The true toughness of human cortical bone measured with realistically short cracks

1Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA
2Department of Materials Science and Engineering, University of California, Berkeley, California 94720, USA

On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone

Holly D. Barth a,b,c,1, Maximilien E. Launey a,1, Alastair A. MacDowell b, Joel W. Ager III a, Robert O. Ritchie a,c,⁎
a Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA
b Experimental Systems Group, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA
Department of Materials Science and Engineering, University of California, Berkeley, CA 94720, USA

Mixed-mode fracture of human cortical bone
Elizabeth A. Zimmermann a,b, Maximilien E. Launey a, Holly D. Barth a,b,c, Robert O. Ritchie a,b,*
Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA
Department of Materials Science and Engineering, University of California, Berkeley, CA 94720, USA
Experimental Systems Group, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA


Bone is more difficult to break than to split. Although this is well known, and many studies exist on the behaviour of long cracks in
bone, there is a need for data on the orientation-dependent crack-growth resistance behaviour of human cortical bone that accurately
assesses its toughness at appropriate size scales.Here,we use in situ mechanical testing to examine howphysiologically pertinent short
(<600 μm) cracks propagate in both the transverse and longitudinal orientations in cortical bone, using both crack-deflection/twist
mechanics and nonlinear-elastic fracture mechanics to determine crack-resistance curves.We find that after only 500 μmof cracking,
the driving force for crack propagation was more than five times higher in the transverse (breaking) direction than in the longitudinal
(splitting) direction owing to major crack deflections/twists, principally at cement sheaths. Indeed, our results show that the true
transverse toughness of cortical bone is far higher than previously reported. However, the toughness in the longitudinal orientation,
where cracks tend to follow the cement lines, is quite low at these small crack sizes; it is only when cracks become several millimetres
in length that bridging mechanisms can fully develop leading to the (larger-crack) toughnesses generally quoted for bone.

In situ mechanical testing coupled with imaging using high-energy synchrotron X-ray diffraction or tomography is gaining in popularity as a technique to investigate micrometer and even sub-micrometer deformation and fracture mechanisms in mineralized tissues, such as bone and teeth. However, the role of the irradiation in affecting the nature and properties of the tissue is not always taken into account.
Accordingly, we examine here the effect of X-ray synchrotron-source irradiation on the mechanistic aspects of deformation and fracture in human cortical bone. Specifically, the strength, ductility and fracture resistance (both work-of-fracture and resistance-curve fracture toughness) of human femoral bone in the transverse (breaking) orientation were evaluated following exposures to 0.05, 70, 210 and 630 kGrays (kGy) irradiation. Our results show that the radiation typically used in tomography imaging can have a major and deleterious impact on the strength, post-yield behavior and fracture toughness of cortical bone, with the severity of the effect progressively increasing with higher doses of radiation. Plasticity was essentially suppressed after as little as 70 kGy of radiation; the fracture toughness was decreased by a factor of five after 210 kGy of radiation. Mechanistically, the irradiation was found to alter the salient toughening mechanisms, manifest by the progressive elimination of the bone's capacity for plastic deformation which restricts the intrinsic toughening from the formation “plastic zones” around crack-like defects. Deep-ultraviolet Raman spectroscopy indicated that this behavior could be related to degradation in the collagen integrity.
Published by Elsevier Inc.

Although the mode I (tensile opening) fracture toughness has been the focus of most fracture mechanics studies of human cortical bone, bones in vivo are invariably loaded multiaxially. Consequently, an understanding of mixed-mode fracture is necessary to determine whether a mode I fracture toughness test provides the appropriate information to accurately quantify fracture risk. In this study, we examine the mixed-mode fracture of human cortical bone by characterizing the crack-initiation fracture toughness in the transverse (breaking) orientation under combined mode I (tensile opening) plus mode II (shear) loading using samples loaded in symmetric and asymmetric four-point bending. Whereas in most structural materials, the fracture toughness is increased with increasing mode-mixity (i.e., where the shear loading component gets larger), in the transverse orientation of bone the situation is quite different. Indeed, the competition between the maximum applied mechanical mixed-mode driving force and the weakest microstructural paths in bone results in a behavior that is distinctly different to most homogeneous brittle materials. Specifically, in this orientation, the fracture toughness of bone is markedly decreased with increasing mode-mixity.
Published by Elsevier Ltd.