Effects of Aging on the Toughness of Human Cortical Bone: A Study from Nano to Macro Size-Scales

Abstract

Age-related deterioration of both the fracture properties and the architecture of bone, coupled with increased life expectancy, are factors leading to the increasing incidence of bone fracture in the elderly. In order to facilitate the development of treatments which counter this increased fracture risk, a thorough understanding of how fracture properties degrade with age is required. The present study describes ex vivo fracture experiments to quantitatively assess the effects of aging on the fracture toughness of human cortical bone in the longitudinal direction. Because cortical bone exhibits rising crack-growth resistance with crack extension, we depart from most previous studies by evaluating the toughness in terms of resistance-curve (R-curve) behavior, measured for bone taken from donors 34 to 99 years old. Using this approach, both the crack-initiation and crack-growth toughness are determined and are found to deteriorate with age; the initiation toughness decreases ~40% from 40 to 100 years, while the growth toughness is effectively eliminated over the same age range. Evidence from x-ray synchrotron tomography is provided to support the hypothesis that the reduction in crack-growth toughness is associated primarily with a degradation in the degree of extrinsic toughening, in particular involving crack bridging at the microstructural level in the wake of the crack. Atomic force microscope-based nanoidentation of individual collagen fibers revealed changes at the collagen fibrillar level and deep-ultraviolet Raman spectroscopy showed that the cross-linking at the nanostructural level also changes with age. These results should provide for a better mechanistic understanding of the increased propensity for bone fracture with age.

This is a preview of subscription content, access via your institution.

References

  1. 1.

    R. Heaney, Bone 33, 457 (2003).

    Article  Google Scholar 

  2. 2.

    W. Bonfield, J. Biomech. 20, 1071 (1987).

    CAS  Article  Google Scholar 

  3. 3.

    J. D. Currey, K. Brear and P. Zioupos, J. Biomech. 29, 257 (1996).

    CAS  Article  Google Scholar 

  4. 4.

    Y. N. Yeni, C. U. Brown, Z. Wang and T. L. Norman, Bone 21, 453 (1997).

    CAS  Article  Google Scholar 

  5. 5.

    X. Wang, X. Shen, X. Li and C. M. Agrawal, Bone 31, 1 (2002).

    Article  Google Scholar 

  6. 6.

    D. Vashishth, J. C. Behiri and W. Bonfield, J. Biomech. 30, 763 (1997).

    CAS  Article  Google Scholar 

  7. 7.

    C. L. Malik, S. M. Stover, R. B. Martin and J. C. Gibeling, J. Biomech. 36, 191 (2003).

    CAS  Article  Google Scholar 

  8. 8.

    G. Pezzotti and S. Sakakura, J. Biomech. 65A, 229 (2003).

    CAS  Google Scholar 

  9. 9.

    R. K. Nalla, J. J. Kruzic and R. O. Ritchie, Bone 34, 790 (2004).

    CAS  Article  Google Scholar 

  10. 10.

    R. K. Nalla, J. J. Kruzic, J. H. Kinney and R. O. Ritchie, Biomater. 26, 217 (2005).

    CAS  Article  Google Scholar 

  11. 11.

    J. F. Knott, Fundamentals of fracture mechanics (Butterworth & Co., 1976).

    Google Scholar 

  12. 12.

    R. O. Ritchie, Mater. Sci. Eng. 103, 15 (1988).

    Article  Google Scholar 

  13. 13.

    A. G. Evans, J. Am. Ceramic Soc. 73, 187 (1990).

    CAS  Article  Google Scholar 

  14. 14.

    J-Y. Rho, L. Kuhn-Spearing and P. Zioupos, Med. Eng. Physics 20, 92 (1998).

    CAS  Article  Google Scholar 

  15. 15.

    J. H. Kinney and M. C. Nichols, Annu. Rev. Mater. Sci. 22, 121 (1992).

    CAS  Article  Google Scholar 

  16. 16.

    G. M. Pharr, W. C. Oliver and F. R. Brotzen, J. Mater. Res. 7, 613 (1992).

    CAS  Article  Google Scholar 

  17. 17.

    R. K. Nalla, M. Balooch, J. W. Ager III, J. J. Kruzic, J. H. Kinney and R. O. Ritchie, Acta Biomater. 1, 31 (2005).

    CAS  Article  Google Scholar 

  18. 18.

    E. P. Paschalis, K. Verdelis, S. B. Doty, A. L. Boskey, R. Mendelsohn and M. Yamauchi, J. Bone Miner. Res. 16, 1821 (2001).

    CAS  Article  Google Scholar 

  19. 19.

    A. Carden and M. D. Morris, J. Biomed. Opt. 5, 259 (2000).

    CAS  Article  Google Scholar 

  20. 20.

    J. Bandekar, Biochimica et Biophysica Acta. 1120, 123 (1992).

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Institutes of Health (Grant No. 5R01 DE015633), and the Office of Science, Office of Basic Energy Science, Division of Materials Sciences and Engineering, Department of Energy (No. DE-AC03-76SF00098 for JJK, JWA, MCM, ROR).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ravi K. Nalla.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nalla, R.K., Kruzic, J.J., Kinney, J.H. et al. Effects of Aging on the Toughness of Human Cortical Bone: A Study from Nano to Macro Size-Scales. MRS Online Proceedings Library 844, 10 (2004). https://doi.org/10.1557/PROC-844-Y8.10

Download citation