMedCrossRefGoogle Scholar
  5. 5.
    Battie MC, Videman T, Levalahti E, Gill K, Kaprio J (2007) Heritability of low back pain and the role of disc degeneration. Pain 131:272–280PubMedCrossRefGoogle Scholar
  6. 6.
    Bibby SR, Urban JP (2004) Effect of nutrient deprivation on the viability of intervertebral disc cells. Eur Spine J 13(8):695–701Google Scholar
  7. 7.
    Boos N, Nerlich AG, Wiest I, von der Mark K, Aebi M (1997) Immunolocalization of type X collagen in human lumbar intervertebral discs during ageing and degeneration. Histochem Cell Biol 108:471–480PubMedCrossRefGoogle Scholar
  8. 8.
    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 27:2631–2644PubMedCrossRefGoogle Scholar
  9. 9.
    Buckwalter JA (1995) Aging and degeneration of the human intervertebral disc. Spine 20:1307–1314PubMedGoogle Scholar
  10. 10.
    Buckwalter JA, Roughley PJ, Rosenberg LC (1994) Age-related changes in cartilage proteoglycans: quantitative electron microscopic studies. Microsc Res Tech 28:398–408PubMedCrossRefGoogle Scholar
  11. 11.
    Busscher I, Ploegmakers JJ, Verkerke GJ, Veldhuizen AG (2010) Comparative anatomical dimensions of the complete human and porcine spine. Eur Spine J 19:1104–1114PubMedCrossRefGoogle Scholar
  12. 12.
    Chan D, Song Y, Sham P, Cheung KM (2006) Genetics of disc degeneration. Eur Spine J 15(Suppl 3):S317–S325 (epub;%2006 Jul 4)Google Scholar
  13. 13.
    Christe A, Laubli R, Guzman R, Berlemann U, Moore RJ, Schroth G, Vock P, Lovblad KO (2005) Degeneration of the cervical disc: histology compared with radiography and magnetic resonance imaging. Neuroradiology 47:721–729PubMedCrossRefGoogle Scholar
  14. 14.
    Coventry MB, Ghormley RK, Kernohan JW (1945) The intervertebral disc: its microscopic anatomy and pathology. Part I. Anatomy, development, and physiology. J Bone Joint Surg Am 27:105–112Google Scholar
  15. 15.
    Coventry MB, Ghormley RK, Kernohan JW (1945) The intervertebral disc: its microscopic anatomy and pathology. Part II. Changes in the intervertebral disc concomitant with age. J Bone Joint Surg Am 27:233–247Google Scholar
  16. 16.
    Coventry MB, Ghormley RK, Kernohan JW (1945) The intervertebral disc: its microscopic anatomy and pathology. Part III. Pathological changes in the intervertebral disc. J Bone Joint Surg Am 27:460–474Google Scholar
  17. 17.
    Dai L (1998) Disc degeneration and cervical instability. Correlation of magnetic resonance imaging with radiography. Spine (Phila Pa 1976) 23:1734–1738CrossRefGoogle Scholar
  18. 18.
    Furusawa N, Baba H, Miyoshi N, Maezawa Y, Uchida K, Kokubo Y, Fukuda M (2001) Herniation of cervical intervertebral disc: immunohistochemical examination and measurement of nitric oxide production. Spine 26:1110–1116PubMedCrossRefGoogle Scholar
  19. 19.
    Gilad I, Nissan M (1986) A study of vertebra and disc geometric relations of the human cervical and lumbar spine. Spine (Phila Pa 1976) 11:154–157CrossRefGoogle Scholar
  20. 20.
    Girard CJ, Schweitzer ME, Morrison WB, Parellada JA, Carrino JA (2004) Thoracic spine disc-related abnormalities: longitudinal MR imaging assessment. Skeletal Radiol 33:216–222PubMedCrossRefGoogle Scholar
  21. 21.
    Gore DR (2001) Roentgenographic findings in the cervical spine in asymptomatic persons: a ten-year follow-up. Spine (Phila Pa 1976) 26:2463–2466CrossRefGoogle Scholar
  22. 22.
    Gore DR, Sepic SB, Gardner GM (1986) Roentgenographic findings of the cervical spine in asymptomatic people. Spine (Phila Pa 1976) 11:521–524CrossRefGoogle Scholar
  23. 23.
    Guehring T, Wilde G, Sumner M, Grunhagen T, Karney GB, Tirlapur UK, Urban JP (2009) Notochordal intervertebral disc cells: sensitivity to nutrient deprivation. Arthritis Rheum 60:1026–1034PubMedCrossRefGoogle Scholar
  24. 24.
    Hadjipavlou AG, Tzermiadianos MN, Bogduk N, Zindrick MR (2008) The pathophysiology of disc degeneration: a critical review. J Bone Joint Surg Br 90:1261–1270PubMedCrossRefGoogle Scholar
  25. 25.
    Haefeli M, Kalberer F, Saegesser D, Nerlich AG, Boos N, Paesold G (2006) The course of macroscopic degeneration in the human lumbar intervertebral disc. Spine 31:1522–1531PubMedCrossRefGoogle Scholar
  26. 26.
    Horner HA, Urban JP (2001) 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 26:2543–2549PubMedCrossRefGoogle Scholar
  27. 27.
    Johnson WE, Roberts S (2003) Human intervertebral disc cell morphology and cytoskeletal composition: a preliminary study of regional variations in health and disease. J Anat 203:605–612PubMedCrossRefGoogle Scholar
  28. 28.
    Kalichman L, Hunter DJ (2008) The genetics of intervertebral disc degeneration. Associated genes. Joint Bone Spine 75:388–396PubMedCrossRefGoogle Scholar
  29. 29.
    Kalichman L, Hunter DJ (2008) The genetics of intervertebral disc degeneration. Familial predisposition and heritability estimation. Joint Bone Spine 75:383–387PubMedCrossRefGoogle Scholar
  30. 30.
    Kettler A, Rohlmann F, Neidlinger-Wilke C, Werner K, Claes L, Wilke HJ (2006) Validity and interobserver agreement of a new radiographic grading system for intervertebral disc degeneration. Part II. Cervical spine. Eur Spine J 15:732–741PubMedCrossRefGoogle Scholar
  31. 31.
    Kettler A, Wilke HJ (2006) Review of existing grading systems for cervical or lumbar disc and facet joint degeneration. Eur Spine J 15:705–718PubMedCrossRefGoogle Scholar
  32. 32.
    Kokubo Y, Uchida K, Kobayashi S, Yayama T, Sato R, Nakajima H, Takamura T, Mwaka E, Orwotho N, Bangirana A, Baba H (2008) Herniated and spondylotic intervertebral discs of the human cervical spine: histological and immunohistological findings in 500 en bloc surgical samples. Laboratory investigation. J Neurosurg Spine 9:285–295PubMedCrossRefGoogle Scholar
  33. 33.
    Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174PubMedCrossRefGoogle Scholar
  34. 34.
    Matsumoto M, Okada E, Ichihara D, Watanabe K, Chiba K, Toyama Y, Fujiwara H, Momoshima S, Nishiwaki Y, Hashimoto T, Takahata T (2010) Age-related changes of thoracic and cervical intervertebral discs in asymptomatic subjects. Spine (Phila Pa 1976) 35:1359–1364CrossRefGoogle Scholar
  35. 35.
    Miller JA, Schmatz C, Schultz AB (1988) Lumbar disc degeneration: correlation with age, sex, and spine level in 600 autopsy specimens. Spine (Phila Pa 1976) 13:173–178CrossRefGoogle Scholar
  36. 36.
    Moroney SP, Schultz AB, Miller JA, Andersson GB (1988) Load-displacement properties of lower cervical spine motion segments. J Biomech 21:769–779PubMedCrossRefGoogle Scholar
  37. 37.
    Nachemson A (1975) Towards a better understanding of low-back pain: a review of the mechanics of the lumbar disc. Rheumatol Rehabil 14:129–143PubMedCrossRefGoogle Scholar
  38. 38.
    Nachemson A, Elfstrom G (1970) Intravital dynamic pressure measurements in lumbar discs. A study of common movements, maneuvers and exercises. Scand J Rehabil Med Suppl 1:1–40Google Scholar
  39. 39.
    Nachemson AL, Schultz AB, Berkson MH (1979) Mechanical properties of human lumbar spine motion segments. Influence of age, sex, disc level, and degeneration. Spine (Phila Pa 1976) 4:1–8CrossRefGoogle Scholar
  40. 40.
    Nerlich AG, Boos N, Wiest I, Aebi M (1998) Immunolocalization of major interstitial collagen types in human lumbar intervertebral discs of various ages. Virch Arch 432:67–76CrossRefGoogle Scholar
  41. 41.
    Nerlich AG, Schleicher ED, Boos N (1997) 1997 Volvo Award winner in basic science studies. Immunohistologic markers for age-related changes of human lumbar intervertebral discs. Spine 22:2781–2795PubMedCrossRefGoogle Scholar
  42. 42.
    Nerlich AG, Weiler C, Zipperer J, Narozny M, Boos N (2002) Immunolocalization of phagocytic cells in normal and degenerated intervertebral discs. Spine 27:2484–2490PubMedCrossRefGoogle Scholar
  43. 43.
    Okada E, Matsumoto M, Ichihara D, Chiba K, Toyama Y, Fujiwara H, Momoshima S, Nishiwaki Y, Hashimoto T, Ogawa J, Watanabe M, Takahata T (2009) Aging of the cervical spine in healthy volunteers: a 10-year longitudinal magnetic resonance imaging study. Spine (Phila Pa 1976) 34:706–712CrossRefGoogle Scholar
  44. 44.
    Petren-Mallmin M, Linder J (2001) Cervical spine degeneration in fighter pilots and controls: a 5-yr follow-up study. Aviat Space Environ Med 72:443–446PubMedGoogle Scholar
  45. 45.
    Pluijm SM, van Essen HW, Bravenboer N, Uitterlinden AG, Smit JH, Pols HA, Lips P (2004) Collagen type I alpha1 Sp1 polymorphism, osteoporosis, and intervertebral disc degeneration in older men and women. Ann Rheum Dis 63:71–77PubMedCrossRefGoogle Scholar
  46. 46.
    Quint U, Wilke HJ (2008) Grading of degenerative disk disease and functional impairment: imaging versus patho-anatomical findings. Eur Spine J 17:1705–1713PubMedCrossRefGoogle Scholar
  47. 47.
    Roberts S, Evans EH, Kletsas D, Jaffray DC, Eisenstein SM (2006) Senescence in human intervertebral discs. Eur Spine J 15(Suppl 3):S312–316Google Scholar
  48. 48.
    Roberts S, Evans H, Trivedi J, Menage J (2006) Histology and pathology of the human intervertebral disc. J Bone Joint Surg Am 88(Suppl 2):10–14PubMedCrossRefGoogle Scholar
  49. 49.
    Ross JS, Perez-Reyes N, Masaryk TJ, Bohlman H, Modic MT (1987) Thoracic disk herniation: MR imaging. Radiology 165:511–515PubMedGoogle Scholar
  50. 50.
    Roughley PJ (2004) Biology of intervertebral disc aging and degeneration: involvement of the extracellular matrix. Spine 29:2691–2699PubMedCrossRefGoogle Scholar
  51. 51.
    Shirazi-Adl A, Taheri M, Urban JP (2010) Analysis of cell viability in intervertebral disc: effect of endplate permeability on cell population. J Biomech 43:1330–1336PubMedCrossRefGoogle Scholar
  52. 52.
    Siivola SM, Levoska S, Tervonen O, Ilkko E, Vanharanta H, Keinanen-Kiukaanniemi S (2002) MRI changes of cervical spine in asymptomatic and symptomatic young adults. Eur Spine J 11:358–363PubMedCrossRefGoogle Scholar
  53. 53.
    Sohn HM, You JW, Lee JY (2004) The relationship between disc degeneration and morphologic changes in the intervertebral foramen of the cervical spine: a cadaveric MRI and CT study. J Korean Med Sci 19:101–106PubMedCrossRefGoogle Scholar
  54. 54.
    Thompson JP, Pearce RH, Schechter MT, Adams ME, Tsang IK, Bishop PB (1990) Preliminary evaluation of a scheme for grading the gross morphology of the human intervertebral disc. Spine 15:411–415PubMedCrossRefGoogle Scholar
  55. 55.
    Trout JJ, Buckwalter JA, Moore KC (1982) Ultrastructure of the human intervertebral disc: II. cells of the nucleus pulposus. Anat Rec 204:307–314PubMedCrossRefGoogle Scholar
  56. 56.
    Trout JJ, Buckwalter JA, Moore KC, Landas SK (1982) Ultrastructure of the human intervertebral disc. I. Changes in notochordal cells with age. Tissue Cell 14:359–369PubMedCrossRefGoogle Scholar
  57. 57.
    Urban JP, Roberts S (2003) Degeneration of the intervertebral disc. Arthritis Res 5:120–130Google Scholar
  58. 58.
    Urban JP, Smith S, Fairbank JC (2004) Nutrition of the intervertebral disc. Spine 29:2700–2709PubMedCrossRefGoogle Scholar
  59. 59.
    Vanichkachorn JS, Vaccaro AR (2000) Thoracic disk disease: diagnosis and treatment. J Am Acad Orthop Surg 8:159–169PubMedGoogle Scholar
  60. 60.
    Videman T, Battie MC, Parent E, Gibbons LE, Vainio P, Kaprio J (2008) Progression and determinants of quantitative magnetic resonance imaging measures of lumbar disc degeneration: a five-year follow-up of adult male monozygotic twins. Spine 33:1484–1490PubMedCrossRefGoogle Scholar
  61. 61.
    Videman T, Saarela J, Kaprio J, Nakki A, Levalahti E, Gill K, Peltonen L, Battie MC (2009) Associations of 25 structural, degradative, and inflammatory candidate genes with lumbar disc desiccation, bulging, and height narrowing. Arthritis Rheum 60:470–481PubMedCrossRefGoogle Scholar
  62. 62.
    Viikari-Juntura E, Raininko R, Videman T, Porkka L (1989) Evaluation of cervical disc degeneration with ultralow field MRI and discography. An experimental study on cadavers. Spine (Phila Pa 1976) 14:616–619CrossRefGoogle Scholar
  63. 63.
    Walraevens J, Liu B, Meersschaert J, Demaerel P, Delye H, Depreitere B, Vander SJ, Goffin J (2009) Qualitative and quantitative assessment of degeneration of cervical intervertebral discs and facet joints. Eur Spine J 18:358–369PubMedCrossRefGoogle Scholar
  64. 64.
    Weiler C, Nerlich AG, Zipperer J, Bachmeier BE, Boos N (2002) 2002 SSE Award Competition in Basic Science: expression of major matrix metalloproteinases is associated with intervertebral disc degradation and resorption. Eur Spine J 11:308–320PubMedCrossRefGoogle Scholar
  65. 65.
    Wilke HJ, Rohlmann F, Neidlinger-Wilke C, Werner K, Claes L, Kettler A (2006) Validity and interobserver agreement of a new radiographic grading system for intervertebral disc degeneration. Part I. Lumbar spine. Eur Spine J 15:720–730PubMedCrossRefGoogle Scholar
  66. 66.
    Wood KB, Schellhas KP, Garvey TA, Aeppli D (1999) Thoracic discography in healthy individuals. A controlled prospective study of magnetic resonance imaging and discography in asymptomatic and symptomatic individuals. Spine 24:1548–1555PubMedCrossRefGoogle Scholar
  67. 67.
    Zhao CQ, Wang LM, Jiang LS, Dai LY (2007) The cell biology of intervertebral disc aging and degeneration. Ageing Res Rev 6:247–261PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • C. Weiler
    • 1
  • M. Schietzsch
    • 1
  • T. Kirchner
    • 1
  • A. G. Nerlich
    • 2
  • N. Boos
    • 3
    • 4
  • K. Wuertz
    • 3
    • 4
  1. 1.Institute of PathologyUniversity of MunichMunichGermany
  2. 2.Institute of PathologyAcademic Clinic Munich-BogenhausenMunichGermany
  3. 3.Spine Research Group, Competence Center for Applied Biotechnology and Molecular Medicine (CABMM)University of ZurichZurichSwitzerland
  4. 4.AOSpine Research NetworkDuebendorfSwitzerland

Personalised recommendations