Skip to main content
SpringerLink
Log in

Trabecular Shear Stresses Predict In Vivo Linear Microcrack Density but not Diffuse Damage in Human Vertebral Cancellous Bone

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Linear microcracks and diffuse damage (staining over a broad region) are two types of microscopic damage known to occur in vivo in human vertebral trabecular bone. These damage types might be associated with vertebral failure. Using microcomputed tomography and finite element analysis for specimens of cancellous bone, we estimated the stresses in the trabeculae of human vertebral tissue for inferosuperior loading. Microdamage was quantified histologically. The density of in vivo linear microcracks was, but the diffuse damage area was not, related to the estimates of von Mises stress distribution in the tissue. In vivo linear microcrack density increased with increasing coefficient of variation of the trabecular von Mises stress and with increasing average trabecular von Mises stress generated per superoinferior apparent axial stress. Nonlinear increase in linear crack density, similar to the increase of the coefficient of variation of trabecular shear stresses, with decreasing bone stiffness and bone volume fraction suggests that damage may accumulate rather rapidly in diseases associated with low bone density due to the dramatic increase of shear stresses in the tissue. © 2003 Biomedical Engineering Society.

PAC2003: 8719Rr, 8719Xx, 8759Ls, 8759Fm, 8710+e

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Burr, D. B., M. R. Forwood, D. P. Fyhrie, R. B. Martin, M. B. Schaffler, and C. H. Turner. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J. Bone Miner. Res.12:6–15, 1997.

    Google Scholar 

  2. Burr, D. B., C. H. Turner, P. Naick, M. R. Forwood, W. Ambrosius, M. S. Hasan, and R. Pidaparti. Does microdamage accumulation affect the mechanical properties of bone. J. Biomech.31:337–345, 1998.

    Google Scholar 

  3. Norman, T. L., Y. N. Yeni, C. U. Brown, and Z. Wang. Influence of microdamage on fracture toughness of the human femur and tibia. Bone23:303–306, 1998.

    Google Scholar 

  4. Hoshaw, S. J., D. D. Cody, A. M. Saad, and D. P. Fyhrie. Decrease in canine proximal femoral ultimate strength and stiffness due to fatigue damage. J. Biomech.30:323–329, 1997.

    Google Scholar 

  5. Boyce, T. M., D. P. Fyhrie, M. C. Glotkowski, E. L. Radin, and M. B. Schaffler. Damage type and strain mode associations in human compact bone bending fatigue. J. Orthop. Res.16:322–329, 1998.

    Google Scholar 

  6. Burr, D. B., R. B. Martin, M. B. Schaffler, and E. L. Radin. Bone remodeling in response to fatigue microdamage. J. Biomech.18:189–200, 1985.

    Google Scholar 

  7. Verborgt, O., G. J. Gibson, and M. B. Schaffler. Loss of osteocyte integrity in association with microdamage and bone remodeling after fatigue. J. Bone Miner. Res.15:60–67, 2000.

    Google Scholar 

  8. Martin, B.Mathematical model for repair of fatigue damage and stress fracture in osteonal bone. J. Orthop. Res.13:309–316, 1995.

    Google Scholar 

  9. Frost, H. M.Presence of microscopic cracks in bone. Henry Ford Hosp. Bull.8:25–35, 1960.

    Google Scholar 

  10. Fazzalari, N. L., M. R. Forwood, B. A. Manthey, K. Smith, and P. Kolesik. Three-dimensional confocal images of microdamage in cancellous bone. Bone23:373–378, 1998.

    Google Scholar 

  11. Bentolila, V., T. M. Boyce, D. P. Fyhrie, R. Drumb, T. M. Skerry, and M. B. Schaffler. Intracortical remodeling in adult rat long bones after fatigue loading. Bone23:275–281, 1998.

    Google Scholar 

  12. Fazzalari, N. L., M. R. Forwood, K. Smith, B. A. Mathey, and P. Herreen. Assessment of cancellous bone quality in severe osteoarthrosis: Bone mineral density, mechanics, and microdamage. Bone22:381–388, 1998.

    Google Scholar 

  13. Zioupos, P.Accumulation of fatigue microdamage and its relation to biomechanical properties in aging human cortical bone. J. Microsc.201:270–278, 2001.

    Google Scholar 

  14. Norman, T., and T. Little. The incidence and role of diffuse damage in human cortical bone. Proceedings of the 48th Annual Meeting, Orthopaedic Research Society, Dallas, TX, 10–13 February 2002, p. 0545.

    Google Scholar 

  15. Parsamian, G. P., and T. L. Norman. Diffuse damage accumulation in the fracture process zone of human cortical bone specimens and its influence on fracture toughness. J. Mater. Sci.: Mater. Med.12:779–783, 2001.

    Google Scholar 

  16. Carter, D. R., and W. C. Hayes. Compact bone fatigue damage. I. Residual strength and stiffness. J. Biomech.10:325–337, 1977.

    Google Scholar 

  17. Keaveny, T. M., E. F. Wachtel, X. E. Guo, and W. C. Hayes. Mechanical behavior of damaged trabecular bone. J. Biomech.27:1309–1318, 1994.

    Google Scholar 

  18. Keaveny, T. M., E. F. Wachtel, and D. L. Kopperdahl. Mechanical behavior of human trabecular bone after overloading. J. Orthop. Res.17:346–353, 1999.

    Google Scholar 

  19. Reilly, G. C., and J. D. Currey. The effects of damage and microcracking on the impact strength of bone. J. Biomech.33:337–343, 2000.

    Google Scholar 

  20. Yeni, Y. N., and D. P. Fyhrie. Fatigue damage-fracture mechanics interaction in cortical bone. Bone30:509–514, 2002.

    Google Scholar 

  21. Fondrk, M., E. Bahniuk, D. T. Davy, and C. Michaels. Some viscoplastic characteristics of bovine and human cortical bone. J. Biomech.21:623–630, 1988.

    Google Scholar 

  22. Jepsen, K. J., and D. T. Davy. Comparison of damage accumulation measures in human cortical bone. J. Biomech.30:891–894, 1997.

    Google Scholar 

  23. Wenzel, T. E., M. B. Schaffler, and D. P. Fyhrie. microcracks in human vertebral trabecular bone. Bone19:89–95, 1996.

    Google Scholar 

  24. Vashishth, D., J. Koontz, S. J. Qiu, D. Lundin-Cannon, Y. N. Yeni, M. B. Schaffler, and D. P. Fyhrie. diffuse damage in human vertebral cancellous bone. Bone26:147–152, 2000.

    Google Scholar 

  25. Fyhrie, D. P., S. J. Hoshaw, M. S. Hamid, and F. J. Hou. Shear stress distribution in the trabeculae of human vertebral bone. Ann. Biomed. Eng.28:1194–1199, 2000.

    Google Scholar 

  26. Fyhrie, D. P., and M. B. Schaffler. Failure mechanisms in human vertebral cancellous bone. Bone15:105–109, 1994.

    Google Scholar 

  27. Moore, T. L. A., and L. J. Gibson. Microdamage accumulation in bovine trabecular bone in uniaxial compression. J. Biomech. Eng.124:63–71, 2002.

    Google Scholar 

  28. Hou, F. J., S. M. Lang, S. J. Hoshaw, D. A. Reimann, and D. P. Fyhrie. Human vertebral body apparent and hard tissue stiffness. J. Biomech.31:1009–1015, 1998.

    Google Scholar 

  29. Ladd, A. J., J. H. Kinney, D. L. Haupt, and S. A. Goldstein. Finite-element modeling of trabecular bone: Comparison with mechanical testing and determination of tissue modulus. J. Orthop. Res.16:622–628, 1998.

    Google Scholar 

  30. Yeni, Y. N., F. J. Hou, D. Vashishth, and D. P. Fyhrie. Trabecular shear stress in human vertebral cancellous bone: Intra-and interindividual variations. J. Biomech.34:1341–1346, 2001.

    Google Scholar 

  31. Ulrich, D., T. Hildebrand, B. Van Rietbergen, R. Muller, and P. Ruegsegger. The quality of trabecular bone evaluated with micro-computed tomography, fea and mechanical testing. Stud. Health Technol. Inform.40:97–112, 1997.

    Google Scholar 

  32. Bury, K. Statistical Distributions in Engineering. Cambridge, U.K.: Cambridge University Press, 1999.

    Google Scholar 

  33. Malvern, L. E. Introduction to the Mechanics of a Continuous Medium. Englewood Cliffs, NJ: Prentice-Hall, 1969.

    Google Scholar 

  34. Fyhrie, D. P., and D. Vashishth. Bone stiffness predicts strength similarly for human vertebral cancellous bone in compression and for cortical bone in tension. Bone26:169–173, 2000.

    Google Scholar 

  35. Yeni, Y. N., and D. P. Fyhrie. Finite element predicted apparent stiffness is a consistent predictor of apparent strength in human cancellous bone tested with different boundary conditions. J. Biomech.34:1649–1654, 2001.

    Google Scholar 

  36. Yeni, Y. N., and D. P. Fyhrie. Viscoelastic microcrack-bridging can explain the strain rate dependency of cortical bone apparent strength. Proceedings of the 48th Annual Meeting, Orthopaedic Research Society, Dallas, TX, 10–13 February 2002, p. 0018.

    Google Scholar 

  37. Rubin, C. T., and L. E. Lanyon. Regulation of bone mass by mechanical strain magnitude. Calcif. Tissue Int.37:411–417, 1985.

    Google Scholar 

  38. Mosley, J. R., and L. E. Lanyon. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone23:313–318, 1998.

    Google Scholar 

  39. Knothe Tate, M. L., U. Knothe, and P. Niederer. Experimental elucidation of mechanical load-induced fluid flow and its potential role in bone metabolism and functional adaptation. Am. J. Med. Sci.316:189–195, 1998.

    Google Scholar 

  40. Tate, M. L., P. Niederer, and U. Knothe. tracer transport through the lacunocanalicular system of rat bone in an environment devoid of mechanical loading. Bone22:107–117, 1998.

    Google Scholar 

  41. Dodd, J. S., J. A. Raleigh, and T. S. Gross. Osteocyte hypoxia: A novel mechanotransduction pathway. Am. J. Physiol.277:C598–C602, 1999.

    Google Scholar 

  42. Gross, T. S., N. Akeno, T. L. Clemens, S. Komarova, S. Srinivasan, D. A. Weimer, and S. Mayorov. Selected contribution: Osteocytes upregulate hif-1alpha in response to acute disuse and oxygen deprivation. J. Appl. Physiol.90:2514–2519, 2001.

    Google Scholar 

  43. Porter, B. D., R. Zauel, S. H. Cartmell, D. Fyhrie, R. E. Guldberg, and H. W. Stockman. Three-dimensional computational modeling of media flow through scaffolds in a perfusion bioreactor. Proceedings of the 49th Annual Meeting, Orthopaedic Research Society, New Orleans, LA, 2–5 February 2003, p. 0274.

    Google Scholar 

  44. Ciarelli, T. E., D. P. Fyhrie, H. W. Stockman, and R. Zauel. Simulation of pressure driven flow through anatomically accurate canalicular systems of cortical bone. Proceedings of the 49th Annual Meeting, Orthopaedic Research Society, New Orleans, LA, 2–5 February 2003.

    Google Scholar 

  45. Tami, A. E., P. Nasser, O. Verborgt, M. B. Schaffler, and M. L. Knothe Tate. The role of interstitial fluid flow in the remodeling response to fatigue loading. J. Bone Miner. Res.17:2030–2037, 2002.

    Google Scholar 

  46. Choi, K., D. P. Fyhrie, and M. B. Schaffler. Failure mechanisms of compact bone in bending: A microstructural analysis. Proceedings of the 40th Annual Meeting, Orthopaedic Research Society, New Orleans, LA, p. 425.

  47. Charras, G. T., and R. E. Guldberg. Improving the local solution accuracy of large-scale digital image based finite lement analyses. J. Biomech.33:255–259, 2000.

    Google Scholar 

  48. Guldberg, R. E., S. J. Hollister, and G. T. Charras. The accuracy of digital image-based finite element models. J. Biomech. Eng.120:289–295, 1998.

    Google Scholar 

  49. Niebur, G. L., J. C. Yuen, A. C. Hsia, and T. M. Keaveny. Convergence behavior of high-resolution finite element models of trabecular bone. J. Biomech. Eng.121:629–635, 1999.

    Google Scholar 

  50. van Rietbergen, B., H. Weinans, R. Huiskes, and A. Odgaard. A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. J. Biomech.28:69–81, 1995.

    Google Scholar 

  51. Jacobs, C. R., B. R. Davis, C. J. Rieger, J. J. Francis, M. Saad, and D. P. Fyhrie. Nacob presentation to asb young scientist award: Postdoctoral. The impact of boundary conditions and mesh size on the accuracy of cancellous bone tissue modulus determination using large-scale finite-element modeling. North American congress on biomechanics. J. Biomech.32:1159–1164, 1999.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Bone and Joint Center, Department of Orthopaedic Surgery, Henry Ford Hospital, 2799 West Grand Boulevard, Detroit, MI

    Yener N. Yeni, Traci Ciarelli & David P. Fyhrie

  2. Shell International Exploration and Production, Inc., Bellaire Technology Center, 3737 Bellaire Boulevard, Houston, TX

    Fu J. Hou

  3. Department of Biomedical Engineering, Room 7046, Rensselaer Polytechnic Institute, 110 8th Street, Troy, NY

    Deepak Vashishth

Authors
  1. Yener N. Yeni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fu J. Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Traci Ciarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deepak Vashishth
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David P. Fyhrie
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yeni, Y.N., Hou, F.J., Ciarelli, T. et al. Trabecular Shear Stresses Predict In Vivo Linear Microcrack Density but not Diffuse Damage in Human Vertebral Cancellous Bone. Annals of Biomedical Engineering 31, 726–732 (2003). https://doi.org/10.1114/1.1569264

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1114/1.1569264

Search

Navigation