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Irradiation Effects on Human Cortical Bone Fracture Behavior Print

Human bone is strong but still fallible. To better predict fracturing in bone, researchers need a mechanistic framework to understand the changes taking place on different size scales within bone, as well as the role of sustained irradiation damage. Combining in situ mechanical testing with synchrotron x-ray diffraction imaging and/or tomography, is a popular method of investigating micrometer deformation and fracture behavior in bone. However, the role that irradiation plays in these high-exposure experiments, and how it affects the properties of bone tissue, are not yet fully understood. A team of researchers led by Robert O. Ritchie at the Lawrence Berkeley National Laboratory and the University of California, Berkeley used synchrotron radiation micro-tomography at Advanced Light Source Beamline 8.3.2 to investigate changes in crack path and toughening mechanisms in human cortical bone with increased exposure to radiation, finding that exposure to high levels of irradiation can lead to drastic losses in strength, ductility, and toughness.

Bones Resisting Fracture

Bone derives its resistance to fracture from a multitude of deformation and toughening mechanisms at its various length scales. The fracture of bone is a mutual competition between intrinsic damage mechanisms acting ahead of the crack tip to promote cracking and extrinsic toughening mechanisms acting in the wake of the crack tip to inhibit cracking by shielding the crack from the applied driving force. Intrinsic toughening mechanisms act to resist crack initiation and crack growth by creating ‘plastic zones’ around crack like defects in an attempt to limit microstructural damage. The extrinsic mechanisms are predominately at length scales of more than 1 µm and involve crack deflection, out-of-plane twist, and microcracking.

Cortical bone’s toughening mechanisms are activated at each level of bone’s hierarchy; therefore, a better mechanistic understanding of bone from the nano- to the macro-scale will provide new insight into bone-related diseases, aging, and the remodeling properties of bone, aiding the evaluation of therapeutic drug treatments for a variety of bone diseases.

Cortical bone is the hard outer layer of bone that is designed to resist fracture. It is a unique and highly complex biomaterial due to its being both light and tough. At the molecular level, bone is made up of fibrous polymer collagen and hard mineral nanoparticals of hydroxyapatite that reinforce it. At the micron level, bone contains osteons - bone cylinders ~100µm in diameter with a central, longitudinal, tubular cavity (Haversian canal), blood vessels, and nerves. Bone’s mechanical behavior is a function of this multi-scaled, hierarchical structure.

The structure of bone showing the seven levels of hierarchy with prevailing toughening mechanisms. At the smallest level—at the scale of the tropocollagen molecules and mineralized collagen fibrils, (intrinsic) toughening, i.e.—plasticity, is achieved via mechanisms of molecular uncoiling and intermolecular sliding of molecules. At coarser levels like the scale of the fibril arrays, microcracking and fibrillar sliding act as plasticity mechanisms and contribute to the intrinsic toughness. At micrometer dimensions, the breaking of sacrificial bonds at the interfaces of fibril arrays contributes to increased energy dissipation, together with crack bridging by collagen fibrils. At the largest length-scales (10's to 100's µm), the primary sources of toughening are extrinsic and result from extensive crack deflection and crack bridging by uncracked ligaments, both mechanisms that are motivated by the occurrence of microcracking.

Human bone is exposed to irradiation for a wide range of medical and scientific research. For example, bones are sterilized through gamma source irradiation for bone allograft surgery, where the standard dose is between 25 kGy to 35 kGy (a fatal dose received by the body is 5 gray, where 1 gray= 1 J/kg). Despite this established standard dose, the effect of irradiation on the mechanical integrity of bone remains controversial.

Irradiation effects resulting from experiments using in situ testing with high-energy synchrotron x-ray diffraction and tomography imaging remain a concern for researchers. A typical tomography experiment involves irradiation at a rate of ~100 Gy/s, leading to as much as ~MGy of irradiation resulting from long exposure times.

Mechanical properties of human cortical bone subjected to varying degrees of x-ray irradiation. (a) Stress–strain curves from three-point bending tests (offset for clarity) for hydrated human cortical bone in the transverse orientation at different levels of irradiation. (b) Changes in mechanical properties of hydrated human cortical bone with irradiation dose. The graphs show that there is a severe and progressive degradation in mechanical properties, specifically in the bending stress/strain properties, with increase in x-ray irradiation dose. Values plotted are normalized to the highest value for each group (=100%).

Synchrotron radiation microtomography was employed to evaluate the changes in the fracture resistance of bone exposed to high levels of irradiation. Researchers collected three-dimensional images of the crack paths and microstructures in bone subjected to different degrees of irradiation (0 kGy, 50 Gy, 70 kGy, 210 kGy, and 630 kGy); the higher doses were comparable to the x-ray irradiation levels typically encountered during x-ray computed microtomography (µXCT) scans.

The effect of irradiation is to dramatically degrade the strength and toughness of bone together with any capacity for plastic deformation (which relates to bones’ ability to break and reform bonds). For example, bone toughness decreased by a factor of five after 210 kGy of irradiation. This is associated with degradation mechanisms at numerous length-scales. Specifically, at the nanoscale, irradiation leads to a marked increase in collagen cross-linking and molecular damage (assessed using Raman spectroscopy), resulting in a loss in strength and plasticity. Additionally, at length-scales above a micron, toughening mechanisms can be markedly changed. Cortical bones’ resistance to fracture in the transverse (breaking) orientation can be associated with radical changes in the crack path, such as crack deflection and twisting, as a growing crack encounters the boundaries of the osteons. The technique of X-ray microtomography has been utilized here to identify changes in these toughening mechanisms at this significant length scale.

Comparison of crack propagation through microstructure. Synchrotron x-ray tomography images from ALS Beamline 8.3.2 showing the crack path in the non-irradiated (a) and 210 kGy irradiated (b) hydrated human cortical bone (notch shown by orange arrow; crack surface is purple/pink; Haversian canals are yellow). Two-dimensional tomographs (c and d) of the paths from the back face of the sample. The crack deflects upon encountering the osteons. Such crack deflection and crack twisting is the prime extrinsic toughening mechanism in bone in the transverse orientation. Note, however, that the frequency of such deflections is increased whereas their severity is decreased with irradiation, resulting in less meandering crack paths in irradiated bone.

The three-dimensional tomographic images show the crack path and the microstructure for both the non-irradiated human cortical bone and the bone irradiated with 210 kGy. It was observed that the crack path in cortical bone following significant levels of irradiation, still displayed crack deflection at the boundaries of the osteon; however, the frequency of such deflections increases with irradiation, leading to smaller amplitude deflections and less tortuous crack paths, both of which lessen the toughening from this mechanism.

This study shows that when biological tissue such as bone is exposed to high levels of irradiation, serious deleterious effects to the collagen can occur, leading to drastic losses in strength, ductility and toughness. It is therefore critical that studies on bone using in situ tests involving radiation, such as deformation and fracture testing coupled with x-ray diffraction and/or tomography, take this into careful consideration.

 


 

Research conducted by H.D. Barth and R.O. Ritchie (Berkeley Lab and University of California, Berkeley), M.E Launey, J.W. Ager III and A.A. MacDowell (Berkeley Lab).

Research funding: Laboratory Directed Research and Development Program of Lawrence Berkeley National Laboratory. Operation of the ALS is supported by the U.S. Department of Energy (DOE), Office of Basic Energy Sciences.

Publication about this research: H.D. Barth, M.E Launey, A.A. MacDowell, J.W. Ager III and R.O. Ritchie, On the Effect of X-ray Irradiation on the Deformation and Fracture Behavior of Human Cortical Bone, Bone, Vol. 46 (6), 2010.

ALS Science Highlight #212

 

ALSNews Vol. 311