Modeling of Bone Failure by Cohesive

Zone Models

Thomas Siegmund1 , Matthew R. Allen2 , and David B. Burr2,3,4

1
School of Mechanical Engineering, Purdue University
2
Department of Anatomy and Cell Biology, Indiana University School
of Medicine
3
Department of Orthopaedic Surgery, Indiana University School of Medicine
4
Biomedical Engineering, Indiana University-Purdue University at Indianapolis

Abstract. Cohesive zone models are a powerful tool for investigations of

non-linear deformation and failure processes. For the nanoscale, the use of
cohesive zone models is particularly attractive as the ratio of interface to
volume is high, and because locally acting bonds between material compo-
nents can become relevant. The present paper demonstrates the relevance of
cohesive zone modelling approaches to the development of a nano-mechanical
composite model of the mineralized collagen fibril, a fundamental building
block of bone. As difficulties exist in determining the independent biomechan-
ical effects of collagen cross-linking using in vitro and in vivo experiments,
computational modeling can provide insight into the nanoscale processes.
Stress-strain curves for mineralized collagen fibrils were obtained under ten-
sile loading for various collagen cross-linking conditions. Our model predicts
that the elastic deformation mode, the yield response and the final failure
of the mineralized collagen fibril may depend significantly on the state of
collagen cross-linking.

1 Introduction

Cohesive zone models have emerged as an important tool in the modeling and
simulation of the mechanical behavior of materials. These models capture the
processes occurring during material separation as a constitutive model and
describe the formation of a new defect or the extension of an already existing
defect. The use of CZMs in the context of the finite element method (FEM)
has drawn particular attention. The capability of the FEM to solve non-linear
full field problems has enabled solutions to interesting problems related to
failure of materials and structures. Studies of crack growth in a variety of
material systems and load conditions have greatly benefited from this mod-
eling approach (Hutchinson and Evans 2000). Thereby, the CZM approach
218 T. Siegmund, M.R. Allen, and D.B. Burr

can be particularly useful if crack growth resistance emerges as a combina-

tion of creation of fracture surface and bulk dissipation, and if large strains
need to be considered. In micromechanical investigations of failure of multi-
phase materials CZMs have been used to incorporate the phase-to-phase
interface behavior (Needleman 1987) as well as particle fracture into the anal-
ysis. Such studies have highlighted the role of reinforcement particle mechan-
ical properties, size and geometry on the composite response under uniaxial
and multiaxial loading. More recently, CZMs have also attracted attention
for the development of models for nano-composites (Tan et al. 2007). From
these models, the importance of the the interplay between reinforcement size
and interface bond conditions emerges.
We describe a nano-scale mechanical model for the mineralized collagen
fibril (MCF) underlying bone, and demonstrate that the use of CZMs enable
such efforts. In the past, several continuum mechanics-based models for the
MCF were proposed, including the equivalent inclusion method (Hellmich
et al. 2004, Fritsch and Hellmich 2007), shear-lag models (Jäger and Fratzl
2000, Kotha and Guzelsu 2003, Wang and Qian 2006), and numerical models
based on a shear-lag type geometry (Ji and Gao 2004, Arnoux et al. 2002).
An extended continuum mechanistic model of a MCF is presented with
detailed consideration of the potential deformation modes in collagen, the
debonding between collagen and mineral, and fracture of the mineral. We
consider two types of interactions between individual collagen helix domains
in the overall collagen matrix. Weak and distributed interactions between
collagen would occur due to hydrogen bonds, non-collageneous proteins, and
electrostatic interaction, whereas strong and local interactions are due to en-
zymatic and non-enzymatic cross-linking. We hypothesize that the predicted
stress-strain curves would exhibit significantly different characteristics as the
state of collagen is changed, and that such differences would also be reflected
in the distribution of strains and stresses in collagen and mineral.
The significance of the development of a model accounting for detailed fea-
tures of the collagen structure arises from the need for a better understanding
of deformation and failure behavior of bone, and ultimately its relationship
to bone health. The mechanical behavior of bone is significantly influenced
by bone mass, mineral density, and micro-architecture, but contributions of
collagen to bone’s pre- and post-yield properties are less well understood
(Burr 2002). Collagen appears to play a major role on the bone nano-scale.
While the mineral dictates much of the tissue stiffness, collagen has a pro-
found effect on bone’s post-yield properties (e.g. energy absorption) (Burr
2002). The effects of collagen depend largely on cross-linking (Knott and
Bailey 1998, Viguet-Carrin et al. 2006a, Wang et al. 2003) which can oc-
cur either enzymatically or non-enzymatically (Bailey et al. 1998, Eyre et al.
1988, Viguet-Carrin et al. 2006a). Experiments in vitro (Vashishth et al. 2004,
Wu et al. 2003, Catanese et al. 1999) and in vivo (Boxberger and Vashishth
2004, Tang et al. 2005), (Wang et al. 2002, Viguet-Carrin et al. 2006b, Allen
et al. 2008) have documented that increases in collagen cross-linking are