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Bone indentation recovery time correlates with bond reforming time

Nature volume 414, pages 773–776 (2001)Cite this article

Abstract

Despite centuries of work, dating back to Galileo1, the molecular basis of bone's toughness and strength remains largely a mystery. A great deal is known about bone microsctructure2,3,4,5 and the microcracks6,7 that are precursors to its fracture, but little is known about the basic mechanism for dissipating the energy of an impact to keep the bone from fracturing. Bone is a nanocomposite of hydroxyapatite crystals and an organic matrix. Because rigid crystals such as the hydroxyapatite crystals cannot dissipate much energy, the organic matrix, which is mainly collagen, must be involved. A reduction in the number of collagen cross links has been associated with reduced bone strength8,9,10 and collagen is molecularly elongated (‘pulled’) when bovine tendon is strained11. Using an atomic force microscope12,13,14,15,16, a molecular mechanistic origin for the remarkable toughness of another biocomposite material, abalone nacre, has been found12. Here we report that bone, like abalone nacre, contains polymers with ‘sacrificial bonds’ that both protect the polymer backbone and dissipate energy. The time needed for these sacrificial bonds to reform after pulling correlates with the time needed for bone to recover its toughness as measured by atomic force microscope indentation testing. We suggest that the sacrificial bonds found within or between collagen molecules may be partially responsible for the toughness of bone.

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Figure 1: Pulling on collagen.
Figure 2: Pulling on bone.
Figure 3: Indentation of bone.

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Acknowledgements

We thank E. Oroudjev, J. Cooper, D. Kohn and L. Fisher for their assistance and discussion. We also thank the reviewers of our paper for their helpful suggestions. We thank S. Babbitt and the American Philosophical Society for granting us permission to use the drawing of a rat femur30 shown in Figs 2 and 3. This work was supported by the Materials Research Division and MCB Division of the National Science Foundation, the Materials Research Laboratory Program of the National Science Foundation, and the MURI programme of the Army Research Office.

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Authors and Affiliations

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

    James B. Thompson, Johannes H. Kindt, Barney Drake, Helen G. Hansma & Paul K. Hansma

  2. Department of Molecular, Cellular and Developmental Biology, University of California, Santa Barbara, 93106, California, USA

    Daniel E. Morse

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  1. James B. Thompson
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Correspondence to James B. Thompson.

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Thompson, J., Kindt, J., Drake, B. et al. Bone indentation recovery time correlates with bond reforming time. Nature 414, 773–776 (2001). https://doi.org/10.1038/414773a

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