Abstract
Toughness is crucial to the structural function of bone. Usually, the toughness of a material is not just determined by its composition, but by the ability of its microstructure to dissipate deformation energy without propagation of the crack1. Polymers are often able to dissipate energy by viscoplastic flow or the formation of non-connected microcracks2. In ceramics, well-known toughening mechanisms are based on crack ligament bridging and crack deflection3. Interestingly, all these phenomena were identified in bone4,5,6,7,8,9,10,11,12, which is a composite of a fibrous polymer (collagen) and ceramic nanoparticles (carbonated hydroxyapatite)13,14,15,16. Here, we use controlled crack-extension experiments to explain the influence of fibre orientation on steering the various toughening mechanisms. We find that the fracture energy changes by two orders of magnitude depending on the collagen orientation, and the angle between collagen and crack propagation direction is decisive in switching between different toughening mechanisms.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Hahn, G. T. The influence of microstructure on brittle fracture toughness. Metall. Trans. A 15, 947–959 (1984).
Bower, D. I. An Introduction to Polymer Physics (Cambridge Univ. Press, Cambridge, 2002).
Sakai, M. & Bradt, R. C. Fracture toughness testing of brittle materials. Int. Mater. Rev. 38, 53–78 (1993).
Thompson, J. B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773–776 (2001).
Fantner, G. E. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bond fracture. Nature Mater. 4, 612–616 (2005).
Zioupos, P. & Currey, J. D. The extent of microcracking and the morphology of microcracks in damaged bone. J. Mater. Sci. 29, 978–986 (1994).
Zioupos, P., Wang, X. T. & Currey, J. D. The accumulation of fatigue microdamage in human cortical bone of two different ages in vitro. Clin. Biomech. 11, 365–375 (1996).
Vashishth, D., Tanner, K. E. & Bonfield, W. Experimental validation of a microcracking-based toughening mechanism for cortical bone. J. Biomech. 36, 121–124 (2003).
Liu, D., Weiner, S. & Wagner, H. D. Anisotropic mechanical properties of lamellar bone using miniature cantilever bending specimens. J. Biomech. 32, 647–654 (1999).
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).
Nalla, R. K., Kruzic, J. J. & Ritchie, R. O. On the origin of the toughness of mineralized tissue: microcracking or crack bridging? Bone 34, 790–798 (2004).
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).
Currey, J. D. The design of mineralised hard tissues for their mechanical functions. J. Exp. Biol. 202, 3285–3294 (1999).
Weiner, S. & Wagner, H. D. The material bone: structure mechanical function relations. Annu. Rev. Mater. Sci. 28, 271–298 (1998).
Fratzl, P., Gupta, H. S., Paschalis, E. P. & Roschger, P. Structural and mechanical quality of the collagen-mineral nano-composite in bone. J. Mater. Chem. 14, 2115–2123 (2004).
Gao, H., Baohua, J., Jäger, I. L., Arzt, E. & Fratzl, P. Materials become insensitive to flaws at nanoscale: lessons from nature. Proc. Natl Acad. Sci. USA 100, 5597–5600 (2003).
Keckes, J. et al. Cell-wall recovery after irreversible deformation of wood. Nature Mater. 2, 810–814 (2003).
Kamat, S., Su, X., Ballarini, R. & Heuer, A. H. Structural basis for the fracture toughness of the shell of the conch Strombus gigas. Nature 405, 1036–1040 (2000).
Aizenberg, J. et al. Skeleton of Euplectella sp.: Structural hierarchy from the nanoscale to the macroscale. Science 309, 275–278 (2005).
Giraud-Guille, M. Plywood structures in nature. Curr. Opin. Solid State Mater. Sci. 3, 221–227 (1998).
Wagner, H. D. & Weiner, S. On the relationship between the microstructure of bone and its mechanical stiffness. J. Biomech. 25, 1311–1320 (1992).
Gupta, H. S. et al. Nanoscale deformation mechanisms in bone. Nano Lett. 5, 2108–2111 (2005).
Peterlik, H. Crack bridging stresses in alumina during crack extension. J. Mater. Sci. Lett. 20, 1703–1705 (2001).
Behiri, J. C. & Bonfield, W. Orientation dependence of the fracture-mechanics of cortical bone. J. Biomech. 22, 863–872 (1989).
Martin, R. B. & Boardman, D. L. The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. J. Biomech. 26, 1047–1054 (1993).
Reilly, D. T. & Burstein, A. H. The elastic and ultimate properties of compact bone tissue. J. Biomech. 8, 393–405 (1975).
Currey, J. D. Bones—Structure and Mechanics (Princeton Univ. Press, Princeton, New Jersey, 2002).
Katz, J. L. & Meunier, A. The elastic anisotropy of bone. J. Biomech. 20, 1063–1070 (1987).
Hull, D. & Clyne, T. W. An Introduction to Composite Materials 2nd edn (Cambridge Univ. Press, Cambridge, 1996).
Martin, R. B. & Ishida, J. The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J. Biomech. 22, 419–426 (1989).
Acknowledgements
This study was supported by the AUVA (Austrian Insurance for Occupational Risk), by the WGKK (Social Health Insurance Vienna) and the FWF (Austrian Science Funds, project P16880-B13). We acknowledge A. Nader from the Institute for Pathology at the Hanusch Krankenhaus in Vienna for supplying the bone tissue.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary appendices A, B and C and figures 1-4 (PDF 1987 kb)
Rights and permissions
About this article
Cite this article
Peterlik, H., Roschger, P., Klaushofer, K. et al. From brittle to ductile fracture of bone. Nature Mater 5, 52–55 (2006). https://doi.org/10.1038/nmat1545
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nmat1545
This article is cited by
-
Heterostructured metal matrix composites for structural applications: a review
Journal of Materials Science (2024)
-
Unraveling the effect of collagen damage on bone fracture using in situ synchrotron microtomography with deep learning
Communications Materials (2022)
-
Computational homogenisation based extraction of transverse tensile cohesive responses of cortical bone tissue
Biomechanics and Modeling in Mechanobiology (2022)
-
Aggravated stress fluctuation and mechanical size effects of nanoscale lamellar bone pillars
NPG Asia Materials (2021)
-
An Interfacial Dynamic Crosslinking Approach toward Catalyst-free and Mechanically Robust Elastomeric Vitrimer with a Segregated Structure
Chinese Journal of Polymer Science (2021)