TY - JOUR
T1 - Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales
AU - Zimmermann, Elizabeth A.
AU - Schaible, Eric
AU - Bale, Hrishikesh
AU - Barth, Holly D.
AU - Tang, Simon Y.
AU - Reichert, Peter
AU - Busse, Bjoern
AU - Alliston, Tamara
AU - Ager, Joel W.
AU - Ritchie, Robert O.
PY - 2011/8/30
Y1 - 2011/8/30
N2 - The structure of human cortical bone evolves over multiple length scales from its basic constituents of collagen and hydroxyapatite at the nanoscale to osteonal structures at near-millimeter dimensions, which all provide the basis for its mechanical properties. To resistfracture, bone's toughness is derived intrinsically through plasticity (e.g., fibrillar sliding) at structural scales typically below a micrometer and extrinsically (i.e., during crack growth) through mechanisms (e.g., crack deflection/bridging) generated at larger structuralscales. Biological factors such as aging lead to a markedly increased fracture risk, which is often associated with an age-related loss in bone mass (bone quantity). However, we find that age-related structural changes can significantly degrade the fracture resistance(bone quality) over multiple length scales. Using in situ small-angle X-ray scattering and wide-angle X-ray diffraction to characterize submicrometer structural changes and synchrotron X-ray computed tomography and in situ fracture-toughness measurements in the scanning electron microscope to characterize effects at micrometerscales, we show how these age-related structural changes at differing size scales degrade both the intrinsic and extrinsic toughness of bone. Specifically, we attribute the loss in toughness to increased nonenzymatic collagen cross-linking, which suppresses plasticity at nanoscale dimensions, and to an increased osteonal density, which limits the potency of crack-bridging mechanisms at micrometer scales. The link between these processes is that the increasedstiffness of the cross-linked collagen requires energy to be absorbedby "plastic" deformation at higher structural levels, which occurs by the process of microcracking.
AB - The structure of human cortical bone evolves over multiple length scales from its basic constituents of collagen and hydroxyapatite at the nanoscale to osteonal structures at near-millimeter dimensions, which all provide the basis for its mechanical properties. To resistfracture, bone's toughness is derived intrinsically through plasticity (e.g., fibrillar sliding) at structural scales typically below a micrometer and extrinsically (i.e., during crack growth) through mechanisms (e.g., crack deflection/bridging) generated at larger structuralscales. Biological factors such as aging lead to a markedly increased fracture risk, which is often associated with an age-related loss in bone mass (bone quantity). However, we find that age-related structural changes can significantly degrade the fracture resistance(bone quality) over multiple length scales. Using in situ small-angle X-ray scattering and wide-angle X-ray diffraction to characterize submicrometer structural changes and synchrotron X-ray computed tomography and in situ fracture-toughness measurements in the scanning electron microscope to characterize effects at micrometerscales, we show how these age-related structural changes at differing size scales degrade both the intrinsic and extrinsic toughness of bone. Specifically, we attribute the loss in toughness to increased nonenzymatic collagen cross-linking, which suppresses plasticity at nanoscale dimensions, and to an increased osteonal density, which limits the potency of crack-bridging mechanisms at micrometer scales. The link between these processes is that the increasedstiffness of the cross-linked collagen requires energy to be absorbedby "plastic" deformation at higher structural levels, which occurs by the process of microcracking.
UR - http://www.scopus.com/inward/record.url?scp=80052277874&partnerID=8YFLogxK
U2 - 10.1073/pnas.1107966108
DO - 10.1073/pnas.1107966108
M3 - Article
C2 - 21873221
AN - SCOPUS:80052277874
SN - 0027-8424
VL - 108
SP - 14416
EP - 14421
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 35
ER -