Multiple scale modeling for cortical bone

fracture in tension using X-FEM

Élisa Budyn∗,1 – and Thierry Hoc∗∗

∗
Department of Mechanical and Industrial Engineering, University of Illinois at
Chicago, 842 West Taylor Street, Chicago IL. 60607, USA.

∗∗
Department of Material Science, LMSSMat, UMR 8579, Ecole Centrale
Paris, Grande Voie des Vignes, Chatenay Malabry, F-92295.

ABSTRACT. We present a multiple scale method for modeling multiple crack growth in corti-
cal bone under tension. The four phase composite Haversian microstructure is discretized by
a Finite Element Method. The geometrical and mechanical bone parameters obtained by ex-
periments mimic the heterogeneity of bone at the micro scale. The cracks are initiated at the
micro scale where a critical elastic-damage strain driven criterion is met and are grown until
complete failure in heterogeneous linear elastic media when a critical stress intensity factor
criterion is reached. The cracks are modeled by the eXtended Finite Element Method. The sim-
ulations provide the global response at the macroscopic level and stress and strain fields at the
microscopic level. The model emphasizes the importance of the microstructure on bone failure
in assessing the fracture risk.
RÉSUMÉ. Nous proposons une méthode multi-échelle pour modéliser la propagation de fissures
multiples dans l’os cortical sous traction. La microstructure Haversienne composite à quatre
phases est discrétisée par une méthode éléments finis. Les paramètres du tissu osseux géomé-
triques et mécaniques obtenus par l’expérience décrivent l’hétérogénéité à l’échelle microsco-
pique. Les fissures sont initiées à l’échelle micro où un critère élastic-endommagement piloté en
déformation est atteint et sont propagées jusqu’à rupture complète dans des milieux linéaires
élastique hétérogènes. Les fissures sont modélisées par la méthode des éléments finis enrichis
(X-FEM). Les simulations montrent la réponse globale à l’échelle macroscopique et les champs
de contraintes et de déformations à l’échelle microscopique. Le modèle montre l’importance de
la microstructure dans le mécanisme de rupture en vue de déterminer un risque fracturaire.
KEYWORDS: finite element, X-FEM, cortical bone, fracture, composite, multi-scale method.
MOTS-CLÉS : element finis, X-FEM, os cortical, rupture, composite, méthode multi-échelle.

REMN – 16/2007, X-FEM, pages 215 à 238

216 REMN – 16/2007, X-FEM

1. Introduction

We present a multiple scale method for modeling multiple crack growth in cortical
bone under tension. The model is decomposed into two parts : the modeling of ran-
dom Haversian bone microstructures as a multi phase composite and the modeling of
multiple crack growth inside this heterogeneous microstructure.
Haversian cortical bone microstructure has been extensively studied as a factor in-
fluencing the mechanical behavior of the failure process of bone (Katz, 1976; Aoubiza
et al., 1996; Gottesman et al., 1980; Hogan, 1992). At the micro scale, cortical bone
is composed of densely packed concentric lamellar structures (osteons) that are em-
bedded in an interstitial matrix (Figure 1). The cement line is an interface between the
osteon and the interstitial matrix. Bone porosity is principally due to Haversian canals.
Moreover, bone is a living tissue that can adapt both its structure and its architecture to
its mechanical environment (Currey, 2003). This process produces a heterogeneous
material with a high variability in osteon bone-mineral density that is related to the
level of maturation of the newly-formed tissue.
A mechanistic understanding of the role of this complex microstructure is strongly
relevant to predicting the risk of fracture associated with age and disease. From a
statistical point of view, several studies have demonstrated that cortical bone fracture
toughness can be related to osteon density and porosity (Wright et al., 1977; Hui et
al., 1988; Schaffler et al., 1988; O.Brien et al., 2005). At the microstructural scale,
considerable work has been developed to study the initiation and growth of micro-
cracks that have been shown to act as a stimulus for bone remodeling. In in vivo
conditions, cement lines act as a microstructural barrier for the majority of cracks. In
contrast, in transverse loading the underlying microstructure does not have any signif-
icant influence on the crack propagation (Nalla et al., 2003).
Due to the complex microstructural hierarchy, the mechanical behavior and the
fracture mechanisms have been very difficult to predict. Haversian cortical bone has
often been compared to a composite where discontinuities within the material may
generate mechanical stress concentration sites for crack initiation. Several models
using homogenization theory have been developed to predict macroscopic behav-
ior (Gottesman et al., 1980; Katz, 1971; Aoubiza et al., 1996), but they do not resolve
the spatial distribution of local strain. Dong et al. (2005) developed a self-consistent
model for multi-coated cylinders to obtain more precise bounds for cortical bone.
Some attempts to model larger unit cells have been developed by Prendergast et al.
(1996), however the geometrical and mechanical local anisotropy were not included.
The objective of this work is to develop a model for Haversian cortical bone based
on a multiscale approach in order to study the influence of the microstructure features
on the strain localization pattern, which is strongly relevant in the mechanism of bone
fracture.
To solve this problem the eXtended Finite Element Method (X-FEM) which is a
numerical method for treating arbitrary discontinuities without remeshing (Belytschko
et al., 1999; Belytschko et al., 2001) is an efficient tool. In this method, cracks are
 Multiple scale modeling for cortical bone 217

initiated at the micro scale at osteonal locations where a critical elastoplastic strain
driven criterion is met. The cracks can therefore be randomly located within the mi-
crostructure. In the present paper, the Haversian microstructure that is a four phase
composite: Haversian canal, osteons, cement line and matrix, is discretized by a fi-
nite element method. The geometrical and mechanical bone parameters obtained by
nanoindentation measurements are randomly distributed to mimic the nature of bone
at the micro scale.
The discontinuities are represented by enriching the standard finite element ap-
proximation space. For cracks in the framework of linear elastic fracture mechanics,
suitable enrichments are the Heaviside function for the crack and the Westergaard
field for the crack tip. X-FEM is an application of the partition of unity (Melenk et
al., 1996) and was introduced in (Belytschko et al., 1999; Dolbow et al., 2001; Moës
et al., 1999) and later adapted for multiple cracks in Budyn et al. (2004). The crack
topology is represented by vector level sets, a method that was developed by Osher et
al. (1988) and Sethian (1999) for problems of interface tracking and later improved
by Burchard et al. (2001) and Osher et al. (2002) for the evolution of curves. Here
we use a narrow banded vector level set method developed by Ventura et al. (2002)
and Ventura et al. (2003), because this method simplifies the process of freezing the
existing level sets for cracks (Belytschko et al., 2001).
The cracks are then grown in heterogeneous linear elastic media when a critical
stress intensity factor criterion is met. The cracks with the maximum stress intensity
factors are grown so that they remain approximately at the critical stress intensity fac-
tor by adjusting the load parameter and solving for the corresponding displacement.
The solution method follows a "crack length control" algorithm. In the case of com-
peting crack tips, a stability analysis is performed to determine the crack configuration
path that leads to the maximum decrease in the potential energy. Stress intensity fac-
tors are computed by means of an interaction integral (Moran et al., 1987).
The outline of this paper is as follows. In a first part, the description of the Finite
Element Method to create the random Haversian bone microstructure is given (Sec-
tion 2). The eXtended Finite Element Method for initiation and multiple crack growth
problems until coalescence of cracks and percolation is presented (Section 3.3). Sec-
tion 4 presents the results and compared with experimental results. Conclusions are
given in Section 5.

2. Cortical bone microstructure

We consider three dimensional unit cells of cortical bone of 0.5 millimeter width
and 0.1 millimeter height. Cortical bone microstructures are represented by a four
phase composite composed by an interstitial matrix and osteonal fibers (hollow discs
in two dimensions, hollow tubes in three dimensions) coated by viscous cement lines
and hollowed by Haversian canals considered as free boundaries where normally cy-
toplasmic fluid flows freely, see Figure1b.
218 REMN – 16/2007, X-FEM

Γt
t = λ tο

Γcr1
l2 Γcr
2
l1

Ω
l3 l4
y
Γcr3 Γcr4
Γu
x
A B

(a) (b)

Figure 1. (a) Light microscope bone observation. (b) Schematic model of the cortical
unit cell

2.1. Geometrical description

All geometrical parameters are experimentally measured from light microscope

pictures of bovine bone samples as in Figure 1a. In our measurements the volumetric
fraction of the interstitial matrix is about 34 percent and the average width of the
cement lines is close to 5 µm. The distributions of the diameters of the osteons and
the Haversian canals are statistically measured from the microscopic observations and
regularized by a Gaussian fit (see Figure 2) denoted Ho for the osteons and Hc for the
Haversian canals. The average diameters are 35 µm for the Haversian canals and 140
µm for the osteons.
The random microstructure is constructed using a hard sphere scheme for which
details can be found in Torquato (2000). In this scheme each osteon i is represented
in two dimensions as a disc and defined by a position Pi (x, y) and a diameter Di .
We assume the osteons are impenetrable. The construction process can be outlined
as follows: the position Pi for one osteon is randomly chosen inside the unit cell. A
diameter Di is randomly chosen within the Ho distribution. If the osteon volume is
included in the unit cell without overlapping another osteon, it is accepted; otherwise,
it is rejected. The procedure is repeated until the surface fraction of osteon covers
more than 65 percent. Finally, a diameter for the Haversian canal for each osteon is
randomly chosen within the Hc distribution in Figure 2. We check that the obtained
porosity is between 5 to 9 percent according to our microscopic observations. The
algorithm to construct the microstructure is programed in Fortran 90 and then en-
 Multiple scale modeling for cortical bone 219

100

90

80

70

60
percent

50

40

30
experiment osteon
20 regularization osteon
experiment Havers
10 regularization Havers
0
0 50 100 150 200 250
diameter (µ m)

Figure 2. Experimental and regularized distribution of the size of the osteon diameters
and the Haversian canal diameters

coded in Python as a script file. This geometry is first discretized using a commercial
three dimensional FEM code (ABAQUS, 2004) and linear tetrahedron elements for
their efficiency and adaptability to complicated geometries. A preliminary local strain
field analysis is performed to determined the locations where the cracks are initiat-
ing. The same geometry is then discretized in a two dimensional X-FEM code using
Maltab (MATLAB7, 2006) and Gmsh (GMSH, 2006) and quadratic triangles. The
longitudinal axis of the osteons is parallel to the z-direction.

2.2. Mechanical properties

In this study the material properties are assigned in each phase based on experi-
mental observations. The four phases of the interstitial matrix, the Haversian canals,
the cement lines and the osteons can be described by four different constitutive laws.
However, the bone remodeling process produces a heterogeneous material with a high
variability in osteon bone-mineral densities and geometries.Therefore, the local me-
chanical properties of the osteons and the cement lines will be different in each osteon.
The osteons are chosen to be transversally isotropic in the three dimensional FEM
Abaqus model used for preliminary strain field analysis and isotropic in the two
dimensional XFEM Matlab/Gmsh final model. Hoc et al. (2006) have performed
nanoindentation measurements of the local Young’s modulus in wet conditions for
over a hundred osteons in the longitudinal osteonal axis (Fan et al., 2002). It is
shown that the local Young’s modulus and the bone-mineral content is reasonably
correlated (r2 =0.75).We assumed the Young’s moduli to be directly related to the
mineral content in our model. Humid nanoindentation measurement was also per-
220 REMN – 16/2007, X-FEM

100
E exp.
T
90 ET regul.
E exp.
80 L
E regul.
L
70

60
percent

50

40

30

20

10

0
5 10 15 20 25
E (GPa)

Figure 3. Experimental and regularized distributions of the Young’s moduli of the

osteons measured by nanoindentation in the transversal plane and along the axis of
the osteons

formed in the transversal direction. The obtained experimental distributions of the

Young’s moduli were regularized by a Gaussian fit (see Figure 3) denoted HT in the
transversal direction and HL in the longitudinal direction. Gaussian distributions for
local longitudinal and transversal Poisson’s ratio HνL and HνT are constructed from
micro-extensometry measurements on millimetric bone samples. The transverse shear
modulus GT is described by a Gaussian distribution HG of mean value and standard
deviation taken from Reilly et al. (1975). The attribution of the material properties
for each osteon i can be outlined as follows: a probability pi is randomly chosen to
which corresponds a longitudinal Young’s modulus within HL distribution, a transver-
sal Young’s modulus within HT and the shear modulus within HG . For the Poisson’s
ratio, the probability is fixed to 1 − pi in order to obtain the longitudinal and transver-
sal Poisson’s ratio νLi and νTi . In our model, we imposed a larger Poisson’s ratio to
osteons with lower Young’s moduli considering that less mineralized osteons contain
more collagen (Katz et al., 1971). The critical stress intensity factors of the cement
lines are linearly correlated to its Young’s modulus by a factor 10−4 to fit in the range
of 0.7 to 2 MPa (Shelton et al., 2003; Hazenberg et al., 2006). Table 1 summarizes
the material properties of the osteons.
Lakes has shown cement lines present a specific chemical composition which gives
an isotropic viscoelastic behavior (Lakes et al., 1979). This composition confers dif-
ferent elastic properties compared to the osteons that are encircled by the cement lines.
The Young’s modulus is taken 25 percent lower than the Young’s modulus of the os-
teon it encircles. The Poisson’s ratio is chosen to be 0.49 (Sabelman et al., 1997
Jul 20-23). Although only the elastic properties of the cement lines are used in this
study, The critical stress intensity factors of the cement lines are linearly correlated
 Multiple scale modeling for cortical bone 221

Table 1. Microscopic elastic properties

Osteons ET (GPa) EL (GPa) νT νL GT (GPa)

Mean value 11.51 20.71 0.17 0.18 3.57
Standard deviation 1.84 3.10 0.06 0.06 0.25
Extremum min 7.79 14.33 0 0 2.82
Extremum max 15.55 24.71 0.343 0.353 4.3
Matrix 12.66 22.78 0.153 0.162 3.93

to its Young’s modulus by a factor 10−4 and increased by 40 percent. The Haversian
canals are modeled by free boundaries and assume no viscous contact between the
cytoplasmic fluid and the canal walls.
The interstitial matrix is considered homogeneous and transversally isotropic with
Young’s moduli about 10 percent stronger than the mean values of the osteonal mod-
uli. This assumption is consistent with nanoindentation tests performed by Rho et al.
(2002) that reveal higher Young’s moduli in the matrix than in the osteons. The Pois-
son’s ratio are chosen 10 percent lower than the mean value of the osteonal Poisson’s
ratio.

3. Multiple crack growth by X-FEM

3.1. Elastic-damage strain driven criterion to initiate cracks

A linear elastic analysis using a FEM discretization with a commercial code

Abaqus is applied to cortical bone microstructures. The transversal Young modu-
lus E2 was determined for 4 different microstructure sizes (0.2, 0.3, 0.4 and 0.5 mm)
and was found to be constant (11.5 GP a) for microstructures of size greater than
0.3 mm. Therefore we choose a microstructure of 0.5 mm height and width and 0.1
mm thickness that is statistically significant . As many biological materials, failure in
bone can be described by an elastic-damage strain driven criterion. In this study we
determine the initial crack locations in the microstructure by using the critical maxi-
mum principal strain. When a critical value of 0.4 % (Pattin et al., 1996; Bayraktar
et al., 2004) has been reached in the elastic calculation, cracks are initialized for the
XFEM calculation.
Tension tests are performed on the microstructure (0.5 mm) given in Figure 4 in
the y-direction to determine regions where the critical yield strain is reached. Note
that the strain localization zone direction depends on the loading direction (Budyn et
al., 2005). The FEM analysis shows that cracks can be initiated perpendicularly to
the direction of maximum principal stress, mode I in tension. Under vertical tension
loading, initial cracks are placed horizontally starting from the edge of Haversian
222 REMN – 16/2007, X-FEM

Figure 4. 0.5 mm unit cell under 0.3% strain tension on the top face where the local
region over 0.4% are in light grey near the Haversian canals

canals. Note that we progressively increases the displacement at the top of the face
until local zones with a strain above 0.4% appear; Figure 4 shows the local maximum
principal strain fields when the top face of the bone cell is submitted to 0.3%.

3.2. Description of the problem

For our X-FEM multiple crack growth problem, we consider a two dimensional
elastic unit cell Ω with boundary Γ, nc cracks with surfaces Γcr = {Γα cr , α = 1 to
nc }, and nt crack tips as shown in Figure 1b. The normal to a surface is denoted by
n. The cracks are assumed to be traction free. Prescribed tractions t are imposed on
the boundary Γt and prescribed displacements are imposed on Γu . According to 3.1
for the boundary conditions we can prescribe a uniform traction along the top edge
of the cell and fix the displacement in the y-direction along the bottom edge and the
displacement in the x-direction of node A in Figure 1b. The implementation is limited
to linear elastic fracture mechanics in np multi phase unit cells. The equilibrium
equation and boundary conditions are given by:

∇ · σ = 0 in Ω [1]
σ · n = t on Γt [2]
u = ū on Γu [3]

where σ is the stress, u(x) is the displacement field, uT = {ux , uy }; ū is the

prescribed displacement on Γu .
 Multiple scale modeling for cortical bone 223

Each phase of material is considered elastic governed by C the tensor of elastic

moduli, and in small deformation. The length of each crack is denoted ℓi ; the set of
crack lengths is represented by a matrix ℓ = {ℓi }, i = 1 to nt . The imposed traction
t depends linearly on a scalar parameter called the load factor λ: t = λto , where to
is a reference traction field.
For a preliminary study of multiple crack growth in cortical bone modeling, the
crack propagation is described by linear elastic fracture mechanics for brittle multi
phase body by the following Lagrangian form Budyn et al. (2004):
nt
X Z
L(ℓ, u) = W(ℓ, u) + Gic dℓi [4]
i=1 Γicr

where W(ℓ, u) is the potential energy of the system, Gic is the critical energy release
rate at crack tip i. Gic is a constant parameter characteristic of each phase and a
function of (x, y). If we define nact as the number of active crack tips, the second
term in the right hand side of Equation [4] is the energy dissipated during the growth
of the nact active crack tips. The potential energy W(ℓ, u) can be decomposed into
the strain energy W int and the load potential W ext :

W(ℓ, u) = W int (ℓ, u) − W ext (u) [5]

where
1
Z
W int (ℓ, u) = ǫ(ℓ, u) : C : ǫ(ℓ, u) dΩ [6]
2 Ω\Γcr
Z
W ext (u) = λ to · u dΓ [7]
Γt

The equilibrium states of the body Ω correspond to the stationary points of [4] or
points on the boundary of the feasible domain, so the solution u ∈ U corresponds to:
nt  
X ∂W(ℓ, u)
δL = δu W(ℓ, u)δu + + Gic δℓi > 0, ∀δu ∈ Uo , ∀δℓi > 0
i=1
∂ℓi
[8]
where δu W(ℓ, u) is the variation of W with respect to u, δu is the variation of the
displacement and dℓi is a crack length differential and:

U = {uu ∈ H1 (Ω \ Γcr ) , [[u · n̄]] > 0 on Γα

cr , u = ū on Γu } [9]

Uo = U ∩ {uu = 0 on Γu } [10]
where n̄ is the normal to the crack and H1 is the Hilbert space of functions with
square integrable derivatives. Note that the displacement field is discontinuous
across the crack and that the jump [[]] in the normal displacement is required to be
non-negative.
224 REMN – 16/2007, X-FEM

The above gives:

δu W(ℓ, u) = 0 [11]
∂W(ℓ, u)
+ Gic = −Gi + Gic > 0, ∀i ∈ {1, .., nt } [12]
∂ℓi
where the energy release rate is defined as:

∂W(ℓ, u)
Gi = − [13]
∂ℓi
and [11] is the equilibrium Equation and [12] is the Griffith criterion for each crack tip
i. As it is often common to express the crack growth law in terms√ of stress intensity
factors, the energy release rate at tip i can be rewritten Ki = E ′ Gi where E ′ is the
effective Young’s modulus. At each tip i, we compute the equivalent stress intensity
i
factor Keq (Paris et al., 1965) expressed as the norm of the contribution in mode I
and mode II of the interaction integrals (Yau et al., 1980; Belytschko et al., 1999) as a
surface integral (Budyn et al., 2004):
q
i

2 i 2


Keq = KIi + KII [14]

The crack growth law in linear elastic fracture mechanics of Equation [12] can be
written:
i
< Kci ∆ℓi = 0 ( no growth )

if 0 < Keq
[15]
if Keq = Kci
i
∆ℓi ≥ 0 ( growth )
where ∆ℓi is the crack growth increment of tip i. We do not consider any closure of
the cracks, though we note that ∆ℓi < 0 is not a valid solution. If the crack closes, the
inequality [[u · n̄]] > 0 must be enforced. The cracks are grown in the direction of the
maximum hoop stress, θi :
  
1
q
2
i i i i i
θ = 2 arctan KI /KII ± KI /KII + 8 [16]
4

The above gives two directions; we choose the angle that corresponds to the posi-
tive maximum hoop stress. The stress intensity factors KIi and KII i
are computed by
an interaction integral. The equivalent stress intensity factor is computed by (14). The
expressions for the J-integral and the interaction integral as domain integrals can be
found in Moran et al. (1987).
An explicit algorithm is used to satisfy both Equations [11] and [12]. The Equi-
librium [11] is discretized and solved for a prescribed traction to and then the load
parameter λ is adjusted to satisfy [12], so that the crack with the maximum stress
intensity factor met its critical value. The crack growth increments are set at the be-
ginning of each step based on a “crack length control” scheme so that the evolution
is controlled by a monotonically increasing function of the total crack length ∆ℓtot ,
i.e. the sum of all active crack lengths (Bocca et al., 1991). In some cases, several
cracks are close to their critical stress intensity factors, the number of nact active
 Multiple scale modeling for cortical bone 225

crack to grow is determined by stability analysis and a set of competitive crack tips
Ncomp is determined as in Budyn et al. (2004). A stability analysis is conducted by
applying a second variation of the Lagrangian form [4] to determine the most stable
crack configuration evolution corresponding to that with the minimum energy dissi-
pation (Budyn et al., 2004). The derivatives of the energy release rate with respect to
the crack length (Nguyen et al., 1985; Nguyen et al., 1990), are computed by the gen-
eralized X-FEM formulation (Budyn et al., 2004) of the FEM formulation developed
by Suo et al. (1989), Suo et al. (1992) and Suo et al. (1998), All subdeterminants of
this matrix [∂Gi /∂ℓj ] are computed at time tn−1 and the maximum subdeterminant
gives the set of tips Nact that will grow at time step tn determined by:
  2
∂ L(ℓ, u)
   
∂ (Gi (σo ))
Nact = i ∈ Ncomp  max det − = max det ≥0
{i,j}∈Ncomp ∂ℓi ∂ℓj {i,j}∈Ncomp ∂ℓj
[17]
The variation of Gic in Equation [17] vanishes as we considered strong discon-
tinuities in bone material properties and Gic constant in each material phase. Note
that when multiple cracks grow at the same time, the Griffith criterion [12] is exactly
satisfied at the crack with the maximum stress intensity factor met its value, and ap-
proximately satisfied at the other cracks.

3.3. X-FEM discretization

The eXtended Finite Element Method (X-FEM) is applied to approximate the dis-
placement field and incorporate the crack representation with a step function enrich-
ment for the discontinuity of the interior of a crack and the asymptotic near-tip dis-
placement field enrichment at the tips of the cracks (Belytschko et al., 1999; Moës et
al., 1999; Budyn et al., 2004). Figure 5 displays the enrichment scheme. In a mesh
with a set of nodes I, all corner nodes of elements crossed by a crack will be enriched.
J n contains the set of corner nodes of the elements cut by the crack n enriched by
the step function of crack n (circled nodes in Figure 5). Km contains the set of corner
nodes of the element that contains the crack tip m enriched by the branch function
(squared nodes in Figure 5). Nc is the set of cracks and Nt the set of crack tips
in the entire model. The crack geometry of crack n is described by narrow banded
level set functions interpolated by signed distance function f n (x) through (Ventura
et al., 2003).
The displacement field is based on modified functions (Stazi et al., 2002) adapted
for multiple crack problems (Budyn et al., 2004) is as follows:
nc X nt X 4
!
X X X X
h n n m m
u (x) = NI (x)uI + ÑJ (x)aJ H̄J (x)+ ÑK (x) blK F̄lK (x)
I∈I n=1J∈J n m=1K∈Km l=1
[18]
where NI (x) are the shape functions for the continuous displacement field; ÑJ (x)
are the shape functions applied to the enrichment field. This choice of shape functions
226 REMN – 16/2007, X-FEM

(a) (b)

Figure 5. X-FEM representation of a crack. The circled nodes are enriched by the
step function of crack n and the square nodes are enriched with the tip enrichment of
tip m. The function f gives the distance of a point to the crack

for the enrichment field is explained in (Stazi et al., 2002; Chessa et al., 2003). aJn
are the additional unknowns for the modified step enrichment H̄Jn (x) of crack n and
m
blK are the additional unknowns for the tip enrichment of tip m for the modified lth
m
branch function F̄lK (x); and xJ is the position of node J. The modified enrichment
n m
functions H̄J and F̄lK are given in Budyn et al. (2004). As the enrichment for each
crack is local, the size of the global stiffness matrix of the system is not much larger
than that of the standard stiffness (Budyn et al., 2004).

3.4. Crack tip reaching a free boundary or another crack

Within each step, the length of each active crack tip is increased in the direction of
the maximum hoop stress by:
∆ℓtot
∆ℓi = [19]
nact
where nact is the number of active cracks that grow at the beginning of step n; nact is
determined by a stability analysis at the end of step n − 1 described in (17).

Three possibilities can arise before percolation: a crack can reach the external free
boundary, reach the free boundary of an Haverse canal or coaslesce with another crack.
When this occurs, the crack tip is annihilate or “kill” the crack tip and its near enrich-
ment removed and replaced by either a simple step function for free boundaries or a
“junction” enrichment for the linked discontinuities derived in Budyn et al. (2004).
The decision to join boundaries or an another cracks is based on heuristic consider-
ations based on the idea that a very small amount of brittle material subjected to a
 Multiple scale modeling for cortical bone 227

tensile stress will break and therefore join the boundary or another crack (Kienzler
et al., 2002; Rubinstein, 1996; Demir et al., 2001; Deng et al., 1992; Nemat-Nasser
et al., 1987). Note that a special enrichment is developed in this model when a crack
joins another crack in the same element where the tip of the connected crack is lo-
cated. In this special case of junction, the near tip enrichment of the connected crack
should be removed as well and changed into a step enrichment to ensure a perfect
strong discontinuity within this entire element that contains the junction.
For each crack tip i that is identified to grow, we consider a virtual increment
∆ℓivirt that is either set, when approaching free boundaries, to ∆ℓivirt = ∆ℓtot , where
∆ℓtot is the total crack growth per step, or more restrictively when approaching cracks,
to ∆ℓivirt = max(∆ℓi , ri ), where ∆ℓi is the increment of growth of [19] and ri is the
radius of the domain of computation of the interaction integral at tip i; the radius
ri being about twice the element length. When the mesh is fine, we have observed
that when the elements of the annular domain on which the J-integral is computed
are partially truncated by the internal (Haverse canals) or external boundary of the
model or contains another crack or another phase, the stress intensity factors still gives
the correct direction of propagation. When another phase encounters the domain of
calculation of the J-integral, the correct direction of crack propagation is still obtained
because the gradient between the moduli of the phases is not too large. However the
restrictive approach criterion is considered when many cracks interact. The length of
the added increment ∆ℓi is also adjusted when the growing crack encounters a free
boundary or another crack so that the tip dies on the boundary edge.

4. Results

We consider a square of cortical bone of width 0.5 mm containing 58 cracks

initiated after the analysis of the local strain field shown in Figure 4. The init cell is
loaded by tension in the x-direction; the force is prescribed at the top edges and the
displacement in the y-direction is prescribed equal to zero at the bottom edge. The
displacement of the bottom left corner node in the x-direction is prescribed equal to
zero in Figure 1b. The material properties are random and representative of cortical
bone microstructure as described previously and Figure 6 shows the distribution of the
local transverse Young’s moduli.
The force-deflection curves, expressed as a nominal stress versus nominal
strain curve, are shown for a osteons/cement lines SIF’s contrast of about 6 and 3
respectively in Figure 7a and c. The evolution of the nominal stress at each time step
are shown for a osteons/cement lines SIF’s contrast of about 6 and 3 respectively
in Figure 7b and d.In the present study, analysis is static and we consider two
cases when the average Stress intensity factor (SIF) of the cement lines are six
times or three times tougher as the osteons. In the first case the load deflection
curve (Figure 7a) shows three phases: from step 1 to 36 the cracks are growing
inside the osteons, which produces a strain hardening, from step 36 to 68, one
dominant crack is able to cross through the cement line of the osteon it originated
228 REMN – 16/2007, X-FEM

4
x 10
0.25
1.9 58 57
0.2 38 5037 4926 25 3445
46 33
22 21
1.8
0.15
12 11
1.7
52 51
0.1
1.6 4 3
2 1
0.05 1.5 10 9 30 29
0 1.4
24 23 44 43
−0.05 1.3 20 19
1.2
14 13
−0.1
48 47 36 35
1.1
42 41 8 7
−0.15
1 40 39 28 27
−0.2 6 5
0.9 16 15
54 53 32 18 17
−0.25
−0.3 −0.2 −0.1 0 0.1 0.2 0.3
5631 55

(a) (b)

Figure 6. (a) Heterogeneous E2 Young’s moduli distribution (MPa). (b) Initial mi-
crostructure that is implemented to start the XFEM simulations; the locations of the
initial 58 cracks are determined by the ABAQUS pre-calculation

Table 2. Case when the cement lines are three times tougher than the osteons. The
active crack’s names are given in Figure 6b. Several events can happen: A: reaches
the outer boundary, B: connects to crack 7, C: reaches an Haversian canal, D: reaches
crack 35 but cannot connect 35 again, E: reaches an Haversian canal, F: reaches the
outer boundary, G: reaches the outer boundary, H: reaches the outer boundary

step 2-5 6-10 11 12 13-15 16-18 19 20

active crack 7 8 7 36 4 3 4 3
event
step 21 22-25 26-29 30 31-41 42 43-44 45-46
active crack 35 36 8 36 8 7 8 7
event A B C D
step 47-49 50-51 52-53 54 55
active crack 48 42 10 51 58
event E F G H
 Multiple scale modeling for cortical bone 229

200 200

150 150

nominal stress (MPa)

nominal stress (MPa)

100 100

50 50

0 0
0 2 4 6 8 10 12 0 20 40 60 80 100
nominal strain (%) step

(a) (b)

200
200

150 150
nominal stress (MPa)
nominal stress (MPa)

100 100

50 50

0 0
0 2 4 6 8 10 12 0 20 40 60 80 100
nominal strain (%) step

(c) (d)

Figure 7. (a) Load deflection curve (SIF’s contrast of 6), (b) evolution of the load
versus time (SIF’s contrast of 6). (c) load deflection curve (SIF’s contrast of 3), (d)
evolution of the load versus time (SIF’s contrast of 3). The ratio of cement line average
SIF’s to osteonal average SIF’s is about 6 (upper curves, the work of separation is
1.48 × 10−3 µN.mm ) and about 3 (lower curves, the work of separation is 1.73 ×
10−4 µN.mm)

from, and damage the matrix. During this period a strain softening is observed as
the matrix looses progressively its structural integrity. Finally from 68 to 88 the
cracks grow until complete percolation, but the microstructure had already lost most
of its integrity. In the second case when the cement line are three times tougher
than the osteons, The same patterns are observed in the global load deflection
curve: from step 1 to 20 the cracks are growing inside the osteons, which produces
a strain hardening, from step 20 to 44, one dominant crack crosses through the
230 REMN – 16/2007, X-FEM

(a) (b)

(c) (d)

Figure 8. (a) Initial crack paths, (b) Crack paths ate step 36 (hardening phase), (c)
Crack paths at step 68 (softening phase), (d) Crack paths at step 88 (broken mi-
crostructure). The ratio of cement line average SIF’s to osteonal average SIF’s is
about 6

cement line of the osteon it originated from, and damages the matrix, which results
in a strain softening. Finally from 44 to 55 the cracks grow until complete percolation.

We also note the effect of the cement lines over the strain field distribution in
Figure 4b and the crack paths in Figure 8 and Table 2 and Figure 9d and Table 3.
In Budyn et al. (2005), the structural function of the cement lines was studied in
transversal compression by comparing the local strain field distributions in the same
osteonal geometry in a microstructure including cement lines around the osteons and
another microstructure without cement lines. It was noticed in the absence of cement
lines the osteons tend to transfer more deformation to the matrix; with cement lines,
 Multiple scale modeling for cortical bone 231

(a) (b)

(c) (d)

Figure 9. (a) Initial crack paths, (b) Crack paths ate step 20 (hardening phase), (c)
Crack paths at step 44 (softening phase), (d) Crack paths at step 55 (broken mi-
crostructure). Then the ratio of cement line average SIF’s to osteonal average SIF’s
is about 3

the osteons remains confined and exhibit a wider range of deformations. This phe-
nomenon can partially explain the hardening phase observed in the global behavior
due to primary growth of cracks inside as many osteons as possible before damaging
the matrix. Despite very similar crack paths in Figures 8 and 9, by comparing the two
load deflection curves in Figure 7a, we observe that more inhomogeneity makes the
response richer (Belytschko, 2006). Note that the hardening is more developed when
the cement lines are tougher and more energy is needed to break the microstructure:
the work of separation is 1.48 × 10−3 µN.mm when the cement lines are six times
tougher than the osteons and 1.73 × 10−4 µN.mm when the cement lines are three
times tougher than the osteons. Therefore the cement lines appear as critical elements
232 REMN – 16/2007, X-FEM

Table 3. Case when the cement lines are six times tougher than the osteons. The active
crack’s names are given in Figure 6b. Several events can happen: A: reaches the outer
boundary, B: reaches the outer boundary, C: reaches the outer boundary, D: connects
to crack 7, E: reaches an Haversian canal, F: reaches the outer boundary, G: reaches
the outer boundary, H: reaches the outer boundary, I: reaches the outer boundary, J:
connects to crack 6

step 2-5 6-10 11 12 13-15 16-18 19 20

active crack 7 8 7 36 4 3 4 3
event
step 21 22 23 24-26 27-29 30-32 33 34
active crack 35 22 21 5 6 28 27 15
event A B
step 35 36 37-39 40-51 52-53 54-55 56-57 58-62
active crack 16 32 7 8 6 5 6 8
event C
step 63 64-66 67 68 69-70 71 72-73 74-76
active crack 7 36 7 10 7 42 10 21
event D E F G
step 77-78 79-81 82 83-88
active crack 14 13 58 8
event H I J

in the protection of bone against fracture and relevant structural elements to study their
evolution in osteoporosis. When the cement lines are less tough, other physical results
changes: a snap-back is less pronounced, the softening phase is smoothened. Some
experimental observation of the effect of the cement lines as osteonal barriers can be
seen in Mohsin et al. (2006). However more experimental data are necessary to inves-
tigate the local fracture properties such as the stress intensity factors. Once the matrix
is damaged, softening appears at the macroscopic level as the structural integrity of
bone is lost.

5. Conclusion

The results of this preliminary study present a multiple scale approach to describe
multiple crack growth in cortical bone under tension. The Haversian microstructure is
discretized by a statistical finite element model of cortical bone material to investigate
the influence of the local geometrical and mechanical parameters of the microstructure
on the mechanical behavior of bone material. Even if in our model majority of geo-
metrical and material parameters were based on physical data, some limitations can
be given. For the geometrical description the osteons are modeled by disjoint circu-
 Multiple scale modeling for cortical bone 233

lar tubes, which is an idealized geometry and does not allow them to connect to each
other through Volkman canals (Jones et al., 2004). We study bone at the osteonal level
and do not include osteocyte lacunae (Qiu et al., 2005; Prendergast et al., 1996). We
also modeled interstitial matrix as homogeneous material. In our study we focused
our investigations on the effect of the toughness heterogeneities due to microstruc-
ture. Other heterogeneities such as the spatial distribution and shape of the osteons,
cement line thickness, the initial defect orientation and distribution ... influence the
crack paths and will be studied in further work.
To implement crack growth the eXtended Finite Element Method is particularly
suitable for multiple crack growth because remeshing is avoided. Higher order ele-
ments have been chosen, they are quadratic for the standard displacement field and
linear for the enrichment to give an accurate crack solution. In contrast to boundary
element methods, the method can easily handle the heterogeneities of the microstruc-
ture. The method is explicit, applied to static crack growth and is developed to satisfies
exactly both the equilibrium [11] and the brittle crack growth law [12] at each time
step of the load deflection curve. A stability analysis based on energy consideration
enable to solve the case of competitive crack growth. The response of the unit cell
is tracked until complete failure when the cracks have percolated the cell, joined and
reached the free boundaries. Some improvement in precision in the load deflection
curve will be obtained by using smaller steps and finer meshes to refine the heuris-
tic criterion for crack bridging and crack connecting to the free boundaries. In the
present study we considered traction loading applied to the top edge of the cell. We
are currently investigating consistency between the average local stress field when a
displacement is applied on the top edge and the average local strain field when the
corresponding traction loading to the first displacement boundary case is applied to
the top of cells containing defects. We have already studied these issues for cells of
uniform materials containing defects and the global responses was extremely similar
in both cases when load BC or corresponding displacement BC were imposed to the
top of the cells. For heterogeneous cells of 0.5 mm without defect it is also possi-
ble to recover the same macro field by applying displacement BC or the traction BC
corresponding to the first load BC case.
The model accesses two different scales: a macro scale at the unit cell level and
a micro scale for the strain field inside the osteons, in a mimetic osteonal microstruc-
ture. At macroscopic scale, the model is able to provide the overall stress and strain
response.
At the microscopic level, even if the matrix is homogeneous its strain field is not.
Moreover, our results show that cement lines have an important role in isolating the
osteons from the matrix. This explains why cement lines are implicated with energy in
fracture processes in the deflection of crack propagation by slowing it down (Advani
et al., 1987) or debonding the osteon (Guo et al., 1995). Cement lines have also been
linked to energy absorption (Akkus et al., 2001) and viscous damping (Lakes, 2001;
Dong et al., 2004) in allowing osteon movement inside the interstitial matrix.
234 REMN – 16/2007, X-FEM

In summary, this model presents preliminary results that characterize the local
properties of cortical bone and emphasizes the importance of the cement lines as an
efficient structural component to ensure internal movement at the material level and to
prevent the progression of localization damage zones and cracks. Our results suggest
how critical circular porosity (Haversian canals) are sources of localization and frac-
ture nucleation for transversal tension loading. More validations of experiments will
be developed for this type of numerical approach, where a dialog between numerical
modeling and experimental investigation can be established. Further investigations of
the physiological and mechanical properties of the cement lines and the matrix will
also help to refine the modeling of damage and fracture in cortical bone. In the future,
introduction in this model of more experimental damage and fracture parameters need
to be determined to make the model more physiological and extended to compression
loading. This will lead towards a multiscale study of bone fracture in an entire bone.

Acknowledgments

The authors are grateful for the research support of the University of Illinois at
Chicago. The first author is also grateful to the CNRS for a Post-doctoral fellowship.
We are also grateful to Professor Ted Belytschko for his comments and suggestions.

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1. A RTICLE POUR LA REVUE :

REMN – 16/2007, X-FEM

2. AUTEURS :
Élisa Budyn∗,1 – and Thierry Hoc∗∗

3. T ITRE DE L’ ARTICLE :
Multiple scale modeling for cortical bone fracture in tension using X-
FEM

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Multiple scale modeling for cortical bone

5. DATE DE CETTE VERSION :

15th February 2007

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∗
Department of Mechanical and Industrial Engineering, University of
Illinois at Chicago, 842 West Taylor Street, Chicago IL. 60607, USA.

∗∗
Department of Material Science, LMSSMat, UMR 8579, Ecole
Centrale Paris, Grande Voie des Vignes, Chatenay Malabry, F-92295.
– téléphone : (1) 312 996 96 31
– télécopie : (33) 01 41 13 16 16
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