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Mechanistic fracture criteria for the failure of human cortical bone

Abstract

A mechanistic understanding of fracture in human bone is critical to predicting fracture risk associated with age and disease. Despite extensive work, a mechanistic framework for describing how the microstructure affects the failure of bone is lacking. Although micromechanical models incorporating local failure criteria have been developed for metallic and ceramic materials1,2, few such models exist for biological materials. In fact, there is no proof to support the widely held belief that fracture in bone is locally strain-controlled3,4, as for example has been shown for ductile fracture in metallic materials5. In the present study, we provide such evidence through a novel series of experiments involving a double-notch-bend geometry, designed to shed light on the nature of the critical failure events in bone. We examine how the propagating crack interacts with the bone microstructure to provide some mechanistic understanding of fracture and to define how properties vary with orientation. It was found that fracture in human cortical bone is consistent with strain-controlled failure, and the influence of microstructure can be described in terms of several toughening mechanisms. We provide estimates of the relative importance of these mechanisms, such as uncracked-ligament bridging.

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Figure 1: The difference between failure criteria, the test geometry and the orientations used.
Figure 2: Scanning electron micrographs of the area near the unbroken notch for various orientations.
Figure 3: Scanning electron micrographs illustrating toughening mechanisms in bone through interactions between the crack and the microstructure interactions.

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References

  1. Ritchie, R.O., Knott, J.F. & Rice, J.R. On the relationship between critical tensile stress and fracture toughness in mild steel. J. Mech. Phys. Solids 21, 395–410 (1973).

    Article  CAS  Google Scholar 

  2. Ritchie, R.O., Server, W.L. & Wullaert, R.A. Critical fracture stress and fracture strain models for the prediction of lower and upper shelf toughness in nuclear pressure vessel steels. Metall. Trans. A 10, 1557–1570 (1979).

    Article  Google Scholar 

  3. Yeh, O.C. & Keaveny, T.M. Relative roles of microdamage and microfracture in the mechanical behaviour of trabecular bone. J. Orthopaed. Res. 19, 1001–1007 (2001).

    Article  CAS  Google Scholar 

  4. Keyak, J.H. & Rossi, S.A. Prediction of femoral fracture load using finite element models: an examination of stress- and strain-based failure theories. J. Biomech. 33, 209–214 (2000).

    Article  CAS  Google Scholar 

  5. Lewandowski, J.J. & Thompson A.W. in Advances in Fracture Research (Fracture 84): Proc. 6thInt. Conf. on Fracture (ed. Valluri, S. R.) 1515–1522 (Pergamon, New York, USA, 1984).

    Google Scholar 

  6. http://ttb.eng.wayne.edu/~grimm/ME518/L3F3.html, from Park, J.B. & Lakes, R.S. Biomaterials: An Introduction (Plenum, New York, USA, 1992).

    Book  Google Scholar 

  7. Rho, J.Y., Kuhn-Spearing, L. & Zioupos, P. Mechanical properties and the hierarchical structure of bone. Med. Eng. Phys. 20, 92–102 (1998).

    Article  CAS  Google Scholar 

  8. Weiner, S. & Wagner, H.D. The material bone: Structure-mechanical function relations. Annu. Rev. Mater. Sci. 28, 271–298 (1998).

    Article  CAS  Google Scholar 

  9. Currey, J.D. 'Osteons' in biomechanical literature. J. Biomech. 15, 717 (1982).

    Article  CAS  Google Scholar 

  10. Griffiths, J.R. & Owen, D.R.J. An elastic-plastic stress analysis for a notched bar in plane strain bending. J. Mech. Phys. Solids 19, 419–431 (1971).

    Article  Google Scholar 

  11. Zioupos, P., Currey, J.D., Mirza, M.S. & Barton, D.C. Experimentally determined microcracking around a circular hole in a flat plate of bone: comparison with predicted stresses. Phil. Trans. R. Soc. Lond. B. 347, 383–396 (1995).

    Article  CAS  Google Scholar 

  12. Lotz, J.C., Cheal, E.J. & Hayes, W.C. Fracture prediction for the proximal femur using finite element models: Part I - Linear analysis. J. Biomech. Eng. 113, 353–360 (1991).

    Article  CAS  Google Scholar 

  13. Vashishth, D. et al. In vivo diffuse damage in human vertebral trabecular bone. Bone 26, 147–152 (2000).

    Article  CAS  Google Scholar 

  14. Parsamian, G.P. & Norman, T.L. 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).

    CAS  Google Scholar 

  15. Vashishth, D., Tanner, K.E. & Bonfield, W. Contribution, development and morphology of microcracking in cortical bone during crack propagation J. Biomech. 33, 1169–1174 (2000).

    Article  CAS  Google Scholar 

  16. Yeni, Y.N. & Norman, T.L. Calculation of porosity and osteonal cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth. J. Biomed. Mater. Res. 51, 504–509 (2000).

    Article  CAS  Google Scholar 

  17. Wang, X., Bank, R.A., Tekoppele, J.M. & Agrawal, C.M. The role of collagen in determining bone mechanical properties. J. Orthopaed. Res. 19, 1021–1026 (2001).

    Article  CAS  Google Scholar 

  18. Wang, X., Shen, X., Li, X. & Agrawal, C.M. Age-related changes in the collagen network and the toughness of bone. Bone 31, 1–7 (2002).

    Article  Google Scholar 

  19. Thompson, J.B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773–776 (2001).

    Article  CAS  Google Scholar 

  20. Yeni, Y.N. & Fyhrie, D.P. in Proc. Bioeng. Conf. BED Vol. 50 293–294 (ASME, New York, USA, 2001).

    Google Scholar 

  21. Burr, D.B. The contribution of the organic matrix to bone's material properties. Bone 31, 8–11 (2002).

    Article  CAS  Google Scholar 

  22. Shang, J.H. & Ritchie, R.O. Crack bridging by uncracked ligaments during fatigue-crack growth in SiC-reinforced aluminum-alloy composites. Metall. Trans. A 20, 897–908 (1989).

    Article  Google Scholar 

  23. Campbell, J.P., Venkateswara Rao, K.T. & Ritchie, R.O. The effect of microstructure on fracture toughness and fatigue crack growth behaviour in γ-titanium aluminide based intermetallics. Metall. Mater. Trans. A 30, 563–577 (1999).

    Article  Google Scholar 

  24. Phelps, J.B., Hubbard, G.B., Wang, X. & Agrawal, C.M. Microstructural heterogeneity and the fracture toughness of bone. J. Biomed. Mater. Res. 51, 735–741 (2000).

    Article  CAS  Google Scholar 

  25. Lucksanambool, P., Higgs, W.A.J., Higgs, R.J.E.D. & Swain, M.W. Fracture toughness of bovine bone: influence of orientation and storage media. Biomater. 22, 3127–3132 (2001).

    Article  Google Scholar 

  26. Zioupos, P. & Currey, J.D. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 22, 57–66 (1998).

    Article  CAS  Google Scholar 

  27. Behiri, J.C. & Bonfield, W. Orientation dependence on fracture mechanics of bone. J. Biomech. 22, 863–872 (1989).

    Article  CAS  Google Scholar 

  28. Bilby, B.A., Cardew, G.E. & Howard, I.C. in Fracture 1977 (ed. Taplin, D. H. R.)Vol. 3 197–200 (Pergamon, Oxford, UK, 1978).

    Google Scholar 

  29. Cotterell, B. & Rice, J.R. Slightly curved or kinked cracks. Int. J. Fract. 16, 155–169 (1980).

    Article  Google Scholar 

  30. Ritchie, R.O., Yu, W. & Bucci, R.J. Fatigue crack propagation in ARALL laminates: measurement of the effect of crack-tip shielding from crack bridging. Eng. Fract. Mech. 32, 361–377 (1989).

    Article  Google Scholar 

  31. ASTM E 399–90 (Reapproved 1997). Annual Book of ASTM Standards, Vol. 03.01: Metals- Mechanical Testing; Elevated and Low-temperature Tests; Metallography (ASTM, West Conshohocken, Pennsylvania, USA, 2001).

  32. Haggag, F.M. & Underwood, J.H. Compliance of a three-point bend specimen at load line. Int. J. Fract. 26, 63–65 (1984).

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Institutes of Health under Grant No. P01DE09859 (for R.K.N.) and by the Office of Science, Office of Basic Energy Science of the Department of Energy under Contract No. DE-Ac03-76SF00098 (for R.O.R.). The authors wish to thank Christian M. Puttlitz (University of California, San Francisco) for supplying the human bone used in this study, Jamie J. Kruzic for assistance with the compliance measurements, and John W. Hutchinson for helpful discussion.

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Correspondence to R.O. Ritchie.

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Nalla, R., Kinney, J. & Ritchie, R. Mechanistic fracture criteria for the failure of human cortical bone. Nature Mater 2, 164–168 (2003). https://doi.org/10.1038/nmat832

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