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Fracture resistance of human cortical bone across multiple length-scales at physiological strain rates
Abstract
While most fracture-mechanics investigations on bone have been performed at low strain rates, physiological fractures invariably occur at higher loading rates. Here, at strain rates from 10(-5) to 10(-1) s(-1), we investigate deformation and fracture in bone at small length-scales using in situ small-angle x-ray scattering (SAXS) to study deformation in the mineralized collagen fibrils and at the microstructural level via fracture-mechanics experiments to study toughening mechanisms generating toughness through crack-tip shielding. Our results show diminished bone toughness at increasing strain rates as cracks penetrate through the osteons at higher strain rates instead of deflecting at the cement lines, which is a prime toughening mechanism in bone at low strain rates. The absence of crack deflection mechanisms at higher strain rates is consistent with lower intrinsic bone matrix toughness. In the SAXS experiments, higher fibrillar strains at higher strain rates suggest less inelastic deformation and thus support a lower intrinsic toughness. The increased incidence of fracture induced by high strain rates can be associated with a loss in toughness in the matrix caused by a strain rate induced stiffening of the fibril ductility, i.e., a "locking-up" of the viscous sliding and sacrificial bonding mechanisms, which are the origin of inelastic deformation (and toughness) in bone at small length-scales.
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“Values of KIC, the fracture toughness for so-called mode I loading (tensile loading), range between 2 and 6 MPa√m and tend to be lower for longitudinal than for transverse fracture (15, 16) and to be lower at high strain rates (17, 18).”
From Bone Mechanical Properties in Healthy and Diseased States (2018) · cites this paper as [17]
In the citing paper
“Values of KIC, the fracture toughness for so-called mode I loading (tensile loading), range between 2 and 6 MPa√m and tend to be lower for longitudinal than for transverse fracture (15, 16) and to be lower at high strain rates (17, 18).”
From Bone Mechanical Properties in Healthy and Diseased States (2018) · cites this paper as [17]
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Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890
Epidemiology and outcomes of osteoporotic fractures
Cummings, S. R., & Melton, L. J. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08657-9 · Cited by 3,821
THE MATERIAL BONE: Structure-Mechanical Function Relations
Weiner, S., & Wagner, H. D. (1998) · Annual Review of Materials Science · doi:10.1146/annurev.matsci.28.1.271 · Cited by 2,717
The compressive behavior of bone as a two-phase porous structure
Carter, D., & Hayes, W. (1977) · The Journal of Bone & Joint Surgery · doi:10.2106/00004623-197759070-00021 · Cited by 2,001
Perspective on the Development of High‐Toughness Ceramics
Evans, A. G. (1990) · Journal of the American Ceramic Society · doi:10.1111/j.1151-2916.1990.tb06493.x · Cited by 1,638
Crack deflection processes—I. Theory
Faber, K. T., & Evans, A. G. (1983) · Acta Metallurgica · doi:10.1016/0001-6160(83)90046-9 · Cited by 1,455
Crack deflection at an interface between dissimilar elastic materials
He, M., & Hutchinson, J. W. (1989) · International Journal of Solids and Structures · doi:10.1016/0020-7683(89)90021-8 · Cited by 1,400
On the Fracture Toughness of Advanced Materials
Launey, M. E., & Ritchie, R. O. (2009) · Advanced Materials · doi:10.1002/adma.200803322 · Cited by 976
Self-citationMechanisms of fatigue-crack propagation in ductile and brittle solids
Ritchie, R. O. (1999) · International Journal of Fracture · doi:10.1023/a:1018655917051 · Cited by 963
Self-citationFantner, G. E., Hassenkam, T., Kindt, J. H., Weaver, J. C., Birkedal, H., Pechenik, L., Cutroni, J. A., Cidade, G. A. G., Stucky, G. D., Morse, D. E., et al. (2005) · Nature Materials · doi:10.1038/nmat1428 · Cited by 933
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Metadata
- Authors
- Zimmermann, E. A., Gludovatz, B., Schaible, E., Busse, B., & Ritchie, R. O.
- Affiliations
- Lawrence Berkeley National Laboratory (US)
- Corresponding author
- Ritchie, Robert O.
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2014-07
- Volume
- 35
- Issue
- 21
- Pages
- 5472-5481
- ISSN
- 0142-9612 (ISSN-L)
- OpenAlex
- W1964465273
- Cited by
- 163
- References
- 61
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 18 · 2023: 10 · 2022: 11 · 2021: 16 · 2020: 22 · 2019: 16 · 2018: 14 · 2017: 10 · 2016: 11 · 2015: 14 · 2014: 2
- FWCI
- 12.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Dental and Craniofacial Research (R01DE015633)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Physical Sciences › Materials Science › Biomaterials › Calcium Carbonate Crystallization and Inhibition
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone fractures and treatments
- Keywords
- cortical bone, fracture resistance, strain rate sensitivity, bone toughness, crack deflection, cement lines, osteons, collagen fibrils, small-angle X-ray scattering, crack tip shielding, inelastic deformation, physiological load
- MeSH terms
- Biomechanical Phenomena, Bone Matrix, Humans, Male, Microscopy, Electron, Scanning, Middle Aged, Radiography, X-Ray Diffraction, Fibril-Associated Collagens, Fractures, Bone, Scattering, Small Angle
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