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Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture

Nature Materials volume 4, pages 612–616 (2005)Cite this article

Abstract

Properties of the organic matrix of bone1 as well as its function in the microstructure2 could be the key to the remarkable mechanical properties of bone3. Previously, it was found that on the molecular level, calcium-mediated sacrificial bonds increased stiffness and enhanced energy dissipation in bone constituent molecules4,5. Here we present evidence for how this sacrificial bond and hidden length mechanism contributes to the mechanical properties of the bone composite, by investigating the nanoscale arrangement of the bone constituents6,7,8 and their interactions. We find evidence that bone consists of mineralized collagen fibrils and a non-fibrillar organic matrix2, which acts as a ‘glue’ that holds the mineralized fibrils together. We believe that this glue may resist the separation of mineralized collagen fibrils. As in the case of the sacrificial bonds in single molecules5, the effectiveness of this mechanism increases with the presence of Ca2+ ions.

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Figure 1: Mineralized collagen fibrils interconnected by a glue-like component.
Figure 2: The AFM can measure the restoring forces between mineralized fibrils in the bone.
Figure 3: Possible kinds of sacrificial bonds involved in the glue between the mineralized collagen fibrils.

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Acknowledgements

The authors would like to thank A. Diez-Perez, H. Waite, K. Fields, S. Weiner, M. Rief, W. Landis, P. Fratzl and S. Masahiko for their suggestions and discussion. We also thank Gelson’s Markets, Santa Barbara, especially Phil Vega, for supplying fresh bovine vertebrae. This research was supported by: NASA University Research, Engineering and Technology Institute on Bio Inspired Materials, NIH, NSF, the Institute for Collaborative Biotechnologies from the US Army Research Office, Veeco Instruments, the UCSB Materials Research Laboratory, the NOAA National Sea Grant College Program, US Dept of Commerce through the California Sea Grant College System and a CNPq Fellowship, Brazil. T.H. and H.B. thank the Danish research council for additional support. G.F. thanks the Austrian Academy of Science for a DOC scholarship.

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Authors and Affiliations

  1. Department of Physics, University of California, Santa Barbara, California, 93106, USA

    Georg E. Fantner, Tue Hassenkam, Johannes H. Kindt, Leonid Pechenik, Jacqueline A. Cutroni & Paul K. Hansma

  2. University of California, Santa Barbara, Institute for Collaborative Biotechnologies, California, 93106, USA

    James C. Weaver & Daniel E. Morse

  3. Department of Chemistry and Biochemistry, University of California, Santa Barbara, California, 93106, USA

    Henrik Birkedal & Galen D. Stucky

  4. Federal University of Rio de Janeiro, Biophysics Institute Carlos Chagas Filho, Rio de Janeiro, 21491-590, Brazil

    Geraldo A. G. Cidade

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Correspondence to Georg E. Fantner.

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Fantner, G., Hassenkam, T., Kindt, J. et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Mater 4, 612–616 (2005). https://doi.org/10.1038/nmat1428

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