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**DOI 10.1007/s00466-008-0283-1
**

ORIGINAL PAPER

Fracture strength assessment and aging signs detection in human

cortical bone using an X-FEM multiple scale approach

Elisa Budyn · Thierry Hoc · Julien Jonvaux

Received: 30 April 2007 / Accepted: 18 March 2008 / Published online: 22 April 2008

© Springer-Verlag 2008

Abstract We present a multiple scale approach for mod-

eling multiple crack growth in human cortical bone under

tension. The Haversian microstructure, a four phase com-

posite, is discretized by a classical ﬁnite element method

fed with the morphological and mechanical characteristics,

experimentally measured, to mimic human bone heterogene-

ity at the micro scale. The fracture strength of human bone,

exhibiting aging signs, is investigated through tensional per-

colation simulations in statistical microstructures. The cracks

are initiated at the micro scale at locations where a criti-

cal elastic-damage strain-driven criterion is met. The cracks,

modeled by the eXtended Finite Element Method, are then

grown until complete failure when a critical stress intensity

factor criterion is attained. The model provides the fracture

strength and the global response at the material scale and

the stress–strain ﬁelds at the microscopic level. The model

creates a constitutive law at the material scale and empha-

sizes the inﬂuence of the microstructure on bone failure and

fracture risk assessment. These results are validated against

experiments.

Keywords Cortical bone · Multiple cracks · Failure ·

X-FEM · Multiple scale

E. Budyn (B) · J. Jonvaux

Department of Mechanical and Industrial Engineering,

University of Illinois at Chicago, 842 West Taylor Street,

Chicago, IL 60607, USA

e-mail: ebudyn@uic.edu

T. Hoc

Department of Material Science LMSSMat,

Ecole Centrale Paris, Grande Voie des Vignes,

92295 Chatenay Malabry, France

1 Introduction

We present a statistical X-FEM multiple scale method for

modeling failure of human cortical bone under tension. One

goal of this model creates a constitutive law at the (mac-

roscopic) scale of the material that can later be coupled to

a higher and/or lower scale(s). The model will assess the

fracture strength of human bone microstructures and their

overall behavior during the fracturing process. The model

focuses on the inﬂuence of the microstructure aging signs

on its mechanical response. The construction of the model

falls into two parts: the modeling of random human Haver-

sian bone microstructures as a multi-phase composite and the

modeling of crack growth inside the heterogeneous micro-

structures. Therefore the model provides the global response

at the material (macro) scale and the local (micro) stress and

strain ﬁelds inside the material microstructure.

Haversian cortical bone microstructure has been

extensively studied as a factor inﬂuencing the mechanical

behavior of bone during failure [1–4]. At the micro scale,

cortical bone is composed of densely packed concentric

lamellar structures (osteons) that are embedded in an intersti-

tial matrix (Fig. 1). An interface called a cement line around

each osteon isolates the sub-microstructures from the inter-

stitial matrix. Bone porosity is principally due to Haversian

canals. Bone is also a living tissue with the unique ability to

adapt both its structure and its architecture to its mechanical

environment [5]. This self-healing process termed remod-

eling produces a heterogeneous material highly variable 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 and its aging evolution is highly relevant to

predicting the risk of fracture associated with age and dis-

eases. From a statistical point of view, several studies have

123

580 Comput Mech (2008) 42:579–591

demonstrated that cortical bone fracture toughness can be

related to osteon density and porosity [6–9].

At the microstructural scale, considerable work has been

developed to study the initiation and growth of microcracks,

which have been shown to act as a stimulus for bone remod-

eling. In in vivo conditions, cement lines act as a microstruc-

tural barrier for the majority of cracks [10]. In contrast, in

transverse loading the underlying microstructure does not

have any significant inﬂuence on the crack propagation [11].

Bone mechanical behavior and fracture mechanisms have

been very difﬁcult to predict due to their complex micro-

structural hierarchy. Because Haversian cortical bone can be

compared to a composite where discontinuities within the

material may generate mechanical stress concentration sites

for crack initiation, it is essential to include the microstruc-

tural aspects into our model. Several models using hierarchi-

cal homogenizationtheoryhave beendevelopedtopredict the

macroscopic behavior [3, 12, 2] without resolving the spatial

distribution of local strains. Self-consistent models for multi-

coated cylinders [13, 14] have also been applied to obtain

more precise bounds. Thus attempts to model larger unit

cells [15] have not included the geometrical and mechan-

ical local anisotropy and the local fracturing process. The

objective of this work is to construct a constitutive model

for human Haversian cortical bone based on a multi-scale

approach. The model is intended to capture the inﬂuence of

the microstructure and its pathological aging alterations on

the strain localization pattern inside the material, and the

fracturing process under tension at the scale of the material,

which is strongly relevant in the mechanism of bone fracture

and its prediction.

The fracture process is incorporated into the proposed

model by the eXtended Finite Element Method (X-FEM), a

numerical method for treating arbitrary discontinuities with-

out remeshing [16, 17]. In this method, cracks are initiated at

the micro scale at locations where a critical elastic-damage

strain-driven criterion is met. The cracks can be randomly

located within the microstructure. In the paper, the human

Haversian microstructure is described as a four phase com-

posite (Haversian canal, osteons, cement line and matrix)

that is discretized by a classical ﬁnite element approxima-

tion. The morphological and mechanical bone parameters

are obtained by experiments and are randomly distributed to

mimic the heterogeneous nature of bone at the micro scale.

After initiation, the discontinuities are represented using

an X-FEM formulation by adding to the standard ﬁnite ele-

ment approximation space the following enrichments: the

Heaviside function for the crack edges and the Westergaard

ﬁeld for the crack tip that are suitable for cracks in the frame-

work of linear elastic fracture mechanics. X-FEMis an appli-

cation of the partition of unity [18] introduced in [16, 19, 20]

and adapted for multiple cracks in [21, 22]. The crack topol-

ogy is represented by vector level sets originally developed

by [23–26] for problems of interface tracking and the

evolution of curves. Our model uses a narrow banded vec-

tor level set method [27], in order to simplify the process of

freezing the existing level sets for cracks [17] and allowing

cracks to curve.

The cracks are then grown in heterogeneous linear elas-

tic media when a critical stress intensity factor criterion is

reached. The cracks with the maximum stress intensity fac-

tors that are computedbymeans of aninteractionintegral [28]

are grown and a load parameter is adjusted so that these

cracks remain approximately at the critical stress intensity.

The explicit solution method follows a “crack length con-

trol” algorithm. In the case of competition between cracks,

a stability analysis determines the crack conﬁguration path

that leads to the maximum decrease in the potential energy.

The outline of this paper is as follows. Section 2 presents

the description of the ﬁnite element algorithmapplied to gen-

erate statistically equivalent human Haversian bone micro-

structures. Section 3 explains the X-FEM for initiation and

multiple crack growth problems until coalescence of cracks

and percolation. Section 4 presents the results for microstruc-

tures with different aging effects and are compared against

the experience. Conclusions are given in Sect. 5.

2 Continuum model of statistically equivalent human

cortical bone microstructures

We consider three-dimensional (3D) unit cells of human cor-

tical bone of 1.5–2 mm width denoted L and 0.1 mm thick-

ness. Note that the thickness is chosen arbitrarily small for

computation efﬁciency but sufﬁciently thick to ensure the 3D

effect and the presence of several elements in the thickness

discretization. Cortical bone microstructures are represented

as four phase composites composed by an interstitial matrix

and osteonal ﬁbers (hollow ellipses in two dimensions, hol-

low elliptic tubes in three dimensions) coated by thin cement

lines and hollowed by Haversian canals considered as free

boundaries where invivocytoplasmic ﬂuidwouldﬂowfreely,

see Fig. 2.

2.1 Geometrical description

All geometrical parameters are experimentally measured

from light microscope pictures of eight women bone spec-

imens. The paper concentrates on the speciﬁc cases of the

three women as in Fig. 1: (a) denoted w02_07, (b) denoted

w03_07 and (c) denoted w10_07 for their distinctive mor-

phologies. Our morphological measurements include global

parameters such as the osteonal volume fraction denoted F

and porosity denoted p in Table 1. Local parameters such as

the osteonal density ρ

ost

is also measured. Note that w02_07

and w03_07 have similar porosities p but w03_07 has a

123

Comput Mech (2008) 42:579–591 581

Fig. 1 a Light microscope

human bone observation w02

0

7.

b Light microscope human bone

observation w03

0

7. c Light

microscope human bone

observation w10

0

7

OR

l

l

1

2

Γ

u

Ω

A

B

x

y

Γ

t

t = t λ

ο

l l

3 4

Γ

4

cr

cr

Γ

3

cr

Γ

1

Γ

2

cr

τ

u Γ

u = u

ο

λ

Fig. 2 Schematic model of the cortical unit cell

higher osteonal fraction F and a lower osteonal density ρ

ost

thus larger osteons that can be observed in the case of low

remodeling activity and also in patients treated for osteopo-

rosis. w10_07 displays osteoporosis symptoms with a sig-

nificantly higher porosity and an average osteonal fraction.

The thickness of cement lines is taken as 5 µm on aver-

age from experimental observations. The distributions of the

major and minor axis and their angle of the elliptic osteons

and the Haversian canals are statistically measured from the

microscopic observations of each woman and an example is

given in Fig. 3. These distributions are denoted H

o

for the

osteons and H

c

for the Haversian canals.

The random microstructure is constructed using a hard

sphere-type scheme for which details can be found in

Torquato [29]. In this scheme each osteon i is represented in

two dimensions as an ellipse and deﬁned by a center P

i

(x, y)

and a major axis B

i

, a minor axis A

i

and an angle α

i

. We

assume the osteons are impenetrable. The construction pro-

cess can be outlined as follows:

1. The position P

i

for one osteon is randomly chosen inside

the unit cell.

2. A major axis B

i

is randomly chosen within the H

oB

distribution.

3. A minor axis A

i

is randomly chosen within the H

oA

distribution.

4. An angle α

i

is randomly chosen within the H

oα

distribution.

5. If the osteon volume is included in the unit cell without

overlapping another osteon, it is accepted; otherwise, it

is rejected.

6. The procedure is repeated until the surface osteonal

fraction covers more than speciﬁc patient osteonal frac-

tion F.

Finally, a major axis and a minor axis for the Haversian

canal for each osteon are randomly chosen within the H

cB

and H

cA

distributions in Fig. 3 and oriented with the same α

i

angle. To reproduce microstructures statistically equivalent

to the patient cortical bone specimen, additional constraints

are added to limit the density of small, large or very distorted

osteons or Haversian canals. The constraint locations within

the morphological distributions are chosen so that the global

osteonal density is respected within 10% of the experimen-

tally observed osteonal density. This procedure leads to a ﬁrst

approximated porosity that is very close to the experimen-

tally measured porosity p. This ﬁrst porosity is then adjusted

exactly to the patient porosity p through an algorithm that

slightly increase Haversian canals that are too small for large

osteons or reduce Haversian canals that are too large for small

osteons.

The algorithm to construct the microstructure is progra-

med in Fortran 90 and then encoded in a Python script. This

geometry is ﬁrst discretized using a commercial 3D FEM

code [30] and linear tetrahedron elements for their efﬁciency

and adaptability to complicated geometries. A preliminary

local strain ﬁeld analysis is performed to determine the loca-

tions where the cracks initiate. The same geometry is then

discretized in a 2D X-FEM code using Matlab [31] and

Gmsh [32] and quadratic triangles. The longitudinal axis of

the osteons is parallel to the z-direction.

The boundary conditions shown in Fig. 2 are chosen to

mimic the experience and are applied in the 3D model on

the top and bottom surfaces and later in the 2D model on the

top and bottom edges to be compatible. We ﬁrst construct

a 3D anisotropic continuum model to initiate the cracks as

precisely as possible despite the fact that the effect of hole

123

582 Comput Mech (2008) 42:579–591

Table 1 Morphological parameters of w02_07, w03_07 and w10_07

Specimen w02_07 w03_07 w10_07

L (mm) 1.5 1.5 2.0

F (%) 41.6 57.6 56.6

p (%) 4.6 6.0 17.7

ρ

ost

48.6 39.4 89.6

is greater in 2D than 3D. Other 2D numerical and physical

criteria are under study before constructing a 3D X-FEM

model.

2.2 Mechanical properties

Inthis studythe material properties are assignedineachphase

based on experimental characterizations shown in Table 2.

The four phases of the interstitial matrix, the Haversian

canals, the cement lines and the osteons can be described by

four different constitutive laws. Note that the bone remodel-

ing process produces an heterogeneous material with a high

variability in osteon bone-mineral densities and geometries.

Therefore, the local mechanical properties of the osteons and

the cement lines will be different in each osteon.

The osteons are chosen transversally isotropic in the 3D

FEM Abaqus model used for preliminary strain ﬁeld analy-

sis and isotropic in the 2DX-FEMMatlab/Gmsh ﬁnal model

representing the transversal plane with respect to the osteon

longitudinal axis. Nanoindentationmeasurements of the local

Young’s modulus are performed in dry conditions for over

a hundred osteons in the longitudinal osteonal axis for each

patient. It is shown that local Young’s moduli and the bone-

mineral content are reasonably correlated (r

2

= 0.75) [33,

34]. We assumed the Young’s moduli to be directly related

to the mineral content in our model. Humid nanoindentation

measurement was also performed in the transversal direction.

The obtained experimental distributions of the Young’s mod-

uli are shown in Fig. 4 denoted H

T

in the transversal direc-

tion and H

L

in the longitudinal direction [22]. The micro-

scopic average transversal moduli in the osteonal (E

ost

2

)

nano

and matrix (E

mat

2

)

nano

phase are shown in Table 2. A matrix

stiffness-hardening ratio is denoted χ.

Gaussian distributions for local longitudinal and trans-

versal Poisson’s ratio H

ν

L

and H

ν

T

are constructed from

microextensometry measurements on millimetric bone sam-

ples [35]. The transverse shear modulus G

T

is described by a

Gaussian distribution H

G

of mean value and standard devia-

tiontakenfrom[36]. The attributionof the material properties

for each osteon i can be outlined as follows: a probability

p

i

is randomly chosen to which corresponds a longitudi-

nal Young’s modulus within H

L

distribution, a transversal

Young’s modulus within H

T

and the shear modulus within

H

G

. For the Poisson’s ratio, the probability is ﬁxed to 1 − p

i

0 100 200 300 400 500

0

20

40

60

80

100

b1,b2 (micrometres)

P

(

%

)

Osteons

Havers canals

(a)

0 1 2 3 4 5

0

20

40

60

80

100

b1/a1, (b2/a2)/(b1/a1)

P

(

%

)

Osteons

Havers canals

(b)

0 50 100 150 200

0

20

40

60

80

100

α (degree)

P

(

%

)

(c)

Fig. 3 Example of w03_07 experimental distribution of osteonnal and

Haversian morphological parameters: a major axis, b minor axis ratio,

c angle

123

Comput Mech (2008) 42:579–591 583

Table 2 Microscopic average Young’s moduli measured by nanoin-

dentation in w02_07, w03_07 and w10_07

Specimen w02_07 w03_07 w10_07

(E

ost

2

)

nano

(GPa) 13.5 14.3 13.9

(E

mat

2

)

nano

(GPa) 14.6 14.6 15.4

χ (%) 8.23 2.01 10.94

10 15 20 25 30 35

0

20

40

60

80

100

E (GPa)

P

(

%

)

Experimental E2

Experimental E3

Fig. 4 Example of w03_07 experimental distributions of the Young’s

moduli of the osteons measured by nanoindentation in the transversal

plane (E2) and along the axis of the osteons (E3)

in order to obtain the longitudinal and transversal Poisson’s

ratio ν

i

L

and ν

i

T

. In our model, we imposed a larger Poisson’s

ratio to osteons with lower Young’s moduli considering that

less mineralizedosteons containmore collagen[37]. The crit-

ical stress intensity factors of the cement lines are linearly

correlated to their Young’s moduli by a factor 10

−4

to ﬁt in

the range of 0.7–2 MPa [38, 39]. Tables 2 and 3 summarizes

the local and macroscopic material properties of women 2, 3

and 10.

Lakes has shown cement lines present a speciﬁc chemical

composition which gives an isotropic viscoelastic behav-

ior [40]. This composition confers different elastic proper-

ties compared to the osteons that are encircled by the cement

lines. The Young’s modulus is taken 25% lower than the

Young’s modulus of the osteon it encircles as experimen-

tally measured [34]. The Poisson’s ratio is chosen to be

25% higher [41]. 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 to

their Young’s moduli by a factor 10

−4

and increased by 40%

as they act as crack barriers [10]. 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 equal to the

Table 3 Average macroscopic Young’s moduli over 10 statistical

microstructures of w02_07, w03_07 and w10_07

Specimen w02_07 w03_07 w10_07

Transversal modulus (GPa) 12.86 12.59 8.69

Longitudinal modulus (GPa) 21.64 22.97 19.29

average of the nanoindentation measurements performed in

this phase. The matrix is usually stronger than the mean val-

ues of the osteonal moduli by a percentage χ that is spe-

ciﬁc to each patient and can indicate healthy or pathological

conditions. These observations are consistent with medical

observations [42] and the nanoindentation tests performed by

Rho et al. [43], which reveal usually higher Young’s moduli

in the matrix than in the osteons. The Poisson’s ratio are cho-

sen with the corresponding χ 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 each patient cortical

bone microstructure. The transversal Young modulus E2 can

be determined and compared to experimental measurements

before any damage occurs in Table 3. As in many biological

materials, bone failure can be described by an elastic-damage

strain driven criterion. Thus we determine the initial crack

locations in the microstructure by using the critical maximum

principal strain. When a critical value of 0.4 % [44, 45] has

been reached in the elastic calculation, cracks are initialized

for the XFEM calculation.

Tension tests are performed on the microstructures such

as in Fig. 5 in the y-direction to determine regions where the

critical yield strain is reached. Note that the strain localiza-

tion zone direction depends on the loading direction [22]. The

FEM analysis shows that cracks can be initiated perpendic-

ularly 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

canals. Note that we progressively increase the displacement

at the top of the face until local zones with a strain above

0.4%appear; Fig. 5shows the local maximumprincipal strain

ﬁelds when the top face of the bone cell is submitted to 0.4%

for patient 3.

3.2 Description of the problem

For our X-FEM multiple crack growth problem, we consider

a 2D elastic unit cell Ω with boundary Γ , n

c

cracks with

surfaces Γ

cr

= {Γ

α

cr

, α = 1 to n

c

}, and n

t

crack tips as

123

584 Comput Mech (2008) 42:579–591

Fig. 5 Example of w03_07 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

shown in Fig. 2. The normal to a surface is denoted by n.

The cracks are assumed to be traction free.

Prescribed tractions t (if present) are imposed on the

boundary Γ

t

and prescribed displacements are imposed on

Γ

u

. We previouslyinvestigatedconsistencybetweenthe aver-

age local stress ﬁeldwhena displacement is appliedonthe top

edge and the average local strain ﬁeld when the correspond-

ing traction load to the ﬁrst displacement boundary case is

applied to the top of cells containing defects [46]. This aspect

had also been studied for cells of uniform materials contain-

ing 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 [21]. For heteroge-

neous cells without defect it is also possible to recover the

same macro ﬁeld by applying displacement BC or the trac-

tion BC corresponding to the ﬁrst load BC case. According

to Sect. 3.1 in the framework of linear elasticity and in an

explicit algorithm, the boundary conditions can be either to

prescribe a uniform traction t or a uniform displacement ¯ u

along the top edge of the cell. Along the bottom edge, the

displacement is ﬁxed in the y-direction and the displacement

in the x-direction of node A is also ﬁxed in Fig. 2. For sta-

bility reason, prescribing a uniform displacement ¯ u along

the top edge usually provided smoother global response than

a prescribed traction. The former are the chosen boundary

conditions to mimic the experimental settings.

The implementation is limited to linear elastic fracture

mechanics in n

p

multi-phase unit cells. The equilibrium

equation and boundary conditions are:

∇ · σ = 0 in Ω (1)

σ · n = t on Γ

t

(2)

u = ¯ u on Γ

u

(3)

where σ is the stress, u(x) is the displacement ﬁeld, u

T

=

_

u

x

, u

y

_

; ¯ u is the prescribed displacement on Γ

u

.

Each phase of material is considered elastic governed by

C, the elastic moduli tensor, under small deformation. The

length of each crack is denoted

i

; the set of crack lengths is

represented by a matrix = {

i

}, i = 1 to n

t

. The imposed

top displacement ¯ u depends linearly on a scalar parameter

called the load factor λ: ¯ u = λ¯ u

o

, where ¯ u

o

is a reference dis-

placement ﬁeld. (If a traction t is imposed instead, it depends

linearly on a scalar parameter called the (traction) load factor

λ

t

: t = λ

t

t

o

, where t

o

is a reference traction ﬁeld. λ

t

is not

necessarily exactly equal to λ due to numerical approxima-

tion).

For a preliminary study of multiple crack growth in cor-

tical bone modeling, the crack propagation is described by

linear elastic fracture mechanics for brittle multi phase body

by the following Lagrangian form [21]:

L(, u) = W(, u) +

n

t

i =1

_

Γ

i

cr

G

i

c

d

i

(4)

where W(, u) is the potential energy of the system, G

i

c

is

the critical energy release rate at crack tip i . G

i

c

is a con-

stant parameter characteristic of each phase and a function

of (x, y). If we deﬁne n

act

as the number of active crack tips,

the second term in the right hand side of Eq. (4) is the energy

dissipated during the growth of the n

act

active crack tips. The

potential energy W(, u) can be decomposed into the strain

energy W

int

and the load potential W

ext

:

W(, u) = W

int

(, u) −W

ext

(u) (5)

where

W

int

(, u) =

1

2

_

Ω\Γ

cr

(, u) : C : (, u) dΩ (6)

W

ext

(u) = λ

t

_

Γ

t

t

o

· u dΓ (7)

Note W

ext

(u) is not present when we impose a displacement

along the top edge of the cell.

The equilibrium states of the body Ω correspond to the

stationary points of Eq.(4) or points on the boundary of the

feasible domain, so the solution u ∈ U corresponds to the

minimization:

δL=δ

u

W(, u)δu +

n

t

i =1

_

∂W(, u)

∂

i

+ G

i

c

_

δ

i

≥ 0,

∀δu ∈ U

o

, ∀δ

i

> 0 (8)

where δ

u

W(, u) is the variation of W with respect to u, δu

is the variation of the displacement and d

i

is a crack length

123

Comput Mech (2008) 42:579–591 585

differential and:

U = {uu∈H

1

(Ω\Γ

cr

) , [[u · ¯ n]] ≥0 on Γ

α

cr

, u= ¯ u onΓ

u

}

(9)

U

o

= U ∩ {uu=0 onΓ

u

} (10)

where ¯ n is the normal to the crack and H

1

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.

The above gives:

δ

u

W(, u) = 0 (11)

∂W(, u)

∂

i

+ G

i

c

= −G

i

+ G

i

c

≥ 0, ∀i ∈ {1, . . . , n

t

}

(12)

where the energy release rate is deﬁned as:

G

i

= −

∂W(, u)

∂

i

(13)

Equation (11) is the equilibrium and Eq. (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 K

i

=

√

E

G

i

where E

**is the effective Young’s modulus. At each tip i ,
**

we compute the equivalent stress intensity factor K

i

eq

[47]

expressed as the norm of the contribution in mode I and

mode II of the interaction integrals [48, 16] as a surface inte-

gral [21]:

K

i

eq

=

_

_

K

i

I

_

2

+

_

K

i

II

_

2

(14)

The crack growth law in linear elastic fracture mechanics of

Eq. (12) can be written:

_

if 0 < K

i

eq

< K

i

c

∆

i

= 0 (no growth)

if K

i

eq

= K

i

c

∆

i

≥ 0 (growth)

(15)

where ∆

i

is the crack growth increment of tip i . We do not

consider any closure of the cracks, though we note that ∆

i

<

0 is not a valid solution. If the crack closes, the inequality

[[u · ¯ n]] ≥ 0 must be enforced. The cracks are grown in the

direction of the maximum hoop stress, θ

i

:

θ

i

= 2 arctan

_

1

4

_

K

i

I

/K

i

II

±

_

_

K

i

I

/K

i

II

_

2

+ 8

__

(16)

The above gives two directions; we choose the angle that

corresponds to the positive maximum hoop stress. The stress

intensity factors K

i

I

and K

i

II

are computed by an interaction

integral. The equivalent stress intensity factor is computed

by Eq. (14). The expressions for the J-integral and the inter-

action integral as domain integrals can be found in [28].

An explicit algorithm is used to satisfy both Eqs. (11) and

(12). The Equilibrium (11) is discretized and solved for a

prescribed top displacement ¯ u

o

and then the load parameter

λ is adjusted to satisfy Eq. (12), so that the crack with the

maximumstress intensity factor met its critical value. (When

a traction t

o

is prescribed along the top edge, the load param-

eter λ

t

is adjusted to satisfy Eq. (12), so that the crack with

the maximum stress intensity factor met its critical value).

The crack growth increments are set at the beginning of each

step based on a “crack length control” scheme so that the

evolution is controlled by a monotonically increasing func-

tion of the total crack length ∆

tot

, i.e. the sum of all active

crack lengths [49]. In some cases, several cracks are close

to their critical stress intensity factors, the number of n

act

active crack to grow is determined by stability analysis and

a set of competitive crack tips N

comp

is determined as in

Budyn et al. [21]. A stability analysis based on a second var-

iation of the Lagrangian form (4) determines the most stable

crack conﬁguration evolution corresponding to that with the

minimum energy dissipation [21, 22]. The derivatives of the

energy release rate with respect to the crack length [50, 51],

are computed by a generalized X-FEM formulation [21] of

the FEM formulation developed by several authors [52–54].

All subdeterminants of this matrix [∂G

i

/∂

j

] are computed

at time t

n−1

and the maximum subdeterminant gives the set

of tips N

act

that will grow at time step t

n

determined by:

N

act

=

_

i ∈ N

comp

max

{i, j }∈N

comp

det

_

−

∂

2

L(, u)

∂

i

∂

j

__

=

_

i ∈ N

comp

max

{i, j }∈N

comp

det

_

∂ (G

i

(σ

o

))

∂

j

_

≥ 0

_

(17)

The variation of G

i

c

in Eq. (17) vanishes as we consid-

ered strong discontinuities in bone material properties and

G

i

c

constant in each material phase. When multiple cracks

grow at the same time, it can be noted that the Grifﬁth crite-

rion (12) is exactly satisﬁed at the crack when the maximum

stress intensity factor meets its critical value, and approxi-

mately satisﬁed at the other cracks.

3.3 Formulation of the X-FEM displacement ﬁeld

The approximated displacement ﬁeld is discretized by the

eXtended Finite Element Method (X-FEM). The method

describes the cracks with a step function enrichment to repro-

duce the discontinuity of the interior of a crack and uses the

asymptotic near-tip displacement ﬁeld enrichment at the tips

of the cracks [16, 20–22]. Figure 6 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

Fig. 6). K

m

contains the set of corner nodes of the element

that contains the crack tip m enriched by the branch function

123

586 Comput Mech (2008) 42:579–591

(a) (b)

Fig. 6 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

(squared nodes in Fig. 6). N

c

is the set of cracks and N

t

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) [27].

The displacement ﬁeld is based on modiﬁed functions [55]

adapted for multiple crack problems [21] is as follows:

u

h

(x) =

I ∈I

N

I

(x)u

I

+

n

c

n=1

J∈J

n

˜

N

J

(x)a

n

J

¯

H

n

J

(x)

+

n

t

m=1

K∈K

m

˜

N

K

(x)

_

4

l=1

b

m

l K

¯

F

m

l K

(x)

_

(18)

where N

I

(x) are the shape functions for the continuous dis-

placement ﬁeld;

˜

N

J

(x) are the shape functions applied to

the enrichment ﬁeld. This choice of shape functions for the

enrichment ﬁeld is explained in [55, 56]. a

n

J

are the additional

unknowns for the modiﬁed step enrichment

¯

H

n

J

(x) of crack

n and b

m

l K

are the additional unknowns for the tip enrichment

of tip m for the modiﬁed lth branch function

¯

F

m

l K

(x); and x

J

is the position of node J. The modiﬁed enrichment functions

¯

H

n

J

and

¯

F

m

l K

are given in Budyn et al. [21].

3.4 Crack tip reaching a free boundary or another crack

Within each step, the length of each active crack tip is incre-

mented in the direction of the maximum hoop stress as fol-

lows:

∆

i

=

∆

tot

n

act

(19)

where n

act

is the number of active cracks that grow at the

beginning of step n; n

act

is determined by a stability analysis

at the end of step n − 1 described in Eq. (17).

Three possibilities can arise before percolation: (a) a crack

can reach the external free boundary, (b) a crack can reach

the free boundary of an Haverse canal or (c) a crack can coas-

lesce with another crack. In each case, the crack tip is annihi-

lated and its near enrichment removed. This tip is replaced by

either a simple step function for free boundaries or a “junc-

tion” enrichment for bridging cracks derived in Budyn et al.

[21, 22]. For each active crack tip i , we ﬁrst consider a virtual

increment ∆

i

virt

that is set to ∆

i

virt

= ∆

tot

when approach-

ing free boundaries. ∆

tot

is the total crack growth per step. A

more restrictive criterion is chosen to ∆

i

virt

= max(∆

i

, r

i

)

when approaching cracks. ∆

i

is the increment of growth of

Eq. (19) and r

i

is the radius of the domain of computation

of the interaction integral at tip i ; the radius r

i

being about

twice the element length. The length of the added increment

∆

i

is adjusted when the growing crack encounters a free

boundary or another crack so that the tip dies exactly on the

boundary edge.

The direction and location where to join boundaries or

another crack is usually determined by the maximum hoop

stress direction when the mesh is ﬁne. However the direc-

tion is chosen equal to the minimal principal strain direction

in front of the crack tip when the interaction integral cal-

culation does not hold anymore. This situation can occur if

many cracks are interacting or when the domain of calcu-

lation of the interaction integral is largely truncated by an

internal (Haverse canals) or external boundary or contains

another crack (and other phases) in a region where only a

very small amount of brittle material remains. In these cases

the calculation of K

I

and particularly K

II

might be impre-

cise and the direction of the maximum hoop stress incorrect.

However a very small amount of brittle material subjected

to a tensile stress will break and therefore join the bound-

ary or another crack [57–61]. Therefore the local minimal

principal strain will provide the correct growth direction. A

“junction” enrichment is applied when a crack joins another

crack. An extreme case can occur when a crack joins another

crack in the same element where the tip of the connected

crack is located also. In this special junction case, 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. Whenonlyanother 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.

4 Results

We consider square unit cells of cortical bone of speciﬁc

width L given in Table 1. In 3-D a thickness of 0.1 mm was

chosen. Five statistical microstructures were generated for

each patient to attach statistics to the results of the compu-

tations. After initiation the sample geometries are given in

Table 4 and Fig. 7. The cells are loaded under tension in the

y-direction; a positive displacement is prescribed at the top

edge and the displacement in the y-direction is prescribed

123

Comput Mech (2008) 42:579–591 587

Table 4 Geometrical parameters of statistical samples of w02_07,

w03_07 and w10_07

Case 1 Case 2 Case 3 Case 4 Case 5

w02_07

Phase number 89 93 95 95 95

Crack number 54 60 66 61 66

w03_07

Phase number 75 75 71 77 83

Crack number 49 50 46 55 54

w10_07

Phase number 167 157 151 159 157

Crack number 49 38 27 43 45

Fig. 7 Cracks are initiated by an elastic-damage criterion (0.4% ε

max

prime

strain [44]) in the gray regions of Fig. 5. Initiated cracks in blue; crack

growths in red using the X-FEM in w02_07 (a, d, g, j, m), w03_07 (b,

e, eh, k, n)) and w10_07 (c, f, i, l, o)

equal to zero at the bottom edge. The displacement of the

bottomleft corner node in the x-direction is prescribed equal

to zero (see Fig. 2). The material properties are random and

representative of each patient cortical bone microstructure as

described previously.

The force–deﬂection curves, expressed as a nominal stress

versus nominal strain curve for ﬁve samples of each women

2, 3 and 10 are given in Fig. 8. Our analysis is static. The

load deﬂection curves of the three women (Fig. 8) typically

display three phases: in the ﬁrst few steps the cracks are

growing inside the osteons, which produces various degree

of strainhardening; after reachinga peak, one dominant crack

is able to cross through the cement line of the osteon it origi-

natedfrom, anddamage the matrix. Duringthis perioda strain

softening is observed with various degree of severity as the

matrix looses progressively its structural integrity. Finally in

the last steps, the structure has lost most of its strength and

integrity and the cracks will grow towards complete perco-

lation. In the case of w10_07, which is very osteoporotic,

the load deﬂection curve displays a short hardening phase

(Table 5).

For each woman the load–deﬂection curves appear rela-

tively consistent in Fig. 8 and Table 6 with a relatively nar-

row standard deviation. Note that for the crack initiation, a

mesh reﬁnement would not affect their initial locations but

slightly reﬁne their initial lengths. The effect of the mesh

reﬁnement for the continuum and the cracks would smooth

the load-defection contour and the crack paths; this phenom-

enon has been demonstrated in a convergence study in Budyn

et al. [21].

Table 6 and Fig. 8 showw02_07 fracture strength is about

one third higher than w03_07 fracture strength despite these

two samples exhibit similar macroscopic moduli in Table 3.

w03_07 has a higher osteonal fraction and slightly higher

porosity but a lower osteonal density than w02_07. There-

fore w03_07 has larger osteons. In Table 2, we also note

that w02_07 has a higher osteons/matrix modulus contrast

and appears more heterogeneous. This would correlate of the

observation of the beneﬁcial structural function of cement

lines on the fracture strength in Budyn et al. [46]. In the for-

mer study it was noticed that in the absence of cement lines

the osteons tend to transfer more deformation to the matrix.

With cement lines, the osteons remain conﬁned and exhibit a

wider range of deformations. This phenomenon can partially

explain the hardening phase observed in the global behav-

ior due to primary growth of cracks inside more numerous

osteons before damaging the matrix. We observe that more

inhomogeneity makes the response richer and contribute to

strengthen the structure. Therefore cement lines and numer-

ous osteons appear as critical elements in the protection of

bone against fracture as some experimental observation of

the effect of cement lines as osteonal barriers can be seen

in Mohsin et al. [10]. However w02_07 exhibits a steeper

123

588 Comput Mech (2008) 42:579–591

0 1 2 3 4 5

0

20

40

60

80

100

120

140

160

nominal strain (%)

n

o

m

i

n

a

l

s

t

r

e

s

s

(

M

P

a

)

w02t1_07

w02t2_07

w02t3_07

w02t4_07

w02t5_07

(a)

0 1 2 3 4 5

0

20

40

60

80

100

120

140

160

nominal strain (%)

n

o

m

i

n

a

l

s

t

r

e

s

s

(

M

P

a

)

w03t2_07

w03t3_07

w03t4_07

w03t5_07

w03t6_07

(b)

0 1 2 3 4 5

0

20

40

60

80

100

120

140

160

nominal strain (%)

n

o

m

i

n

a

l

s

t

r

e

s

s

(

M

P

a

)

w03t2_07

w03t3_07

w03t4_07

w03t5_07

w03t6_07

(c)

Fig. 8 Global stress–strain response in w02_07, w03_07 and w10_07

softening phase than w03_07. Despite having a lesser num-

ber of phases, w03_07 osteonal volume fraction is higher

than in w02_07 and might play a role in slowing down the

Table 5 Fracture strengths of the statistical samples of w02_07,

w03_07 and w10_07

σ

u

(MPa) Case 1 Case 2 Case 3 Case 4 Case 5

w02_07 109.2 144.5 152.6 131.3 127.0

w03_07 112.7 116.7 81.6 77 95.9

w10_07 56.2 50.9 47.9 70.9 49.4

Table 6 Average fracture strengths of w02_07, w03_07 and w10_07

Specimen w02_07 w03_07 w1_07

Numerical strength (MPa) 132.7 101.7 55.4

Standard deviation (MPa) (14.98) (12.52) (8.24)

Experimental strength (MPa) 92 95 low

softening process. On the other hand, w10_07 displays an

significantly higher porosity than the other two women,

which contributes to a lower modulus (Table 3) and lower

fracture strength(Tables 5, 6; Fig. 8). Despite a relativelyhigh

osteonal volume fraction and a high osteon density, w10_07

exhibits almost no hardening but a relatively slow softening.

The numerical fracture strength of w03_07 is in close agree-

ment with the experimental measurements in Table 6. The

numerical fracture strength of w02_07 agrees to some extend

with the experimental measurement performed on this highly

variable biological tissue for which more experimental tests

are scheduled.

5 Conclusion

The results of this preliminary human study present a direct-

simulation “multiple scale” approach to describe fracture in

Haversian cortical bone microstructures under tension. The

human Haversian microstructure is discretized by a statisti-

cal ﬁnite element model to investigate the inﬂuence of the

local patient morphological and mechanical parameters of

the microstructure on its mechanical behavior. The majority

of these parameters were based on physical data, however

some limitations can be given. For the geometrical descrip-

tion the osteons are modeled by disjoint elliptical tubes,

which is an idealized geometry and does not allow them

to connect to each other through Volkman canals [62]. We

study bone at the osteonal level and do not include osteocyte

lacunae [15, 63]. We also modeled interstitial matrix as

homogeneous material. Our study focused on the effect of the

heterogeneities density and size ratio on the microstructure

fracture strength. Other heterogeneities such as cement line

thickness, matrix heterogeneities (remodeling), etc., inﬂu-

ence the crack paths and will be studied in further work.

123

Comput Mech (2008) 42:579–591 589

Improvement in the implementation of the boundary

conditions might also impact the smoothness of the global

response.

The X-FEM is particularly suitable for crack growth in

heterogeneous media because remeshing is avoided. For

accuracy purposes, higher order elements, which are qua-

dratic for the standard displacement ﬁeld and linear for the

enrichment, have been applied. In contrast to boundary

element methods, the method easily handles microstructure

heterogeneities. The method applied to static crack growth

is explicit and satisﬁes exactly both the equilibrium (11) and

the Grifﬁth criterion (12) at each step of the load deﬂec-

tion curve. Astability analysis based on energy consideration

enables us to solve the case of competitive crack growth. The

response of the unit cell is tracked until almost complete fail-

ure when the cracks have joined and reached the free bound-

aries and almost percolated the cell. In the present model we

triedtoimplement boundaryconditions close toexperimental

testing.

The model accesses two different scales: the material

(macro) scale at the unit cell level and the (micro) scale inside

the material for the strainﬁeldinside the osteons, ina mimetic

osteonal microstructure. At the macroscopic scale, the model

provides the overall response and thus the fracture strength

of the material. The present “multi-scale” model shows the

inﬂuence of the local geometrical and mechanical properties

of the microstructure on the macroscopic properties of cor-

tical bone [34], which are the only accessible information in

clinical medical studies [64, 65]. The model shows in particu-

lar howtwo patients (2 and 3) exhibiting similar macroscopic

stiffness, display different fracture strength and failure paths

in tension. The model helps to build a constitutive stress–

strain law at the material scale that can be coupled later on to

a higher and/or lower scale(s) for more complex multi-scale

approaches.

At the microscopic level, even if the matrix is homoge-

neous its strain ﬁeld is not. Our results show how morpho-

logical and mechanical heterogeneities inﬂuence the local

strain ﬁeld and on the macroscopic response. Previously

in [22] cement lines, less stiff but tougher, have been shown

to play an important role in isolating the osteons from the

matrix, explaining only partially why cement lines are impli-

cated with energy in fracture processes in the deﬂection of

crack propagation by slowing it down [66] or debonding the

osteon [67]. Our present results suggest how critical Haver-

sian porosity is source of localization and fracture nucle-

ation for transversal tension loading. The model also shows

how an increase in morphlological (high osteon density) and

mechanical (harder matrix) heterogeneities tend to increase

the hardening phase and the fracture strength. Therefore low

remodeling activity that reduces osteon density lowers the

macroscopic fracture strength. The model shows how high

porosity and large osteons in osteoporosis contribute to lower

the macroscopic moduli and the fracture strength and shorten

strain hardening. Finally the model tends to suggest that high

osteonal volume fractionseems toextendthe softeningphase.

However further investigations on more patients are sched-

uled to reﬁne the understanding between the effects of osteon

density and osteonal volume fraction on the load deﬂection

response.

In summary, this model presents preliminary results that

characterize the local properties of human cortical bone and

emphasizes the importance of the microstructural constitu-

ents (porosity, osteonal fraction and density, cement lines,

etc.) to prevent the progression of localized damage zones

and cracks in healthy bone. Any pathological modiﬁcations

of these constituents alters the integrity of the microstruc-

ture. While some of the alterations are detectable at the mac-

roscopic scale such as a loss in stiffness, however degra-

dation of the fracture strength are not detectable by conven-

tional clinical tools. Our model proposes alternative means to

investigate such properties and diagnose pathologies. More

experimental validations will be developed for this type of

numerical approach. Further investigations include the phys-

iological and mechanical properties of the cement lines and

the matrix to feed this model with more experimental damage

and fracture parameters in tension and compression loading

for a more complete 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 and the CNRS.

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