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The nanocomposite nature of bone drives its strength and damage resistance

Abstract

In human bone, an amorphous mineral serves as a precursor to the formation of a highly substituted nanocrystalline apatite. However, the precise role of this amorphous mineral remains unknown. Here, we show by using transmission electron microscopy that 100–300 nm amorphous calcium phosphate regions are present in the disordered phase of trabecular bone. Nanomechanical experiments on cylindrical samples, with diameters between 250 nm and 3,000 nm, of the bone’s ordered and disordered phases revealed a transition from plastic deformation to brittle failure and at least a factor-of-2 higher strength in the smaller samples. We postulate that this transition in failure mechanism is caused by the suppression of extrafibrillar shearing in the smaller samples, and that the emergent smaller-is-stronger size effect is related to the sample-size scaling of the distribution of flaws. Our findings should help in the understanding of the multi-scale nature of bone and provide insights into the biomineralization process.

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Figure 1: Hierarchy of trabecular bone.
Figure 2: TEM analysis of ordered and disordered nanostructures.
Figure 3: Uniaxial compression results of ordered and disordered pillars.
Figure 4: Yield strengths across pillar diameters with corresponding model prediction.

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Acknowledgements

We thank M. Jett for help acquiring bone, C.-L. Guo for help with sample preparation and C. Garland for help with TEM. The authors are grateful for the financial support of the Institute for Collaborative Biotechnologies through grant W911NF-09-0001 from the US Army Research Office and the National Science Foundation through O.A.T.’s Graduate Research Fellowship Program (NSF GFRP). The content of the information does not necessarily reflect the position or the policy of the Government, and no official endorsement should be inferred.

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J.R.G. and O.A.T. designed the experiments. O.A.T. performed the experiments, analysed the data, and developed the model. O.A.T. and J.R.G. wrote the manuscript.

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Correspondence to Ottman A. Tertuliano.

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The authors declare no competing financial interests.

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Tertuliano, O., Greer, J. The nanocomposite nature of bone drives its strength and damage resistance. Nature Mater 15, 1195–1202 (2016). https://doi.org/10.1038/nmat4719

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