Computational simulation of the bone remodeling using the finite element method: an elasticdamage theory for small displacements
 Ahmed Idhammad^{1}Email author,
 Abdelmounaïm Abdali^{1} and
 Noureddine Alaa^{1}
https://doi.org/10.1186/174246821032
© Idhammad et al.; licensee BioMed Central Ltd. 2013
Received: 24 March 2013
Accepted: 14 April 2013
Published: 13 May 2013
Abstract
Background
The resistance of the bone against damage by repairing itself and adapting to environmental conditions is its most important property. These adaptive changes are regulated by physiological process commonly called the bone remodeling. Better understanding this process requires that we apply the theory of elasticdamage under the hypothesis of small displacements to a bone structure and see its mechanical behavior.
Results
The purpose of the present study is to simulate a two dimensional model of a proximal femur by taking into consideration elasticdamage and mechanical stimulus. Here, we present a mathematical model based on a system of nonlinear ordinary differential equations and we develop the variational formulation for the mechanical problem. Then, we implement our mathematical model into the finite element method algorithm to investigate the effect of the damage.
Conclusion
The results are consistent with the existing literature which shows that the bone stiffness drops in damaged bone structure under mechanical loading.
Keywords
Bone remodeling Damage Elasticity Small displacements hypothesis Bone density Femur Finite element Variational formulation Biomechanics Computation simulationIntroduction
Bone is the main constituent of the skeletal system enable to maintain substantially the shape of the body; to protect the internal organs; to store minerals and lipids; to participate in blood cell production; and to assist body movements by transmitting the force of muscular contraction from one part to another [1].
As a living tissue, bone is able to optimize its structure by redistributing its density under the influence of external forces. Since this publication of Wolff, many theories describing the redistributing of the bone density have been proposed [2–4].
This process, called bone remodeling, was formally developed later by Huiskes et al. using the concept that bone remodeling is induced by a local mechanical signal which activate the regulating cells and cause local bone adaptations [5, 6].
However, when external forces are above a critical level, bone may become more susceptible to fracture by increasing the damage formation which is normally repaired [7, 8].
Therefore, better understanding of bone remodeling process helps to prevent fractures and other kinds of diseases. Several works have been made to relate bone remodeling process to a mathematical point of view, and thereafter perform some computational simulations [6, 7].
The overall aim of this study is to numerically simulate the proximal femur using an elasticdamage theory for small displacements. First, we describe the mechanical problem and we derive its variational formulation. Next, we propose a bone remodeling algorithm and we solve a twodimensional femur problem by using the finite element method.
Finally, some twodimensional computational simulations are presented, and the results are in clear agreement with those reported in literature.
Background
Geometry and material properties
where M and γ are positive constants.
Elasticdamaged bone remodeling theory
The femur can be remodeled in response to external loads to give greater bone matrix in regions that are subjected to higher levels of stress. These external loads induce changes in the mechanical fields and damage to the femur, such as macro cracks or micro cracks [14, 15].
This concept of damage was developed in the 1990s by the scientific community and particularly by Kachanov [16]. The elasticdamage model used in this contribution was initially developed by the French school and notably that of Jean Lemaitre [17, 18]. It describes the constitutive behavior of the material by introducing a scalar variable D which quantifies the influence of microcracking.
Where:
D is the degree of damage with 0 ≤ D ≤ 1
E is Young’s modulus of undamaged elasticity
is the actual modulus of damaged elasticity. The damage is then expressed as the loss of stiffness.
Where:
ρ_{min} the minimal density corresponding to the reabsorbed bone
ρ_{max} the maximal density of cortical bone
Moreover, let ρ_{0} denote the initial bone density
Where:
D_{0} is the initial damage
t is the time
f_{d} is the fatigue life of the bone devoid of the remodeling
Governing equations
Let , be a nonempty open bounded domain in with a Lipschitzcontinuous boundary Γ = ∂ Ω. The boundary is split into two disjoint parts Γ_{1} and Γ_{2} where Γ_{1} is a fixed part of the border on which the femur is fixed, and Γ_{2} is also a part of the border, on which the forces F (F1, F2) are applied.
Everywhere below we use to denote the space of second order symmetric tensors and denote by n the unit outer normal vector to Γ. To simplify, we consider that the body occupying the set isn’t being acted upon by a volume force of density f. Subsequent to modeling, both loads and boundary conditions are defined.
Finally, let be the displacement field, the stress field, strain tensor, the bone density function and T > 0 the time duration.
Here ∇ stands for the gradient operator.
Where:
Div represents the divergence operator
l denotes the identity operator in
are Lame’s coefficients, which are assumed to depend on the bone density denoted by
with:
Many laws of bone remodeling have been published in the world mainly targeting the evolution of the bone density [5, 6, 20]. We adopt the law suggested by Huiskes et al. who used the strain energy density as the stimulus signal to control bone remodeling process [5, 6, 20, 22].
where:
B, s and K are experimental constants
Let: be the double contraction of two tensors which yields a scalar.
Finally, equation system of the problem is defined as follows.
Where
Variational formulation
The variational formulation of this model consists in a variational equation for the displacement field.
Where v is the test functions.
Time discretizations
∆t is the time step size
The proposed algorithm

Step 1. Define the global model: geometry, load conditions and initial bone density distribution. The remodeling is considered for initial model with a uniform density distribution of ρ_{0} = 0.8 g/cm^{3}.

Step 2. Determine Young’s modulus, Poisson’s ratio and Lame’s coefficients.

Step 3. Calculate the displacement, by solving the linear variational equation of the displacement field.

Step 4. Evaluate the strain energy density U at each discrete location using the finite element method.

Step 5. Justify if the mechanical stimulus would cause bone apposition, bone resorption or equilibrium. Then, update the bone density.

Step 6. Update the damage.

Step 7. Check for convergence. The convergence criterion is imposed according to the change in mass during the iterative process. The final topology is obtained when the convergence criterion is satisfied; otherwise, the iterative process continues from Step 2.
Results and discussion
As is wellknown, it is of significance to explore the biomechanical behavior of bone. This work is aimed to simulate an elasticdamage femur in order to provide useful information on the geometrical topology and material properties of bone.
The following data [7, 9, 19, 20, 22, 24] are employed:
ρ_{min} = 0.01 g/cm^{3}, ρ_{max} = 1.74 g/cm^{3}, K = 0.004 J/g, s = 0.1, ρ_{0} = 0.8 g/cm^{3}, γ = 3, B = 1( g/cm^{3})^{2}(MPa. UT)^{ 1}, D_{0} = 0.8, f_{d} = 3 years, f = 0 N/m^{2}, Δt = 10^{ 5}UT, υ = 0.3, M = 3790 (Mpa)( g/cm^{3})^{ 3}, (F_{1}(case1) = 1000 N, F_{2}(case1) = 1200 N), (F_{1}(case2) = 1200 N, F_{2}(case2) = 1500 N).
Several computational simulations are developed concerning bone remodeling of a proximal femur during mechanical stress, assuming the imposition of an elasticdamage in the domain. Also, we take a steady force and fixed constraint as the boundary condition of this model. The proposed algorithm described before is implemented in FreeFEM++ (see [26]), executing multiple simulations for different load cases. Two load cases are considered to evaluate their effect on the density distribution of bone.
Shown in Figure 4(a) is the undamaged bone density distribution from initial time to final time. It can be seen that mechanical loading triggers the process of bone remodeling particularly in the area close to the load. In this area, the bone density is high compared to other areas.
Figure 4(b) plots the changes in the density distribution of damaged bone from initial time to final time. It results the increase in the rate of density during the initial time, and after that it gradually decreased. But it never reaches the density of an undamaged bone.
The results of the study demonstrate that in the area close to the mechanical load, the bone density is higher than normal; and in the area remote from the mechanical load, the bone density is lower than other areas. The results are similar to those obtained by Li et al. [23], Sharma et al. [24] and Li et al. [27].
Comparing Figures 4 and 5, it is possible to observe that the decrease in bone density further leads to decrease in bone stiffness in terms of Young’s modulus, so to an increased risk of fracture. The same results were observed in the works of Tomaszewski et al. [28].
From this comparison, we showed that in a bone, the density decreases in a damaged structure at the initial time, then it can repair the damage itself to some extent at the final time. But this can only happen if the loading isn't so high that the selfrepair mechanism can keep pace with the increasing damage [7, 14, 29, 30].
The selfrepair mechanism in this case is taken into account only the mechanical stimulus, although existing of many biological factors such as immunological, hormonal and haemodynamical stimulus; thus varying from one individual to another [24, 27, 31].
The work presented here may be applied to different models as well as to studies of orthopedic biomaterials and be helpful in further investigations.
Conclusion
In the present study, a model simulating elasticdamage bone remodeling is presented by using a twodimensional mathematical model and a numerical technique based on the finite element method. The effects of both strain and damage in bone structure have been examined.
The results presented in this paper show that in the solicited area, the bone density is important; and allowed us to observe a good agreement with literature findings.
Hence, from a biomechanical perspective it is better to simulate three dimensional femur bone by using the finite element method in order to obtain better understanding of the behavior of the bone.
Declarations
Acknowledgements
We are particularly grateful to the editor in chief, Dr. Paul S. Agutter, for his insightful suggestions and support.
Authors’ Affiliations
References
 Cowin SC: Bone Mechanics Handbook. 2001, USA: CRC Press, Boca Raton, FL, 2Google Scholar
 Wolff J: Das Gesetz der Transformation der Knochen. 1892, Hirschwald: Hirschwald BerlinGoogle Scholar
 Frost HM: The Laws of Bone Structure. 1964, Springfield: Thomas CCGoogle Scholar
 Firoozbakhsh K, Cowin SC: An analytical model of Pauwels’ functional adaptation mechanism in bone. J Biomech Eng. 1981, 103: 246252. 10.1115/1.3138288.View ArticlePubMedGoogle Scholar
 Mullender M, Huiskes R, Weinans H: A physiological approach to the simulation of bone remodeling as self organizational control process. J Biomech. 1994, 27: 13891394. 10.1016/00219290(94)900493.View ArticlePubMedGoogle Scholar
 Huiskes R, Weinans H, van Rietbergen B: The relationship between stress shielding and bone resorption around total hip stems and the effects of flexible materials. Clin Orthop Relat Res. 1992, 274: 124134.PubMedGoogle Scholar
 Doblaré M, Garcıa JM, Gomez MJ: Modelling bone tissue fracture and healing: a review. Eng Fract Mech. 2004, 71: 18091840. 10.1016/j.engfracmech.2003.08.003.View ArticleGoogle Scholar
 Martin RB: Fatigue damage, remodeling, and the minimization of skeletal weight. J Theor Biol. 2003, 220: 271276. 10.1006/jtbi.2003.3148.View ArticlePubMedGoogle Scholar
 Weinans H, Huiskes R, Grootenboer HJ: The behavior of adaptive boneremodeling simulation models. J Biomech. 1992, 25: 14251441. 10.1016/00219290(92)900567.View ArticlePubMedGoogle Scholar
 Jacobs CR, Marc EL, Gary SB, Juan CS, Dennis RC: Numerical instabilities in bone remodeling simulations: The advances of a nodebased finite element approach. J Biomech. 1994, 28: 449459.View ArticleGoogle Scholar
 Op Den Buijs J, DragomirDaescu D: Validated finite element models of the proximal femur using twodimensional projected geometry and bone density. Comput Methods Programs Biomed. 2011, 104: 74168.View ArticleGoogle Scholar
 Currey JD: The effect of porosity and mineral content on theYoung’s modulus elasticity of compact bone. J Biomech. 1988, 21: 131139. 10.1016/00219290(88)900061.View ArticlePubMedGoogle Scholar
 Carter DR, Hayes WC: The compressive behavior of bones as a twophase porous structure. J Bone Joint Surg Am. 1977, 59: 954962.PubMedGoogle Scholar
 Taylor D, Hazenberg JG, Lee TC: Living with cracks: Damage and repair in human bone. Nature Materials. 2007, 6: 263268. 10.1038/nmat1866.View ArticlePubMedGoogle Scholar
 Dunlop JWC, Hartmann MA, Brechet YJ, Fratzl P, Weinkamer R: New suggestions for the mechanical control of bone remodeling. Calcif Tissue Int. 2009, 85: 4554. 10.1007/s002230099242x.PubMed CentralView ArticlePubMedGoogle Scholar
 Kachanov LM: Introduction to Continuum Damage Mechanics. 1986, The Netherlands: Dordrecht, Martinus Nijhoff PublishersView ArticleGoogle Scholar
 Lemaitre J, Chaboche JL: Mechanics of solid materials. 1990, UK: Cambridge University PressView ArticleGoogle Scholar
 Lemaitre J, Desmorat R: Engineering Damage Mechanics. 2005, Berlin: SpringerGoogle Scholar
 Idhammad A, Abdali A, Bussy P: Numerical simulation of the process of bone remodeling in the context of damaged elastic. Int J Adv Sci Tech. 2011, 37: 8798.Google Scholar
 Idhammad A, Abdali A: On a new law of bone remodeling based on damage elasticity: a thermodynamic approach. Theor Biol Med Model. 2012, 9: 5110.1186/17424682951.PubMed CentralView ArticlePubMedGoogle Scholar
 Wang HF: Theory of Linear Poroelasticity with Applications to Geomechanics and Hydrogeology. 2000, NJ: Princeton University PressGoogle Scholar
 Tovar A: Bone Remodeling as a Hybrid Cellular Automaton Optimization Process. 2004, USA: PhD thesis, University of Notre DameGoogle Scholar
 Li W, Lin D, Rungsiyakull C, Zhou S, Swain M, Li Q: Finite element based bone remodeling and resonance frequency analysis for osseointegration assessment of dental implants. Finite Elem Anal Des. 2011, 47: 898905. 10.1016/j.finel.2011.03.009.View ArticleGoogle Scholar
 Sharma GB, Debski RE, McMahon PJ, Robertson DD: Adaptive glenoid bone remodeling simulation. J Biomech. 2009, 42: 14601468. 10.1016/j.jbiomech.2009.04.002.View ArticlePubMedGoogle Scholar
 Coelho PG, Fernandes PR, Rodrigues HC, Cardoso JB, Guedes JM: Numerical modeling of bone tissue adaptation  A hierarchical approach for bone apparent density and trabecular structure. J Biomech. 2009, 42: 830837. 10.1016/j.jbiomech.2009.01.020.View ArticlePubMedGoogle Scholar
 Hecht F, Le Hyaric A, Ohtsuka K, Pironneau O: Freefem++, finite element software. [http://www.freefem.org/ff++/]
 Li J, Li H, Shi L, Fok AS, Ucer C, Devlin H, Horner K, Silikas N: A mathematical model for simulating the bone remodeling process under mechanical stimulus. Dent Mater. 2007, 23: 10731078. 10.1016/j.dental.2006.10.004.View ArticlePubMedGoogle Scholar
 Tomaszewski PK, Verdonschot N, Bulstra SK, Rietman JS, Verkerke GJ: Simulated bone remodeling around two types of osseointegrated implants for direct fixation of upperleg prostheses. J Mech Behav Biomed Mater. 2012, 15: 167175.View ArticlePubMedGoogle Scholar
 Hambli R, Lespessailles E, Benhamou CL: Integrated remodelingtofracture finite element model of human proximal femur behavior. J Mech Behav Biomed Mater. 2013, 17: 89106.View ArticlePubMedGoogle Scholar
 Lee TC, Staines A, Taylor D: Bone adaptation to load: microdamage as a stimulus for bone remodelling. J Anat. 2002, 201: 437446. 10.1046/j.14697580.2002.00123.x.PubMed CentralView ArticlePubMedGoogle Scholar
 Pandorf T, Haddi A, Wirtz DC, Lammerding J, Forst R, Wechert D: Numerical simulation of adaptive bone remodeling. J Theor Appl Mech. 1999, 37: 639658.Google Scholar
Copyright
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.