Archives of Orthopaedic and Trauma Surgery

, Volume 115, Issue 5, pp 262–269 | Cite as

Architecture and distribution of cancellous bone yield vertebral fracture clues

A histomorphometric analysis of the complete spinal column from 40 autopsy specimens
  • M. Amling
  • M. Pösl
  • H. Ritzel
  • M. Hahn
  • M. Vogel
  • V. J. Wening
  • G. Delling
Original Article
Received:

Abstract

The objective of this study was to analyze the structure of cancellous bone and its significance for vertebral fractures. Therefore, the complete spinal column from 40 autopsy cases (18 without diseases affecting the skeleton and 12 osteoporotic) was removed and sectioned in the sagittal plane to a thickness of 1 mm. A surface-stained block grinding technique allowed combined two- and three-dimensional histomorphometric analysis, which included an evaluation of the trabecular bone volume (BV/TV in %) and the trabecular interconnection (TBPf, in mm). In addition, qualitative investigation of the structure of trabecular bone was done. The distribution of trabecular bone volume within the spinal column of a normal skeleton shows a curve, with the highest values in the cervical spine and a decline in the thoracic and lumbar spine. Osteoporosis presents itself with a pathologically diminished trabecular bone volume, whereas the distribution within the spine is comparable to that of the controls. Osteoporotic patients show an apparently reduced trabecular interconnection. It is important that the measured values for TBPf are not only in general higher, but also more widely dispersed. The age-related decrease of trabecular bone mass is due to the transformation from plates to rods. This is quantitatively indicated by the close correlation of BV/TV and TBPf (P < 0.001, r = 0.85). The bone loss in osteoporosis is a loss of structure and a loss of whole trabeculae, which is caused by perforations. It involves a gradual change from normal bone. However, the polyostic heterogenity in osteoporosis is immense. These structural differences demonstrate the development of regions of least resistance within the spine, serving as an explanation of osteoporotic fractures. Due to the polyostotic heterogeneity it is impossible to define a threshold mineral content for crash fractures by diagnostic measurements at any reference site.

Keywords

Osteoporosis Perforation Vertebral Fracture Cervical Spine Trabecular Bone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Amling M, Grote HJ, Pösl M, Hahn M, Delling G (1994) Polyostotic heterogeneity of the spine in osteoporosis. Quantitative analysis and three-dimensional morphology. Bone Miner 27:193–208Google Scholar
  2. 2.
    Amling M, Grote HJ, Vogel M, Hahn M, Delling G (1994) Three-dimensional analysis of the spine in autopsy cases with renal osteodystrophy. Kidney Int 46:733–743Google Scholar
  3. 3.
    Amling M, Hahn M, Wening V, Grote HJ, Delling G (1994) The microarchitecture of the axis as the predisposing factor for fracture of the base of the odontoid process. J Bone Joint Surg [Am] 76:1840–1846Google Scholar
  4. 4.
    Baker SP, Harvey AH (1985) Fall injuries in the elderly: symposium on falls in the elderly: biological aspects and behavioral aspects. Clin Geriatr Med 1:501–508Google Scholar
  5. 5.
    Birkenhager-Frenkel DH, Courpron P, Hüpscher EA, Clermonts E, Coutinho MF, Schmitz PIM, Meunier PJ (1988) Age-related changes in cancellous bone structure. A two-dimensional study in the transiliac and iliac crest biopsy sites. Bone Miner 4:197–216Google Scholar
  6. 6.
    Bordier P, Matrajt H, Miravet L, Hioco D (1964) Measure histologique de la mass et de la resorption des travées osseous. Pathol Biol (Paris) 12:1238–1243Google Scholar
  7. 7.
    Burr DB, Martin RB, Schaffler MB, Radin EL (1985) Bone remodeling in response to in vivo fatique microdamage. J Biomech 18:189–200Google Scholar
  8. 8.
    Chappard D, Alexandre C, Riffat G (1988) Spatial distribution of trabeculae in iliac bone from 145 osteoporotic females. Acta Anat (Basel) 132:137–142Google Scholar
  9. 9.
    Chrischilles E, Shireman T, Wallace R (1994) Costs and health effects of osteoporotic fractures. Bone 15:377–386Google Scholar
  10. 10.
    Compston JE (1994) Connectivity of cancellous bone: assessment and mechanical implications. Bone 15:463–466Google Scholar
  11. 11.
    Compston JE, Mellish RWE, Garrahan NJ (1987) Age-related changes in the iliac crest trabecular microanatomic bone structure in man. Bone 8:289–292Google Scholar
  12. 12.
    Compston JE, Mellish RWE, Croucher P, Newcombe R, Garrahan NJ (1989) Structural mechanisms of trabecular bone loss in man. Bone Miner 6:339–350Google Scholar
  13. 13.
    De Hoff RT, Aigeltinger EH, Craig KR (1972) Experimental determination of the topological properties of three-dimensional microstructures. J Microsc 95:69Google Scholar
  14. 14.
    De Smet AA, Robinson RG, Johnson BE, Lukert BP (1988) Spinal compression fractures in osteoporotic women: patterns and relationship to hyperkyphosis. Radiology 166:497–500Google Scholar
  15. 15.
    Delling G, Amling M (1994) Darstellung der dreidimensionalen Spongiosastruktur in der Wirbelsäule bei renaler Osteopathie nach chronischer Hämodialyse. Pathologe 1:15–21Google Scholar
  16. 16.
    Delling G, Amling M (1995) Biomechanical stability of the skeleton — it is not only bone mass, but also bone structure that counts. Nephrol Dial Transplant 10:601–606Google Scholar
  17. 17.
    Feldkamp LA, Goldstein SA, Parfitt AM, Jesion G, Kleerekoper M (1989) The direct examination of three-dimensional bone architecture in vitro by computed tomography. Bone 4:3–11Google Scholar
  18. 18.
    Frost HM (1981) Clinical management of the symptomatic osteoporotic patient. Orthop Clin North Am 12:671–681Google Scholar
  19. 19.
    Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Möller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sörensen FB, Vesterby A, West MJ (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 96:379–394Google Scholar
  20. 20.
    Gundersen HJG, Boyce RW, Nyengaard JR, Odgaard A (1993) The conneulor: unbiased estimation of connectivity using physical directors under projection. Bone 14:217–222Google Scholar
  21. 21.
    Hahn M, Vogel M, Delling G (1991) Undecalcified preparation of bone tissue: report of technical experience and development of new methods. Virchows Arch [A] 418:1–7Google Scholar
  22. 22.
    Hahn M, Vogel M, Pompesius-Kempa M, Delling G (1992) Trabecular bone pattern factor — a new parameter for simple quantification of bone microarchitecture. Bone 13:327–330Google Scholar
  23. 23.
    Hahn M, Vogel M, Amling M, Grote HJ, Pösl M, Werner M, Delling G (1994) Mikrokallusformationen der Spongiosa. Pathologe 15:297–302Google Scholar
  24. 24.
    Hansson T, Roos B (1981) Microcalluses of the trabeculae in lumbar vertebrae and their relation to the bone mineral content. Spine 6:375–380Google Scholar
  25. 25.
    Harrison JE, Patt N, Müller C, Bayley TA, Budden FH, Josse RG, Murray IM, Sturtridge WC, Srauss A, Goodwin S (1990) Bone mineral mass associated with postmenopausal vertebral deformities. Bone Miner 10:243–251Google Scholar
  26. 26.
    Horne WC, Neff L, Lomri A, Levy JB, Baron R (1992) Osteoclasts express high levels of pp60c-src in association with intracellular membranes. J Cell Biol 119:1003–1013Google Scholar
  27. 27.
    Home WC, Levy JB, Baron R (1993) Proto-oncogenes and osteoclast function. Ital J Miner Electrolyte Metab 7:185–197Google Scholar
  28. 28.
    Jacquet G, Ohley WJ, Mont MA, Siffert R, Schmukler R (1990) Measurement of bone structure by fractal dimensions. Proc Ann Conf IEEE/EMBS 12:1402–1403Google Scholar
  29. 29.
    Kimmel DB, Heaney RP, Avioli LV, Chesnut CH, Recker RR, Lappe JM, Brandenburger GH (1991) Patellar ultrasound velocity in osteoporotic and normal subjects of equal forearm or spinal bone density (Abstract). J Bone Miner Res 6 [Suppl 1]:175Google Scholar
  30. 30.
    Kleerekoper M, Villanueva AR, Stanciu D, Sudhaker Rao D, Parfitt AM (1985) The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tissue Int 37:594–597Google Scholar
  31. 31.
    Mandelbrot BB (1977) Fractals: form, change and dimension. W. H. Freeman, San FranciscoGoogle Scholar
  32. 32.
    Mautalen C, Vega E, Ghiringhelli G, Fromm G (1990) Bone diminution of osteoporotic females at different skeletal sites. Calcif Tissue Int 46:217–221Google Scholar
  33. 33.
    Mellish RWE, Ferguson-Pell MW, Cochran GVB, Lindsay R, Dempster DW (1991) A new manual method for assessing two-dimensional cancellous bone structure: comparison between iliac crest and lumbar vertebra. J Bone Miner Res 6:689–696Google Scholar
  34. 34.
    Melton LJ III, Riggs BL (1985) Risk factors for injury after a fall: symposium on falls in the elderly: biological and behavioral aspects. Clin Geriatr Med 1:1–15Google Scholar
  35. 35.
    Mosekilde L (1988) Age-related changes in vertebral trabecular bone architecture. Assessed by a new method. Bone 9:247–250Google Scholar
  36. 36.
    Mosekilde L (1988) Iliac crest trabecular bone volume as predictor for vertebral compressive strength, ash density and trabecular bone volume in normal individuals. Bone 9:195–199Google Scholar
  37. 37.
    Mosekilde L (1989) Sex differences in age-related loss of vertebral trabecular bone mass and structure. Biomechanical consequences. Bone 10:425–432Google Scholar
  38. 38.
    Mosekilde L (1990) Consequences of remodelling process for vertebral trabecular bone structure: a scanning electron microscopy study (uncoupling of unloaded structures). Bone Miner 10:13–35Google Scholar
  39. 39.
    Odgaard A, Gundersen HJG (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14:173–182Google Scholar
  40. 40.
    Odgaard A, Andersen K, Melsen F, Gundersen HJG (1990) A direct method for fast three-dimensional serial reconstruction. J Microsc 159:335–342Google Scholar
  41. 41.
    Parfitt AM (1979) Quantum concept of bone remodeling and turnover: implications for the pathogenesis of osteoporosis. Calcif. Tissue Int 28:1–5Google Scholar
  42. 42.
    Parfitt AM (1987) Trabecular bone architecture in the pathogenesis and prevention of fracture. Am J Med 82 [Suppl 1B]:68–72Google Scholar
  43. 43.
    Parfitt AM (1988) Bone remodeling: relationship to the amount and structure of bone, and the pathogenesis and prevention of fractures. In: Riggs L, Melton LJ (eds) Osteoporosis: etiology, diagnosis and management. Raven Press, New York, pp 45–93Google Scholar
  44. 44.
    Parfitt AM (1988) Bone histomorphometry: standardization of nomenclature, symbols and units. Summary of proposed system. Bone Miner 4:1–5Google Scholar
  45. 45.
    Parfitt AM (1992) Implications of architecture for the pathogenesis and prevention of vertebral fracture. Bone 13:S41-S47Google Scholar
  46. 46.
    Parfitt AM, Mathews CHE, Villanueva AR, Kleerekoper M (1983) Relationships between surface, volume and thickness of iliac trabecular bone in ages and in osteoporosis. J Clin Invest 72:1396–1409Google Scholar
  47. 47.
    Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche HH, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res 2:595–610Google Scholar
  48. 48.
    Riggs BL, Melton LJ III (1986) Involutional osteoporosis. N Engl J Med 314:1676–1686Google Scholar
  49. 49.
    Riggs BL, Wahner HW, Seeman E, Offord KP, Dunn WL, Mazess RB, Johnson KA, Melton LJ III (1982) Changes in bone mineral density of the proximal femur and spine with aging: differences between the postmenopausal and senile osteoporosis syndrom. J Clin Invest 70:716–723Google Scholar
  50. 50.
    Ross PD, Davis JW, Vogel JM, Wasnich RD (1990) A critical review of bone mass and the risk of fractures in osteoporosis. Calcif Tissue Int 46:149–161Google Scholar
  51. 51.
    Scott WW (1994) Osteoporosis-related fracture syndromes. In: Osteoporosis. Proceedings of the NIH Consensus Development Conference, Bethesda Maryland, pp 20–24Google Scholar
  52. 52.
    Tanaka S, Takahashi N, Udagawa N, Sasaki T, Fukui Y, Kurokawa T, Suda T (1990) Osteoclasts express high levels of p60c-src, preferentially on ruffled border membranes. FEBS Lett 313:85–89Google Scholar
  53. 53.
    Vernon-Roberts B, Pirie CJ (1973) Healing trabecular microfractures in the bodies of lumbar vertebrae. Ann Rheum Dis 32:406–412Google Scholar
  54. 54.
    Vesterby A, Mosekilde L, Gundersen HJG, Melsen F, Holme K, Sorensen S (1991) Biomechanically meaningful determinants of the in vitro strength of lumbar vertebrae. Bone 12:219–224Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • M. Amling
    • 1
  • M. Pösl
    • 1
  • H. Ritzel
    • 1
  • M. Hahn
    • 1
  • M. Vogel
    • 2
  • V. J. Wening
    • 3
  • G. Delling
    • 1
  1. 1.Department of Bone Pathology, Institute of Pathology, Center for Biomechanics UKEUniversity of HamburgHamburgGermany
  2. 2.Department of Orthopedics, Center for Biomechanics UKEUniversity of HamburgHamburgGermany
  3. 3.Department of Trauma Surgery, Center for Biomechanics UKEUniversity of HamburgHamburgGermany

Personalised recommendations