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e-mail: jangin@me.queensu.ca

Il Yong Kim1

e-mail: iykim@me.queensu.ca

Department of Mechanical and Materials

Engineering,

Queens University,

McLaughlin Hall 221,

130 Stuart Street

Kingston, ON, K7L 3N6, Canada

Department of Mechanical Engineering,

Korea Advanced Institute of Science and

Technology,

373-1 Guseong-dong, Yuseong-gu

Daejeon 305-701, South Korea

e-mail: bmkwak@khp.kaist.ac.kr

Based Bone-Remodeling

Algorithm and Structural

Topology Optimization

In bone-remodeling studies, it is believed that the morphology of bone is affected by its

internal mechanical loads. From the 1970s, high computing power enabled quantitative

studies in the simulation of bone remodeling or bone adaptation. Among them, Huiskes et

al. (1987, Adaptive Bone Remodeling Theory Applied to Prosthetic Design Analysis, J.

Biomech. Eng., 20, pp. 11351150) proposed a strain energy density based approach to

bone remodeling and used the apparent density for the characterization of internal bone

morphology. The fundamental idea was that bone density would increase when strain (or

strain energy density) is higher than a certain value and bone resorption would occur

when the strain (or strain energy density) quantities are lower than the threshold. Several

advanced algorithms were developed based on these studies in an attempt to more accurately simulate physiological bone-remodeling processes. As another approach, topology

optimization originally devised in structural optimization has been also used in the computational simulation of the bone-remodeling process. The topology optimization method

systematically and iteratively distributes material in a design domain, determining an

optimal structure that minimizes an objective function. In this paper, we compared two

seemingly different approaches in different fieldsthe strain energy density based boneremodeling algorithm (biomechanical approach) and the compliance based structural

topology optimization method (mechanical approach)in terms of mathematical formulations, numerical difficulties, and behavior of their numerical solutions. Two numerical

case studies were conducted to demonstrate their similarity and difference, and then the

solution convergences were discussed quantitatively. DOI: 10.1115/1.3005202

Keywords: bone remodeling, bone adaptation, topology optimization, computational

simulation

Introduction

self-optimizing capabilities and therefore is able to control its

mass and structure according to its mechanical demands. From the

1970s, the advance of computer capabilities and numerical stress

analysis methods has allowed for the quantitative study of bone

remodeling. Cowin and Hegedus 1 proposed the first quantitative bone-remodeling equations based on continuum mechanics.

Fyhrie and Carter 2 postulated that bone adaptively changes its

structure and density in response to its stress and strain state.

Huiskes et al. 3 proposed another remodeling algorithm based

on the assumption that strain energy density SED acts as the

stimulus for bone density change. In these approaches, the rate of

the bone density change is determined on the basis of the difference between the remodeling stimulus e.g., stress, strain, and

strain energy density and its target value. A number of different

approaches have been proposed afterwards 47.

In the aforementioned studies, the behavior of the bone structure is described by a set of differential equations, and the bone

may be considered as a nonlinear system with a certain number of

degrees of freedom, which is the same as the number of finite

elements in the analysis domain. It is interesting to note that these

1

Corresponding author.

Contributed by the Bioengineering Division of ASME for publication in the JOURNAL OF BIOMECHANICAL ENGINEERING. Manuscript received January 14, 2008; final

manuscript received July 18, 2008; published online November 26, 2008. Review

conducted by Ellen M. Arruda. Paper presented at the 21st Canadian Congress of

Applied Mechanics, 2007.

elementwise differential equations may be replaced by a domainwide objective function in optimization. A similar relationship is

found in Newtonian mechanics, in which the equilibrium state of

objects is obtained by solving the simultaneous governing equations, and the same equilibrium can also be determined by minimizing the energy state of the objects 8.

In mechanical engineering, there has been a significant progress

in structural optimization, which is often classified into size,

shape, and topology optimization. Among these methods, topology optimization iteratively redistributes material in the domain to

determine an optimal material arrangement 911. Since the

1990s, topology optimization has been successfully applied to the

simulation of bone remodeling. Hollister et al. 12 used the homogenization method to obtain microtrabecular bone architecture.

Fernandes and Rodrigues 13 used a weighted sum of strain energy and mass as the objective function in topology optimization

to simulate bone remodeling around cementless hip stems. Bagge

14 used topology optimization with compliance minimization to

determine the initial material distribution for proximal femur.

Huiskes 15 summarized this observation: It has been shown

that computer algorithms for material design optimization, when

given the opportunity, show the tendency to produce trabecular

patterns, similar to bone. These studies provided insight into

bone as an optimized structure, but they rested on the assumption

without any solid foundation of theoretical proof.

Even though it is well known by experience that the two seemingly different approaches in different fieldsthe elementwise

bone-remodeling algorithms and the structural topology optimization with a domain-wide objective functionproduce similar re-

sults, it has not been thoroughly studied how these two approaches are compared explicitly: In terms of mathematical

formulations, numerical difficulties and their remedies, and behavior of their numerical solutions. Only a few studies tried to

derive the relationships between the two methods. Harrigan and

Hamilton 16 formulated a global functional for the simulation of

bone remodeling as the weighted sum of mass and the total strain

energy. They showed that the role of the functional was equivalent

to that of the remodeling equation developed by Huiskes and coworkers 5,6. Subbaraya and Bartel 17 also suggested the same

global functional for local bone-remodeling phenomenon. In the

aforementioned studies, the proposed global functional was totally

equivalent to the bone remodeling equation by Huiskes et al.

However, the simulations based on this functional are unconstrained optimization tasks, and they are different from the typical

topology optimization with a mass constraint that has been used

most widely in various applications including bone-remodeling

simulation. The analogy between this standard topology optimization with a mass constraint and the stain energy based boneremodeling equations has not been studied, and the relationships

between the topology optimization parameters and the boneremodeling equation variables are not yet identified.

In this paper, we formulated the typical form of topology optimization starting from the global functional by Harrigan and

Hamilton 16 and investigated the similarities and differences

between this topology optimization and the strain energy density

based approach in terms of mathematical formulations and numerical implementations. We then determined the matching relationships among the parameters used in the topology optimization

and bone-remodeling algorithm. Two numerical examples were

solved using the two approaches and the behavior of each numerical convergence was discussed.

and Topology Optimization

In the 1990s, macroscopic continuum models for bone remodeling were developed, in which the entire domain was discretized

into a number of design cells, and mechanical variables and biological responses were spatially averaged to yield appropriate apparent variables over the region of each design cell. Indeed all the

bone-remodeling algorithms aforementioned were developed

based on this approach. It is interesting to note that the same

approach has been used in topology optimization. This cell-based

approach has been very widely used in topology optimization.

The second similarity between bone remodeling and topology

optimization is the relationship between the density and Youngs

modulus E. In topology optimization with the solid isotropic material with penalization SIMP approach 10, which is one of the

most popular methods nowadays, an artificial relationship between the density and Youngs modulus is used based on a power

law. The relationship between and E of bone in bone remodeling

5,6 is the same as that of the SIMP model in topology optimization; the mathematical expression is

E = c

constants to be selected.

Third, we gain insight into the behavior of a major state variable over computational iterations in bone-remodeling simulations

and topology optimization. Energy stored in each cell is used as a

state variable in the SED-based bone remodeling equations. As

remodeling progresses, the distribution of the stored energy over

the entire domain becomes more uniform. In structural topology

optimization, the ideal optimum design has the fully stressed

state where all the parts of a structure can be used most efficiently.

In an actual case, however, the optimum solution would not have

a completely constant stress distribution, but the variance in stress

distribution always decreases as optimization progresses.

Finally, it is also worth noting that the SED-based boneremodeling approaches and the topology optimization methods

have the same numerical difficultiescheckerboard patterns and

solution dependency on mesh resolutionand moreover the remedies used in each area are similar although the numerical techniques were developed independently. Weinans et al. 5 found

checkerboard patterns and mesh dependency in their numerical

bone-remodeling simulations. They used the terms patchwork effect for checkerboard pattern and chaotic phenomena for mesh

dependency. To overcome checkerboard patterns in bone remodeling, Jacobs et al. 18 suggested the use of quadratic elements

over bilinear elements and also the use of node-based approach;

these two remedies were also used in the same way in topology

optimization 19,20. More active schemes were developed to resolve the numerical difficulties: Mullender et al. 6 introduced the

influence area of sensors, and similar techniques were developed in topology optimization with the name of sensitivity filtering 21. Mathematical equations of these techniques are presented in Sec. 3.

Mathematical Formulations

Density Based Approach. It is believed that the mass and form of

bone are determined based on the two processesosteoclast resorption and osteoblast formationand the processes are modulated by external loads through osteocytic sensing and signaling.

To consider this biological phenomenon in numerical simulation,

Weinans et al. 5 assumed that a difference between the actual

SED, S = Sx , y , z, and a reference SED, k = kx , y , z, at the same

location was the driving force for adaptation of the apparent density. The stimulus was then approximated by U / , where U is the

apparent SED in the bone and is the apparent density. They

proposed a bone-remodeling equation for multiple load cases:

d j

Ua,j

k ,

=B

dt

j

0 j upper

strain energy density of the jth element. Here,

n

Ua,j =

1

Ui,j

n i=1

where Ui,j is the apparent strain energy density of the jth element

for load case i, and n is the number of load cases. The relation

between Youngs modulus and the density was taken as in Eq. 1.

Usually, in Eq. 1 has a value of 2 or 3. The remodeling process

is considered to converge when d / dt becomes zero in Eq. 2 or

when the density reaches the lower or upper bound.

To make the bone-remodeling process more physiological i.e.,

no checkerboards or no mesh dependency, Mullender et al. 6

introduced a spatial influence function fx to Eq. 2:

d

=

dt

f x

N

Ua,j

j=1

k ,

0 upper

dist x , j the distance between sensor j and location x. They assumed that sensor cells were uniformly distributed over its volume.

3.2 Structural Topology Optimization With Compliance

Minimization. In this section, we will show that the SED-based

bone-remodeling algorithm, which was devised in biomechanics,

can be matched mathematically with the topology optimization

formulation. We will then reveal the relations among the constants

used in the SED-based bone-remodeling algorithm and topology

optimization. We will also discuss how the sensitivity filtering in

topology optimization is compared to the spatial influence func-

Harrigan and Hamilton 16 formulated a global functional for

the simulation of bone remodeling as the weighted sum of mass

and the total strain energy. They showed that the role of the functional was equivalent to that of the remodeling equation developed by Huiskes and co-workers 5,6. Now, starting from this

global functional as an objective function, we formulate an unconstrained optimization problem under multiple loads as

minimize =

where ui is the displacement vector for load case i, n is the number of load cases, K is the global stiffness matrix of the structure,

j is the jth element density, j is the jth element volume, and N

is the total number of elements. We change Eq. 5 to

2u

n

minimize =

T

i

Kui +

i=1

j j M 0

j=1

where M 0 is a constant. Since Eq. 6 is different only by a constant from Eq. 5, they have the same sensitivity and therefore

they will produce the same optimum solutions.

The strain energy and mass together will be minimized as much

as possible in Eq. 6, but if we do not need to reduce mass any

further after we meet a prescribed mass target M 0, we can change

Eq. 6 to

minimize =

i=1

1 T

u Kui + P

2 i

P = max 0,

iv i M 0

i=1

P is continuous, ii P 0 for all , and iii P = 0 if and

N

only if i=1

ivi M 0 0. With these properties of P, Eq. 7

can be changed to its mathematically equivalent form of a constrained optimization 8

2u

n

minimize =

T

i

Kui

i=1

subject to

v M

j j

j=1

It is important to note that Eq. 8 is the typical standard problem formulation for structural topology optimization with compliance minimization subject to a mass constraint.

From the equivalent form of topology optimization in Eq. 7,

sensitivity equations are derived into two different cases under the

assumption of linear elasticity and isotropy, as follows:

i

Case 1: Nj=1 j j M 0.

The sensitivity of the objective function with respect to

the density of the eth element is

=

e

2u

n

i=1

T K

ui + e

finite element see Ref. 22 for the details of this derivation. Assuming a constant density distribution within each

finite element in Eq. 9, K j can be written as

Journal of Biomechanical Engineering

10

where L j is the jth element stiffness matrix with unit density. The sensitivity then becomes

=

e

2

n

2

1

1 T

e u i K eu i

i=1

= ne

1

=

n i=1

= ne

Ua,e

+ e

e

1 T

u K eu i

2 i

e

Ua,e

e

n

2u

n

T K

i=1

+ e

Ua,e =

1

Ui,e

n i=1

ii Case 2: Nj=1 j j M 0.

=

e

u iTL eu i + e

i=1

n

1 T

u Kui + j j

2 i

j=1

i=1

K j = j L j

11

ui = ne

Ua,e

e

12

right-hand side of the equation becomes zero, and the topology

optimization progress converges when the right-hand side of Eq.

11 or Eq. 12 becomes zero. When the mass constraint is not

satisfied Case 1, the form of the sensitivity equation the righthand side of Eq. 11 is exactly the same as that of the boneremodeling equation the right-hand side of Eq. 2. When the

mass constraint is satisfied Case 2, however, topology optimization becomes slightly different: The sensitivity equation, Eq. 12,

does not have a threshold value / n anymore, and the sensitivity

will be always negative as long as the mass constraint is met. It

means that there happens no bone osteoclast resorption regardless

of the magnitude of mechanical stimuli in a bone cell, whenever a

mass constraint is satisfied. From this comparison, we find that

topology optimization and the bone-remodeling algorithm will

have the same solutions when the mass constraint in topology

optimization is not met Case 1, but they will have slightly different solutions when the mass constraint is satisfied in topology

optimization Case 2.

By comparing Eq. 2 for bone remodeling and Eqs. 11 and

12 for topology optimization, we discover the mathematical relationships among B, n, , e, k, and :

B = ne

and

k=

13

bone-remodeling algorithm and topology optimization produce

similar results, it has not been investigated how the constants in

the two approaches are mathematically related. This study indeed

for the first time revealed the relationships, as presented in Eq.

13. The multiplier B in the bone-remodeling algorithm is proportional to the number of load cases n, the exponent , and

the element volume e in topology optimization. We also find

that the reference SED k in the bone-remodeling algorithm is

proportional to the weighting factor for the mass constraint

but inversely proportional to the number of load cases n and the

exponent in topology optimization. With the relationship in

Eq. 13, the topology optimization and SED-based bone algorithm will theoretically produce the same solutions in Case 1 and

slightly different solutions in Case 2. Even though the global funcJANUARY 2009, Vol. 131 / 011012-3

the same as the bone-remodeling equation, this study shows that

the typical topology optimization with a mass constraint and the

bone-remodeling equation are not always the same and hence will

not always produce the same solutions; this study examined the

analogy and differences between the two methods depending on

the mass condition.

Sensitivity filtering has been widely used to resolve numerical

instabilities in topology optimization. The original form, proposed

by Sigmund 21, is

g

=

k

1

N

14

j j

j=1

H

j

j=1

= r distk , j,

where g is a functional to be minimized, and H

j

min

j N distk , j rmin, k = 1 , . . . , N.

Incorporating the sensitivity filtering into Eq. 11, we have

=

e

j=1

jH

j

N

j=1

H

j

Ua,j

k =

j

G x,

N

Ua,j

j=1

15

We then realize that the topology optimization sensitivity equation with sensitivity filtering, Eq. 15, is very similar to the boneremodeling equation with a spatial influence function, Eq. 4, in

their form. The main difference is that Gix , in Eq. 15 is a

function of the density as well as the location.

Several researchers have modified the original sensitivity filtering equation, Eq. 14, to improve the performance: By using a

different type of weighting function, by moving a density term in

the denominator inside the summation 23, by dropping the density terms 24, and so on. In this paper, we used an exponential

= edistk,j/D instead of the linear weighting

weighting function H

j

choosing an equivalent filtering radius between different types of

weighting functions and dropped the density terms in Gix , in

Eq. 15 for equivalence.

Numerical Examples

we first tested the plate model of bone tissue 5,6, which has been

frequently investigated in bone remodeling, as shown in Fig. 1.

The plate was meshed with 80 80 bilinear elements. The bone

material was assumed to be isotropic and linear elastic with

= 2 and c = 100 MPa g cm32 in Eq. 1. Poissons ratio was 0.3,

and the maximal density upper was 1.74 g cm3. For a sensor

influence parameter and a sensitivity filtering radius, D

= 0.025 mm was identically used in Eqs. 4 and 15. The initial

density distribution for bone-remodeling simulation and topology

optimization was = 0.8 g cm3 over the entire domain. We applied two load steps to simulate the transformation of morphology

under different loads. When equilibrium was reached in Load Step

1, an additional shear load was applied for Load Step 2. For terminating criterion, the total number of iterations in both load steps

was set 300.

For SED-based bone-remodeling, the constants in the boneremodeling equation, Eq. 2, were B = 1.0 g cm32

MPa time unit1 and k = 0.25 J g1 5,6. We used the forward

Euler integration scheme with a constant time step t = 0.0005 for

Eq. 4 to obtain the optimum results, as shown in Fig. 2a.

For topology optimization, we used the resultant mass of the

bone-remodeling simulation as the mass constraint M 0 in Eq. 8:

4.470 mg for Load Step 1 and 7.490 mg for Load Step 2. We

model of bone tissue: a Load step 1; b load step 2

criteria method 25. It is observed that the optimum results by

model of bone tissue: a Strain energy density based bone

remodeling; b topology optimization

results by the SED-based bone-remodeling algorithm Fig. 2a.

4.2 Vertebral Model. We used the vertebral model 26,27 as

the second numerical example, as shown in Fig. 3. The rectangular plate was meshed with 320 140 bilinear elements. The bone

material was assumed to be isotropic and linear elastic with

= 2 and c = 100 MPa g cm32 in Eq. 1. Poissons ratio was 0.3,

and the maximal density upper was 1.74 g cm3. For a sensor

influence parameter and a sensitivity filtering radius, D

= 0.025 mm was identically used in Eqs. 4 and 15. The initial

density distribution for bone-remodeling simulation and topology

optimization was = 0.8 g cm3 over the entire domain. For terminating criterion, the total number of iterations was set 400. The

physiological loading conditions 28 were considered using

bending moments and compressive load. In this paper, we used

three different load cases: right lateral bending with compressive

load, left lateral bending with compressive load, and pure compressive load. The moment for the left and right bending was

1.36 N m, this bending was implemented by applying a uniformly

distributed shear load on the top edge. In all cases, we applied a

uniformly distributed compressive load of 400 N on the top and

bottom edges 29.

The apparent strain energy density of the jth element was obtained by using weighted summation of the strain energy density

under each load case:

3

Ua,j =

cU

i

i,j

16

i=1

bending, and subscript 3 denotes pure compression. The weighting factors used in this study were c1 = 0.1, c2 = 0.1, and c3 = 0.8.

For SED-based bone remodeling, the constants in Eq. 2 were

B = 1.0 g cm32 MPa time unit1, k = 0.20 J g1 26, and t

= 0.001 for the forward Euler integration scheme. Figure 4a

shows the optimum result.

With the given three load cases, the topology optimization

problem is stated as

c 2u

3

minimize =

T

i

Kui

i=1

subject to

v M

j j

17

j=1

as the mass constraint for Eq. 17: M 0 = 2.6937 g. The same

Journal of Biomechanical Engineering

Fig. 4 Simulation result of structural configuration for a vertebral model: a Strain energy density based bone remodeling;

b topology optimization

Fig. 4b is very similar to the structure obtained by the SEDbased bone-remodeling algorithm.

Discussion

We showed in Sec. 4 that the SED-based bone-remodeling algorithm and topology optimization produced very similar structures for two case studies. To quantitatively compare the progress

during both simulations, we examined the convergence histories

of mass and total strain energy during the simulations, as shown in

Figs. 5 and 6.

First, in terms of total strain energy, the final values in the 300th

iteration were very close, as shown in Figs. 5 and 6: The differences in the plate model of bone tissue were only 0.42% and

3.35% for Load Case 1 and Load Case 2, respectively, and 5.02%

in a vertebral problem.

Second, based on the experimental data from the literature, we

analyzed the mass convergence histories of the two approaches.

Xinghua et al. 30 examined the functional adaptation in long

bones of young and adult cavia porcellus to study the progress of

the bone-remodeling process quantitatively. They found that the

bone adaptation occurred mainly during the first 20 days: 65.30%

during the first 20 days, 26.30% during the second 20 days, and

8.40% during the third 20 days. Xin et al. 31 also studied the

adaptive bone remodeling in terms of the radius increase for adult

cavia porcellus: The radius increase in percentage was 75% during

the first month, 20% during the second month, and 5% during the

third month. In Figs. 5 and 6, we plotted the experimental data by

Xin et al. 31 for the comparison with numerical simulations in

this study. We find that in terms of the remodeling progress in the

time domain, the SED-based bone-remodeling algorithm produced results that are more consistent with the experimental results in the references; however, topology optimization showed

faster convergences.

The faster convergence of topology optimization in mass may

be explained by the priority of the optimization process: If the

initial design violates the mass constraint, satisfying the constraint

has priority over improving the objective function. Another aspect

JANUARY 2009, Vol. 131 / 011012-5

Fig. 5 Convergence history during simulation of a plate model of bone tissue: a Mass change; b total strain energy

change

the time space, but topology optimization is directly derived in the

density space. That is, the SED-based bone-remodeling algorithm

gradually changes the bone density over the time domain; however, topology optimization undergoes a number of sudden big

changes in the density because the optimization algorithm directly

controls the density. It is observed that the topology optimization

is not proper to simulate the physiological remodeling process

obtaining intermediate states; instead, it produces the equivalent

final state more quickly and efficiently. In addition, if we use

topology optimization, we do not need to be concerned about

choosing a proper t, which plays a critical role in the Euler

integration scheme for stable progress in the bone-remodeling algorithm.

There are two main reasons that we obtained slightly different

results between topology optimization and SED-based boneremodeling equation. First, we have different sensitivities in Case

2 where the mass constraint is satisfied. In the plate problem in

Fig. 5a, it is observed that the mass constraint is satisfied with

some margin during the early iterations in Load Step 2 in the case

of topology optimization which is indicated by a few points with

densities smaller than 7.490 mg. This behavior is Case 2, which

is represented by Eq. 12, and during these iterations the topology

optimization progressed differently from the bone-remodeling

can be different even in Case 1. In the case of topology optimization in this paper, we used the optimality criteria method for optimization. It adopts a heuristic update scheme based on theoretical sensitivity information by Eqs. 11 and 12. This update

scheme behaves slightly differently from the direct update algorithm in Eq. 2. In summary, the first factor is entirely based on

the difference in the mathematical formulation, and the second

factor is due to the choice of optimization or update method.

It should be addressed that the solutions by neither topology

optimization nor the bone-remodeling equation necessarily mean

the actual optimum design by the natureif we consider the

biological process as optimization. We considered only mechanical effects for the simulation, but there are other chemical and

biological phenomena that we did not consider in this study.

Moreover, even the mechanical requirements and properties in

bone are not fully understood yet. However, it is also interesting

to observe that the model with only mechanical parameters produce quite physiological results.

In this paper, we compared two different approaches for computational bone-remodeling simulationthe SED-based boneremodeling algorithm and structural topology optimizationfrom

the view point of mathematical formulations, supplementary numerical schemes, and behavior of the numerical solutions. From

problem: a Mass change; b total strain energy change

algorithm, which had been devised in biomechanics, can be mathematically matched with the structural topology optimization

problem. This study also revealed the mathematical relations

among the constants used in the SED-based bone-remodeling algorithm and topology optimization, and examined the analogy and

differences between the two methods depending on the mass condition; this relationship firmly shows that the bone indeed possesses the self-optimizing ability, as hypothesized in the field of

bone remodeling.

Acknowledgment

This work was supported by the Korea Research Foundation

Grant funded by the Korean Government MOEHRD, KRF2006-352-D00004.

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