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The Multiscale Origins of Fracture Resistance in Human Bone and Its Biological Degradation

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Abstract

Akin to other mineralized tissues, human cortical bone can resist deformation and fracture due to the nature of its hierarchical structure, which spans the molecular to macroscopic length scales. Deformation at the smallest scales, mainly through the composite action of the mineral and collagen, contributes to bone’s strength or intrinsic fracture resistance, while crack-tip shielding mechanisms active on the microstructural scale contribute to the extrinsic fracture resistance once cracking begins. The efficiency with which these structural features can resist fracture at both small and large length scales becomes severely degraded with such factors as aging, irradiation, and disease. Indeed, aging and irradiation can cause changes to the cross-link profile at fibrillar length scales as well as changes at the three orders of magnitude larger scale of the osteonal structures, both of which combine to inhibit the bone’s overall resistance to initiation and growth of cracks.

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Notes

  1. The crack resistance-curve or R-curve provides an assessment of the fracture toughness in the presence of subcritical crack growth. It involves measurements of the crack-driving force, e.g., the stress intensity K or J-integral, as a function of crack extension (Δa). The value of the driving force at Δa → 0 provides a measure of the crack-initiation toughness, whereas the slope (used in this study) and/or the maximum value of the R-curve can be used to characterize the crack-growth toughness. Indeed, the slope of a rising R-curve is directly related to the potency of the extrinsic toughening mechanism involved.

  2. A Gray (Gy) is a unit of adsorbed dose of ionizing radiation, equivalent to absorbed energy per unit mass (1 Gy ≡ 1 J/kg). At the low dose end, the average radiation from an abdominal x-ray is ~1.4 mGy; that from a pelvic CT scan is 25 mGy. At the high dose end (>10 kGy), gamma irradiation is commonly used to terminally sterilize allograft tissues and bones.

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Acknowledgements

This work was supported by the National Institute of Health (NIH/NIDCR) under Grant No. 5R01 DE015633. We acknowledge the use of the two x-ray synchrotron beamlines 7.3.3 (SAXS/WAXD) and 8.3.2 (micro-tomography) at the Advanced Light Source at the Lawrence Berkeley National Laboratory (LBNL), which is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. The authors wish to thank Dr. Tony Tomsia for his support, Drs. Maximilien Launey, Joel Ager, Hrishikesh Bale, Eric Schaible, and Alastair MacDowell at LBNL for their considerable experimental contributions, Prof. Tamara Alliston and Simon Tang at UCSF for performing the AGEs cross-link measurements, and Prof. Tony Keaveny and Mike Jekir at UC Berkeley for allowing us to use their facilities to machine bone samples.

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Authors and Affiliations

  1. Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    E. A. Zimmermann, H. D. Barth & R. O. Ritchie

  2. Experimental Systems Group, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    H. D. Barth

  3. Department of Materials Science & Engineering, University of California, Berkeley, CA, USA

    R. O. Ritchie

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  1. E. A. Zimmermann
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  2. H. D. Barth
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  3. R. O. Ritchie
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Correspondence to R. O. Ritchie.

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Zimmermann, E.A., Barth, H.D. & Ritchie, R.O. The Multiscale Origins of Fracture Resistance in Human Bone and Its Biological Degradation. JOM 64, 486–493 (2012). https://doi.org/10.1007/s11837-012-0298-0

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