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

  • L. P. MullinsEmail author
  • V. Sassi
  • P. E. McHugh
  • M. S. Bruzzi


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.


Bone mechanics Fracture toughness Nanoindentation Indentation fracture Bone quality 



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.


  1. 1.
    Ammann, P., and R. Rizzoli. Bone strength and its determinants. Osteoporos. Int. 14(3):S13–S18, 2003.PubMedGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 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.PubMedGoogle Scholar
  8. 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.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 12.
    Gong, J. K., J. S. Arnold, and S. H. Cohn. Composition of trabecular and cortical bone. Anat. Rec. 149:325–331, 1964.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedGoogle Scholar
  14. 14.
    Hassan, R., A. A. Caputo, and R. F. Bunshah. Fracture toughness of human enamel. J. Dent. Res. 60(4):820–827, 1981.PubMedGoogle Scholar
  15. 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. 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.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. 20.
    Martin, R., O. Yeh, and D. Fyhrie. On sampling bones for microcracks. Bone 40(4):1159–1165, 2007.CrossRefPubMedGoogle Scholar
  21. 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.Google Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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. 32.
    Quinn, D. G. On the Vickers indentation fracture toughness test. J. Am. Ceram. Soc. 90(3):673–680, 2007.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedGoogle Scholar
  36. 36.
    Vashishth, D. Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements. J. Biomech. 37(6):943–946, 2004.CrossRefPubMedGoogle Scholar
  37. 37.
    Viguet-Carrin, S., P. Garnero, and P. D. Delmas. The role of collagen in bone strength. Osteoporos. Int. 17(3):319–336, 2006.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.PubMedGoogle Scholar
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2009

Authors and Affiliations

  • L. P. Mullins
    • 1
    • 2
    Email author
  • V. Sassi
    • 1
    • 2
  • P. E. McHugh
    • 1
    • 2
  • M. S. Bruzzi
    • 1
    • 2
  1. 1.Department of Mechanical and Biomedical EngineeringNational University of IrelandGalwayIreland
  2. 2.National Centre for Biomedical Engineering ScienceNational University of IrelandGalwayIreland

Personalised recommendations