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Differences in the Crack Resistance of Interstitial, Osteonal and Trabecular Bone Tissue

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Abstract

The purpose of this work was to investigate differences which may exist in the crack resistance of the microstructural bone tissues, i.e., osteonal, interstitial and trabecular bone. Indentations, using varying loads were used to initiate cracks of the same size scale as those which exist habitually in bone. The crack lengths and corresponding toughness values are presented for each of the tissues. Specimens were prepared using standard nanoindentation preparation techniques. Young’s modulus and hardness were measured using a Berkovich tip, while cracks were produced using a cube-corner tip. Crack lengths were subsequently measured using scanning electron microscopy. Cracks produced at the same loads were significantly longer in trabecular bone than in interstitial and osteonal cortical bone. Similarly, within individual subjects, cracks produced in interstitial bone were longer than those produced in osteonal bone. These results provide significant experimental evidence that bone microstructural tissues exhibit differing resistance to crack growth and may help explain the incidence of more microcracks in interstitial than osteonal bone. The ability of the technique to distinguish differences between individual bone tissues is promising in an area where the focus has switched to the microscale, and in particular, to measures bone quality.

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References

  1. Ammann, P., and R. Rizzoli. Bone strength and its determinants. Osteoporos. Int. 14(3):S13–S18, 2003.

    PubMed  Google Scholar 

  2. Antis, G. R., P. Chantikul, B. R. Lawn, and D. B. Marshall. A critical evaluation of indentation techniques for fracture toughness: I. Direct crack measurements. J. Am. Ceram. Soc. 64(9):533–538, 1981.

    Article  Google Scholar 

  3. Bevill, G., S. K. Eswaran, A. Gupta, P. Papadopoulos, and T. M. Keaveny. Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. Bone 39(6):1218–1225, 2006.

    Article  PubMed  Google Scholar 

  4. Boivin, G., and P. J. Meunier. The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif. Tissue Int. 70(6):503–511, 2002.

    Article  CAS  PubMed  Google Scholar 

  5. Boyce, H. 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.

    Article  CAS  PubMed  Google Scholar 

  6. Burr, D. B., and M. Hooser. Alterations to the en bloc basic fuchsin staining protocol for the demonstration of microdamage produced in vivo. Bone 17(4):431–433, 1995.

    Article  CAS  PubMed  Google Scholar 

  7. Burr, D. B., and T. Stafford. Validity of the bulk-staining technique to separate artifactual from in vivo bone damage. Clin. Orthop. Relat. Res. 260:305–308, 1990.

    PubMed  Google Scholar 

  8. Currey, J. D., K. Brear, and P. Zioupos. The effects of ageing and changes in mineral content in degrading the toughness of human femora. J. Biomech. 29(2):257–260, 1996.

    Article  CAS  PubMed  Google Scholar 

  9. Fan, Z., P. Smith, F. Rauch, and G. F. Harris. Nanoindentation as a means of distinguishing clinical type of osteogenesis imperfecta. Compos. Part B: Eng. 38:411–415, 2007.

    Article  Google Scholar 

  10. Fan, Z., J. G. Swadener, J. Y. Rho, M. E. Roy, and G. M. Pharr. Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J. Orthop. Res. 20(4):806–810, 2002.

    Article  CAS  PubMed  Google Scholar 

  11. Fazzalari, N. L., and I. H. Parkinson. Fractal properties of cancellous bone of the iliac crest in vertebral crush fracture. Bone 23(1):53–57, 1998.

    Article  CAS  PubMed  Google Scholar 

  12. Gong, J. K., J. S. Arnold, and S. H. Cohn. Composition of trabecular and cortical bone. Anat. Rec. 149:325–331, 1964.

    Article  CAS  PubMed  Google Scholar 

  13. Hansma, P., P. Turner, B. Drake, E. Yurtsev, A. Proctor, P. Mathews, J. Lelujian, C. Randall, J. Adams, and R. Jungmann. The bone diagnostic instrument II. Indentation distance increase. Rev. Sci. Instrum. 79(6):064303, 2008.

    Article  PubMed  Google Scholar 

  14. Hassan, R., A. A. Caputo, and R. F. Bunshah. Fracture toughness of human enamel. J. Dent. Res. 60(4):820–827, 1981.

    CAS  PubMed  Google Scholar 

  15. Heinrich, C., A. M. Wass, and A. S. Wineman. Determination of material properties using nanoindentation and multiple indenter tips. Int. J. Solids Struct. 46:365–376, 2009.

    Google Scholar 

  16. Hodgskinson, R., J. D. Currey, and G. P. Evans. Hardness, an indicator of the mechanical competence of cancellous bone. J. Orthop. Res. 7(5):754–758, 1989.

    Article  CAS  PubMed  Google Scholar 

  17. Imbeni, V., J. J. Kruzic, G. W. Marshall, S. J. Marshall, and R. O. Ritchie. The dentin–enamel junction and the fracture of human teeth. Nat. Mater. 4(3):229–232, 2005.

    Article  CAS  PubMed  Google Scholar 

  18. Koester, K. J., J. W. Ager, and R. O. Ritchie. The true toughness of human cortical bone measured with realistically short cracks. Nat. Mater. 7:672–677, 2008.

    Article  CAS  PubMed  Google Scholar 

  19. Kuhn, J. L., S. A. Goldstein, K. Choi, M. London, L. A. Feldkamp, and L. S. Matthews. Comparison of the trabecular and cortical tissue moduli from human iliac crests. J. Orthop. Res. 7(6):876–884, 1989.

    Article  CAS  PubMed  Google Scholar 

  20. Martin, R., O. Yeh, and D. Fyhrie. On sampling bones for microcracks. Bone 40(4):1159–1165, 2007.

    Article  CAS  PubMed  Google Scholar 

  21. McCalden, R., J. McGeough, M. Barker, and C. Court-Brown. Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J. Bone Joint Surg. (Am.) 75(8):1193–1205, 1993.

    CAS  Google Scholar 

  22. Meunier, P. J., and G. Boivin. Bone mineral density reflects bone mass but also the degree of mineralization of bone: therapeutic implications. Bone 21(5):373–377, 1997.

    Article  CAS  PubMed  Google Scholar 

  23. Morgan, E. F., H. H. Bayraktar, and T. M. Keaveny. Trabecular bone modulus-density relationships depend on anatomic site. J. Biomech. 36(7):897–904, 2003.

    Article  PubMed  Google Scholar 

  24. Mullins, L. P., M. S. Bruzzi, and P. McHugh. Measurement of the microstructural fracture toughness of cortical bone using indentation fracture. J. Biomech. 40(14):3285–3288, 2007.

    Article  CAS  PubMed  Google Scholar 

  25. Mullins, L. P., M. S. Bruzzi, and P. E. McHugh. Calibration of a constitutive model for the post-yield behaviour of cortical bone. J. Mech. Behav. Biomed. Mater. 2(5):460–470, 2009.

    Article  CAS  PubMed  Google Scholar 

  26. Nalla, R. K., J. J. Kruzic, and R. O. Ritchie. On the origin of the toughness of mineralized tissue: microcracking or crack bridging? Bone 34(5):790–798, 2004.

    Article  CAS  PubMed  Google Scholar 

  27. O’Brien, F. J., D. A. Hardiman, J. G. Hazenberg, M. V. Mercy, S. Moshin, D. Taylor, and T. C. Lee. The behaviour of microcracks in compact bone. Eur. J. Morphol. 42(1/2):71–79, 2005.

    Article  PubMed  Google Scholar 

  28. O’Brien, F. J., D. Taylor, G. R. Dickson, and T. C. Lee. Visualisation of three-dimensional microcracks in compact bone. J. Anat. 197:413–420, 2000.

    Article  PubMed  Google Scholar 

  29. O’Brien, F. J., D. Taylor, and T. C. Lee. Microcrack accumulation at different intervals during fatigue testing of compact bone. J. Biomech. 36(7):973–980, 2003.

    Article  PubMed  Google Scholar 

  30. O’Brien, F. J., D. Taylor, and T. C. Lee. The effect of bone microstructure on the initiation and growth of microcracks. J. Orthop. Res. 23(2):475–480, 2005.

    Article  PubMed  Google Scholar 

  31. Oliver, W. C., and G. M. Pharr. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7(6):1564–1583, 1992.

    Google Scholar 

  32. Quinn, D. G. On the Vickers indentation fracture toughness test. J. Am. Ceram. Soc. 90(3):673–680, 2007.

    Article  CAS  Google Scholar 

  33. Rho, J. Y., and G. M. Pharr. Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. J. Mater. Sci.: Mater. Med. 10:485–488, 1999.

    Article  CAS  Google Scholar 

  34. Rho, J. Y., P. Zioupos, J. D. Currey, and G. M. Pharr. Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation. J. Biomech. 35(2):189–198, 2002.

    Article  CAS  PubMed  Google Scholar 

  35. Stein, M. S., C. D. L. Thomas, S. A. Feik, J. D. Wark, and J. G. Clement. Bone size and mechanics at the femoral diaphysis across age and sex. J. Biomech. 31(12):1101–1110, 1998.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  37. Viguet-Carrin, S., P. Garnero, and P. D. Delmas. The role of collagen in bone strength. Osteoporos. Int. 17(3):319–336, 2006.

    Article  CAS  PubMed  Google Scholar 

  38. Wang, X., Y. J. Yoon, and H. Ji. A novel scratching approach for measuring age-related changes in the in situ toughness of bone. J. Biomech. 40(6):1401–1404, 2007.

    Article  CAS  PubMed  Google Scholar 

  39. Wasserman, N., J. Yerramshetty, and O. Akkus. Microcracks colocalize within highly mineralized regions of cortical bone tissue. Eur. J. Morphol. 42(1/2):43–51, 2005.

    Article  PubMed  Google Scholar 

  40. Yan, J., K. B. Clifton, J. Mecholsky, J. John, and R. L. Reep. Fracture toughness of manatee rib and bovine femur using a chevron-notched beam test. J. Biomech. 39(6):1066–1074, 2006.

    Article  PubMed  Google Scholar 

  41. Yeh, O. C., and T. M. Keaveny. Relative roles of microdamage and microfracture in the mechanical behavior of trabecular bone. J. Orthop. Res. 19(6):1001–1007, 2001.

    Article  CAS  PubMed  Google Scholar 

  42. Yeni, Y. N., C. U. Brown, Z. Wang, and T. L. Norman. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 21(5):453–459, 1997.

    Article  CAS  PubMed  Google Scholar 

  43. Zioupos, P. Accumulation of in vivo fatigue microdamage and its relation to biomechanical properties in ageing human cortical bone. J. Microsc. 201(2):270–278, 2001.

    Article  CAS  Google Scholar 

  44. Zioupos, P. In vivo fatigue microcracks in human bone: Material properties of the surrounding bone matrix. Eur. J. Morphol. 42(1/2):31–41, 2005.

    CAS  PubMed  Google Scholar 

  45. Zioupos, P., and J. D. Currey. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 22(1):57–66, 1998.

    Article  CAS  PubMed  Google Scholar 

  46. Zysset, P. K., X. Edward Guo, C. Edward Hoffler, K. E. Moore, and S. A. Goldstein. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J. Biomech. 32(10):1005–1012, 1999.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors wish to acknowledge funding from the Programme for Research in Third Level Institutions (PRTLI), administered by the Higher Education Authority (HEA), Ireland. The vertebrae used in this study were provided by Trinity College Dublin and Royal College of Surgeons under the “Bone for Life” project in partnership with National University of Ireland, Galway.

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Authors and Affiliations

  1. Department of Mechanical and Biomedical Engineering, National University of Ireland, Galway, Ireland

    L. P. Mullins, V. Sassi, P. E. McHugh & M. S. Bruzzi

  2. National Centre for Biomedical Engineering Science, National University of Ireland, Galway, Ireland

    L. P. Mullins, V. Sassi, P. E. McHugh & M. S. Bruzzi

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  1. L. P. Mullins
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  2. V. Sassi
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Correspondence to L. P. Mullins.

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Mullins, L.P., Sassi, V., McHugh, P.E. et al. Differences in the Crack Resistance of Interstitial, Osteonal and Trabecular Bone Tissue. Ann Biomed Eng 37, 2574–2582 (2009). https://doi.org/10.1007/s10439-009-9797-8

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  • DOI: https://doi.org/10.1007/s10439-009-9797-8

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