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The true toughness of human cortical bone measured with realistically short cracks

Nature Materials volume 7, pages 672–677 (2008)Cite this article

Abstract

Bone is more difficult to break than to split. Although this is well known, and many studies exist on the behaviour of long cracks in bone, there is a need for data on the orientation-dependent crack-growth resistance behaviour of human cortical bone that accurately assesses its toughness at appropriate size scales. Here, we use in situ mechanical testing to examine how physiologically pertinent short (<600 μm) cracks propagate in both the transverse and longitudinal orientations in cortical bone, using both crack-deflection/twist mechanics and nonlinear-elastic fracture mechanics to determine crack-resistance curves. We find that after only 500 μm of cracking, the driving force for crack propagation was more than five times higher in the transverse (breaking) direction than in the longitudinal (splitting) direction owing to major crack deflections/twists, principally at cement sheaths. Indeed, our results show that the true transverse toughness of cortical bone is far higher than previously reported. However, the toughness in the longitudinal orientation, where cracks tend to follow the cement lines, is quite low at these small crack sizes; it is only when cracks become several millimetres in length that bridging mechanisms can fully develop leading to the (larger-crack) toughnesses generally quoted for bone.

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Figure 1: Crack-resistance curves (R-curves) showing the orientation and crack-size-dependent fracture resistance for human cortical bone measured at different strain rates and hydration levels.
Figure 2: Crack profiles, schematic diagrams and fractography of the different extrinsic toughening mechanisms in the transverse and longitudinal orientations.
Figure 3: Synchrotron X-ray computed tomography images showing the dominant mechanisms of crack deflection and twisting in the transverse orientation.

References

  1. Currey, J. D. Bones (Princeton Univ. Press, Princeton, 2002).

    Google Scholar 

  2. 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 

  3. Nalla, R. K., Kruzic, J. J., Kinney, J. H. & Ritchie, R. O. Effect of aging on the toughness of human cortical bone: Evaluation by R-curves. Bone 35, 1240–1246 (2004).

    Article  CAS  Google Scholar 

  4. Giannoudis, P., Tzioupis, C., Almalki, T. & Buckley, R. Fracture healing in osteoporotic fractures: Is it really different? A basic science perspective. Injury Sci. Basis Fracture Healing: An Update 38, S90–S99 (2007).

    Google Scholar 

  5. Vashishth, D., Tanner, K. E. & Bonfield, W. Experimental validation of a microcracking-based toughening mechanism for cortical bone. J. Biomech. 36, 121–124 (2003).

    Article  CAS  Google Scholar 

  6. Vashishth, D. Rising crack-growth-resistance behavior in cortical bone: Implications for toughness measurements. J. Biomech. 37, 943–946 (2004).

    Article  Google Scholar 

  7. Ritchie, R. O., Gilbert, C. J. & McNaney, J. M. Mechanics and mechanisms of fatigue damage and crack growth in advanced materials. Int. J. Solids Struct. 37, 311–329 (2000).

    Article  Google Scholar 

  8. Melvin, J. W. & Evans, F. G. Biomechanics Symp. 87–88 (ASME, New York, 1973).

    Google Scholar 

  9. Bonfield, W. & Datta, P. K. Fracture toughness of compact bone. J. Biomech. 9, 131–134 (1976).

    Article  CAS  Google Scholar 

  10. Wright, T. M. & Hayes, W. C. Fracture mechanics parameters for compact bone–effects of density and specimen thickness. J. Biomech. 10, 419–425 (1977).

    Article  CAS  Google Scholar 

  11. Bonfield, W., Grynpas, M. D. & Young, R. J. Crack velocity and the fracture of bone. J. Biomech. 11, 473–479 (1978).

    Article  CAS  Google Scholar 

  12. Behiri, J. C. & Bonfield, W. Fracture mechanics of bone–the effects of density, specimen thickness and crack velocity on longitudinal fracture. J. Biomech. 17, 25–34 (1984).

    Article  CAS  Google Scholar 

  13. Moyle, D. D. & Gavens, A. J. Fracture properties of bovine tibial bone. J. Biomech. 19, 919–927 (1986).

    Article  CAS  Google Scholar 

  14. Norman, T. L., Vashishth, D. & Burr, D. B. in Advances in Bioengineering Vol. 20 (ed. Vanerby, R.) 361–364 (ASME, New York, 1991).

    Google Scholar 

  15. Norman, T. L., Vashishth, D. & Burr, D. B. Fracture toughness of human bone under tension. J. Biomech. 28, 309–320 (1995).

    Article  CAS  Google Scholar 

  16. De Santis, R. et al. Bone fracture analysis on the short rod chevron-notch specimens using the x-ray computer micro-tomography. J. Mater. Sci. - Mater. Med. 11, 629–636 (2000).

    Article  CAS  Google Scholar 

  17. 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 

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

    Article  Google Scholar 

  19. Malik, C. L., Stover, S. M., Martin, R. B. & Gibeling, J. C. Equine cortical bone exhibits rising R-curve fracture mechanics. J. Biomech. 36, 191–198 (2003).

    Article  CAS  Google Scholar 

  20. Yan, J., Mecholsky, J., John, J. & Clifton, K. B. How tough is bone? Application of elastic–plastic fracture mechanics to bone. Bone 40, 479–484 (2007).

    Article  Google Scholar 

  21. Nalla, R. K., Kruzic, J. J., Kinney, J. H. & Ritchie, R. O. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 26, 217–231 (2005).

    Article  CAS  Google Scholar 

  22. Fantner, G. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Mater. 4, 612–616 (2005).

    Article  CAS  Google Scholar 

  23. Vashishth, D., Behiri, J. C. & Bonfield, W. Crack growth resistance in cortical bone: Concept of microcrack toughening. J. Biomech. 30, 763–769 (1997).

    Article  CAS  Google Scholar 

  24. Vashishth, D. Rising crack-growth-resistance behavior in cortical bone: Implications for toughness measurements. J. Biomech. 37, 943–946 (2004).

    Article  Google Scholar 

  25. Brown, C. U., Yeni, Y. N. & Norman, T. L. Fracture toughness is dependent on bone location—a study of the femoral neck, femoral shaft, and the tibial shaft. J. Biomed. Mater. Res. 49, 380–389 (2000).

    Article  CAS  Google Scholar 

  26. Parasamian, G. & Norman, T. 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).

    Article  Google Scholar 

  27. Peterlik, H., Roschger, P., Klaushoffer, K. & Fratzl, P. From brittle to ductile fracture of bone. Nature Mater. 5, 52–55 (2006).

    Article  CAS  Google Scholar 

  28. Nalla, R. K., Kinney, J. H. & Ritchie, R. O. Mechanistic fracture criteria for the failure of human cortical bone. Nature Mater. 2, 164–168 (2003).

    Article  CAS  Google Scholar 

  29. Yeni, Y. N. & Fyhrie, D. P. A rate-dependent microcrack-bridging model that can explain the strain rate dependency of cortical bone apparent yield strength. J. Biomech. 36, 1343–1353 (2003).

    Article  Google Scholar 

  30. Behiri, J. C. & Bonfield, W. Orientation dependence of the fracture mechanics of cortical bone. J. Biomech. 22, 863–867 (1989).

    Article  CAS  Google Scholar 

  31. Knott, J. F. Fundamentals of Fracture Mechanics (Butterworth & Co., London, 1976).

    Google Scholar 

  32. Mullins, L., Bruzzi, M. & McHugh, P. Measurement of microstructural fracture toughness of cortical bone using indentation toughness. J. Biomech. 40, 3285–3288 (2007).

    Article  CAS  Google Scholar 

  33. Burr, D. B. & Martin, R. B. Calculating the probability that microcracks initiate resorption spaces. J. Biomech. 26, 613–616 (1993).

    Article  CAS  Google Scholar 

  34. Taylor, D., Hazenberg, J. G. & Lee, T. C. Living with cracks: Damage and repair in human bone. Nature Mater. 6, 249–317 (2007).

    Article  Google Scholar 

  35. Yeni, Y. & 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 

  36. Cook, J., Gordon, J. E., Evans, C. C. & Marsh, D. M. A mechanism for the control of crack propagation in all-brittle systems. Proc. R. Soc. Lond. A 282, 508–520 (1964).

    Article  Google Scholar 

  37. Evans, A. G. & Faber, K. T. Crack-growth resistance of microcracking brittle materials. J. Am. Ceram. Soc. 67, 255–260 (1984).

    Article  Google Scholar 

  38. Nalla, R. K., Stölken, J. S., Kinney, J. H. & Ritchie, R. O. Fracture in human cortical bone: Local fracture criteria and toughening mechanisms. J. Biomech. 38, 1517–1525 (2005).

    Article  CAS  Google Scholar 

  39. Koester, K. J., Ager, J. W. III & Ritchie, R. O. The effect of aging on crack-growth resistance and toughening mechanisms in human dentin. Biomaterials 29, 1318–1328 (2008).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  41. Faber, K. T. & Evans, A. G. Crack deflection process—I theory. Acta Metall. 31, 565–576 (1983).

    Article  Google Scholar 

  42. E1820, Standard test method for measurement of fracture toughness (American Society for Testing and Materials, West Conshohocken, PA, 2006).

    Google Scholar 

  43. Rice, J. R. A path independent integral and the approximate analysis of strain concentration by notches and cracks. J. Appl. Mech. 35, 379–386 (1968).

    Article  Google Scholar 

  44. Yang, Q. D., Cox, B. N., Nalla, R. K. & Ritchie, R. O. Re-evaluating the toughness of human cortical bone. Bone 38, 878–887 (2006).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Director, Office of Science, Office of Basic Energy Sciences, Division of Materials Sciences and Engineering, of the US Department of Energy under contract no. DE-AC02-05CH11231, and by the Laboratory Directed Research and Development Program of Lawrence Berkeley National Laboratory (LBNL). Computed X-ray tomography was carried out at LBNL’s Advanced Light Source, which is supported under the same contract. The authors thank H. Barth for help in preparing the X-ray computed tomographs.

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Authors and Affiliations

  1. Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA

    K. J. Koester, J. W. Ager III & R. O. Ritchie

  2. Department of Materials Science and Engineering, University of California, Berkeley, California 94720, USA

    R. O. Ritchie

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  1. K. J. Koester
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  2. J. W. Ager III
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  3. R. O. Ritchie
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Contributions

R.O.R. had full access to the experimental data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Data acquisition was carried out by K.J.K. Study design, interpretation and analysis of data and preparation of the manuscript were performed jointly by K.J.K., J.W.A. and R.O.R.

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Correspondence to R. O. Ritchie.

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Koester, K., Ager, J. & Ritchie, R. The true toughness of human cortical bone measured with realistically short cracks. Nature Mater 7, 672–677 (2008). https://doi.org/10.1038/nmat2221

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