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On a new law of bone remodeling based on damage elasticity: a thermodynamic approach
Theoretical Biology and Medical Modelling volume 9, Article number: 51 (2012)
Bone tissue is the main element of the human skeleton and is a dynamic tissue that is continuously renewed by bone-resorbing osteoclasts and bone-forming osteoblasts.
The bone is also capable of repairing itself and adapting its structure to changes in its load environment through the process of bone remodeling.
Therefore, this phenomenon has been gaining increasing interest in the last years and many laws have been developed in order to simulate this process.
In this paper, we develop a new law of bone remodeling in the context of damaged elastic by applying the thermodynamic approach in the case of small perturbations.
The model is solved numerically by a finite difference method in the one-dimensional bone structure of a n-unit elements model.
In addition, several numerical simulations are presented that confirm the accuracy and effectiveness of the model.
The bone remodeling process replaces approximately 20% of bone tissue annually; in healthy adults, bone remodeling occurs in a balanced, highly regulated manner in five phases: activation, resorption, reversal, formation, and quiescence as shown in Figure 1[3–5].
This process is assumed to repair the microdamage and maintain bone quality; and also occurs continuously with each cycle lasting 4 to 7 months .
Over the past, the progress made in understanding bone remodeling, through two groups: phenomenological approach and thermodynamic approach, has been truly spectacular.
The thermodynamic approach was initiated first by chemists and was applied to continuum mechanics by Eckart and Biot around 1950. Furthermore, this approach was adopted by introducing state variables [7, 8] and thermodynamic potential which allows to define associated variables chosen for the study of the phenomenon .
In this study, we adopt thermodynamic approach of irreversible processes to get a new law of bone remodeling taking into account the bone density described by the law of Mullender et al.  and the damage evolution in the bone proposed by Martin .
The found equation is solved by the finite difference method (FDM) in the one-dimensional bone structure of a n-unit elements model.
Finally, we present some examples of numerical simulation results.
In order to construct a general framework for the description of the bone remodeling process, the following simplified assumptions are made:
The bone is considered as a linear-elastic, isotropic and inhomogeneous material.
The external mechanical loading acts as a stimulus for bone remodeling.
The n-unit elements model is applied to the damaged-bone structure in the one-dimensional case.
The small perturbations hypothesis (displacements and their time and spatial variations are small).
The state coupling of damage with elastic strain.
The remodeling processes can be considered isothermal, adiabatic and without internal generation of heat.
The decoupling of the thermodynamic potential is assumed, such that:
ψ e (εe, D) is the thermodynamic potential depending on the elastic strain tensor εe and the damage variable D.
ψ r (ϕ) is the thermodynamic potential depending on the bone density ϕ.
The thermodynamics of irreversible processes allows the modeling of different materials behavior. This is accomplished by defining the state variables and the state potential and also the dissipation potential .
A general definition of the thermodynamic forces associated with the internal variables is given by:
Within the hypothesis of small strains and small displacements, the state variables, observable and internal, are chosen in accordance with the physical mechanisms of deformation and degradation of the bone as follows .
– ε is the total strain tensor associated with the stress tensor σ.
– T is the temperature associated with the specific entropy s.
– εe is the elastic strain tensor associated with the stress tensor σ.
– D is the damage associated with a variable .
– ϕ is the bone density associated with the bone remodeling variable R.
We assume a bone remodeling variable, which is characterized by:
R > 0 in the case of the formation phase.
R = 0 in the case of the equilibrium phase.
R < 0 in the case of the resorption phase.
The state potential: ψ = ψ(εe, D, ϕ)
We assume the following decoupling:
ψ e (εe, D) is the thermodynamic potential depending on the elastic strain tensor and the damage variable.
ψ r (ϕ) is the thermodynamic potential depending on the bone density.
The associated variables are defined by:
The development of the Clausius-Duhem inequality
We note that:
(the thermo-elasticity law) 
Inequality (3) may be written :
Using the previous equations (1) (2) (4), we obtain:
In the case of constant damage:
The inequality (5) gives
In the resorption area:
ϕ˙ ≤0 and R<0
In the formation area:
ϕ˙ ≥0 and R>0
Equilibrium area (dead zone):
The conservation of energy equation
The first principle of thermodynamics gives:
– e is the specific internal energy.
– r is the internal heat source.
– q is the heat flux.
and ρ ψ by its expression as a function of the state variables and the associated variables.
We introduce the specific heat (capacity) defined by:
Using the previous equations (6) (7) (8) (9), we can get:
The classical heat equation corresponds to a process: 
Without internal generation of heat created by the external sources: r=0.
With adiabatic evolution: k. ΔT = 0.
With isothermal transformation: Therefore Then s=0.
Equation (10) may be written:
(the strain energy release rate) 
We have also: (the strain energy)  and the equivalent constraint σ eq is written by (The thermo-elasticity law)
With: σ eq = σ in the one-dimensional case.
The Young's modulus of the bone which is an isotropic material and inhomogeneous is expressed as:
c=100 and α =3 are two constants characteristic of the bone
Equation (14) may be written:
This equation represents the new law of bone remodeling developed by applying the thermodynamic approach in the context of damaged elastic.
The evolution law for the damage is expressed as:
f d : the fatigue life of the bone devoid of the remodeling 
D0 : the initial damage
t : the time
Finally, the new law of bone remodeling may be written as:
The new law of bone remodeling (Equation 15) was solved numerically by dividing it into three parts:
a damage function
a function of bone density
In this study, we use the law of bone density proposed by Mullender et al. :
– ϕ min ≤ ϕ ≤ ϕ max
– ϕ min is the density of completely resorbed bone
– ϕ max is the maximum density defined for a compact bone
– τ is a positive constant related to the reaction time of bone tissue (constant of bone remodeling)
– 1≤ i ≤n
– ϕ i density of bone tissue of element i
– m (m ≤ n) is the total number of osteocytes in the solid
– I k (1 ≤ k ≤m) corresponds to the series of numbers of the elements containing an osteocyte
– S k represents the density of deformation energy in I k
– S ref reference stimulus value
– β is a parameter reflecting the intensity of the stimulus cell
– d is the normalization factor limiting the area of influence of osteocyte
– d(i,I k ) is the distance between the centers of geometric element i and the element I k
Results and discussion
We simulated the case of a uniform distribution of the osteocyte cells, and of another heterogeneous case. The values of the parameters used during the numerical simulations are given in Table 3[23, 28].
Numerical results are shown in Figure 4.
Figure 4 shows the temporal evolution of the variable of bone remodeling in the case of a uniform distribution of the osteocyte cells (n=m=50), and of another heterogeneous case (n≠m with m=30 in the central package of the osteocytes).
The curves consists of three key periods. The first period of the curves corresponds to the resorption phase, where the variable of the bone remodeling was negative. The second period exhibits the formation phase, where the variable of the bone remodeling was positive. The third period defined as the interval between the resorption phase and the formation phase, which the variable of the bone remodeling reached zero.
The resorption phase takes approximately 18 days, which is then followed by an equilibrium phase that can last for up to 10 days and finally by the formation phase from 17 to 35 days. This is in agreement with results from the literature [6, 29, 30].
In this paper, we proposed a thermodynamic approach in small perturbations for bone remodeling process.
The adopted model takes into consideration both the bone density and the damage and gives a new law of bone remodeling. Then, the governing equation of the process was solved by the finite difference method in the one-dimensional bone structure with n-unit elements model.
The numerical results obtained are in accordance with the experimental results found in the literature.
Ahmed Idhammad - He received his engineering degree status at the National School of Mineral Industry in Rabat, Morocco. He is curzently a Doctoral student at the Faculty of Sciences and Technics in Marrakech, Morocco. His research interests are numerical simulation, biomechanics, bone remodeling, thermodynamic, fatigue and damage.
Abdelmounaïm Abdali - PhD in Solid Mechanics and Structures in University of Amiens in 1996, France. He is a Professor in computer science at the University Cadi Ayyad, Faculty of Sciences and Technics, Marrakech, Morocco. Member at the Laboratory of Applied Mathematics and Computer Science (LAMAI) Marrakech, Morocco. His research interests are numerical simulation, biomechanics, bone remodeling and damage, computer science, DTN Network.
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We are particularly grateful to the editor in chief Dr. Paul S. Agutter for his thoughtful suggestions for improving the language and style of the manuscript.
We equally thankful to all members of our laboratory team for stimulating discussions.
The authors declare that they have no competing interests.
Both authors contributed to writing and improving the paper and approved the final manuscript.
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Idhammad, A., Abdali, A. On a new law of bone remodeling based on damage elasticity: a thermodynamic approach. Theor Biol Med Model 9, 51 (2012). https://doi.org/10.1186/1742-4682-9-51
- Numerical simulation
- Thermodynamic approach
- Small perturbations hypothesis
- Bone remodeling
- Bone density
- N-unit elements