262 IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 10, NO. 4, DECEMBER 2011 Numerical Study of Temperature Distribution in a Spherical Tissue in Magnetic Fluid Hyperthermia Using Lattice Boltzmann Method Mansour Lahonian and Ali Akbar Golneshan Abstract—This work applies a three-dimensional lattice Boltzmann method (LBM), to solve the Pennes bio-heat equation (BHE), in order to predict the temperature distribution in a spherical tissue, with blood perfusion, metabolism and magnetic nanoparticles (MNPs) heat sources, during magnetic fluid hyperthermia (MFH). So, heat dissipation of MNPs under an alternating magnetic field has been studied and effect of different factors such as induction and frequency of magnetic field and volume fraction of MNPs has been investigated. Then, effect of MNPs dispersion on temperature distribution inside tumor and its surrounding healthy tissue has been shown. Also, effect of blood perfusion, thermal conductivity of tumor, frequency and amplitude of magnetic field on temperature distribution has been explained. Results show that the LBM has a good accuracy to solve the bio-heat transfer problems. Index Terms—Bio-heat equation, lattice Boltzmann method, magnetic field, magnetic fluid hyperthermia, magnetic nanoparticle. I. INTRODUCTION M FH IS A NOVEL method used for cancer therapy. In MFH, the MNPs are delivered to the tumor. An alternating magnetic field is then applied to the target region, and then MNPs generate heat as localized heat sources. The heat generated increases the temperature of the tumor. The cancerous cells are then destroyed by raising their temperature to about whereas healthy cells will be safe at this temperature. Moroz et al. [1] stated that MFH has the maximum potential for such selective targeting. In order to kill cancer cells without injury to normal tissues, the ability to predict the temperature distribution inside as well as outside the target region as a function of the exposure time, possesses a high degree of importance. This helps to provide a level of therapeutic temperature and to avoid overheating and dammaging of the surrounding healthy tissue [2]–[4]. Two techniques are currently used to deliver MNPs to a tumor. The first is to deliver particles to the tumor vasculature through its supplying artery; however, this method is not effective for poorly perfused tumors. Furthermore, for a tumor with an irregular shape, inadequate MNPs distribution may cause under-dosage of heating in the tumor or overheating of the Manuscript received June 01, 2011; accepted November 09, 2011. Date of current version January 20, 2012. Asterisk indicates corresponding author. *M. Lahonian is with the Mechanical Engineering Department, Kurdistan University, Sanandaj, Iran (e-mail: lahonian@shirazu.ac.ir). A. A. Golneshan is with the Mechanical Engineering Faculty, Shiraz University, Shiraz, Iran (e-mail: golnshan@shirazu.ac.ir). Color versions of one or more of the figures in this paper are available online at http://ieeexplore.ieee.org. Digital Object Identifier 10.1109/TNB.2011.2177100 normal tissue. The second approach, is to directly inject MNPs into the extracellular space in tumors. MNPs diffuse inside the tissue after injection of ferrofluid. If the tumor has an irregular shape, multisite injection can be exploited to cover the entire target region [5]. Maenosono and Saita [6] investigated the feasibility of using face centered cubic iron-platinum (fcc FePt) MNPs for magnetic hyperthermia, as fcc FePt present a high Curie temperature, high saturation magnetization, and high chemical stability. To show the heating capability of these MNPs, Maenosono and Saita [6] carried out theoretical assessment of fcc FePt MNPs as heating elements for hyperthermia by combining the heat generation model and the BHE. Lin and Liu [4] developed a hybrid numerical scheme for solving the transient BHE in spherical coordinates. They estimated the temperature rise in biological tissues for the heating effect of fcc FePt MNPs and claimed that the results of Maenosono and Saita [6] are incorrect. Zhang et al. [7] illustrated the temperature distribution within tumor-normal composite tissue by establishing a multiregion finite difference algorithm using low Curie temperature MNPs. Zablotskii et al. [8] studied the heating effect of tunable arrays of nanoparticles in cancer therapy. Liangruksa et al. [9] studied heating in a tumor with blood perfusion effect due to MFH. They modeled the problem of a spherical tumor and its surrounding healthy tissue, that are heated by exciting a homogeneous dispersion of MNPs infused only into the tumor, under an alternating magnetic field. Pennes BHE model has been widely used among different bio-heat models [10], [11]. This model that is valid only for a region far from large blood vessels, shows the effect of blood flow as a temperature-dependent heat sink term. On complication of tissues and their complex geometry, exact solutions aren’t available for many cases. For many practical applications, numerical models, such as finite element method [12]–[15], finite difference method [16], [17], and Monte Carlo method [18], [19], are widely used nowadays. The usage of the LBM to analyze problems in science and engineering has increased significantly in recent years. As a different approach from the conventional computational fluid dynamics (CFD), the LBM has been demonstrated to be successful in simulation of fluid flow and heat transfer problems and other types of complex physical systems [20]–[22]. In comparison to conventional numerical methods, the LBM advantages include a simple calculation procedure, efficient implementation for parallel computation, and robust handling of complex geometries with regard to numerical stability and accuracy. 1536-1241/$26.00 © 2011 IEEE LAHONIAN AND GOLNESHAN: NUMERICAL STUDY OF TEMPERATURE DISTRIBUTION While the applicability of the LBM in fluid mechanics is well established, its application to thermal energy transport is also gaining momentum recently [23]–[28]. Zhang [29] developed the LBM as a potential solver for the bio-heat problems using Pennes BHE. The results showed that the LBM can give a precise prediction of the temperature distribution, and it is efficient to deal with the space- and time-dependent heat source, which are often encountered in the treatment planning of tumor hyperthermia. To our knowledge, Zhang’s work was the first attempt to use LBM to solve bio-heat problems. Huang et al. [30], introduced a thermal curved boundary condition for the doubled-population thermal lattice Boltzmann equation model, for uniform regular lattices. In this work we use LBM to solve the Pennes BHE with blood perfusion, metabolism, MNPs heat sources, and Neumann curved boundary condition (spherical tissue). Accordingly, heat dissipation of MNPs under an alternating magnetic field is studied and effect of different parameters such as induction and frequency of magnetic field and volume fraction of MNPs is investigated. The temperature rise in biological tissues is predicted for the heating effect of MNPs dispersion. Also, effect of the blood perfusion, thermal conductivity of the tumor, and frequency and amplitude of the magnetic field on temperature distribution is depicted. 263 Fig. 1. Schematic plot of the D3Q15 lattice. where the distribution functions is a set of populations representing the probability of finding a particle at position at time moving along the direction identified by the propagation velocity , the subscript the direction of the thermal population (see Fig. 1), the time step, the dimensionless relaxation time, and the equilibrium distribution of the evolution population (6) is the weight factor and equal to , and propagation velocity is defined as , and the where II. BIO-HEAT EQUATION for for for In a generalized form, the Pennes BHE reads (1) where , , and are the density, the specific heat, and the thermal conductivity of the tissue respectively, is the temperature, the time, , , , and are the perfusion, the density, the specific heat, and the temperature of the blood, and are the metabolic heat generation of the tissue and the distributed volumetric heat source due to spatial heating. Equation (1) can be written in a simple form as (2) to 7 to 15 (7) is the lattice velocity, and where are the discrete lattice sizes. The dimensionless relaxation time is defined as (8) where is the thermal diffusivity. The macroscopic physical quantities can be obtained from the distribution function. For the temperature and heat flux, they are [31], [32] (9) where (3) (10) and where is the dimensionless blood perfusion defined as (4) (11) III. THERMAL LATTICE BOLTZMANN METHOD The internal energy evolution equation of the three-dimensional fifteen-speed (D3Q15) LBM is as below [20]: (5) IV. BOUNDARY CONDITION In the curved boundary condition (see Fig. 2), to evaluate internal energy density distribution functions, the postcollision distribution function obtained by [30] (12) 264 IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 10, NO. 4, DECEMBER 2011 Fig. 2. Curved boundary and lattice nodes (open large circle is computational boundary node, open small circle is media node, filled circle is the physical boundary node in the link of media node and computational boundary). Fig. 3. Schematic plot of tissue and tumor. where is the postcollision distribution function, and are the equilibrium and nonequilibrium part of and . can be obtained from (6). To determine the , extrapolation method is used. is evaluated as (13) is the fraction of the intersected link in the media. where According to Fig. 2, for calculating the unknown internal energy density distribution functions such as , can be obtained as (14) In the Neumann boundary condition, the temperature at the computational boundary nodes (see Fig. 2) can be calculated as below: Fig. 4. 2-D projection of discretized domain and computational boundary nodes (filled circles) for a spherical boundary of radius 7.5 lattice units. The related boundary conditions are (18) (19) (15) (20) From (6) and (13) equilibrium and nonequlilibrium parts of are obtained to fulfill the collision step. (21) and initial conditions are V. RESULTS AND DISCUSSION Two concentric spherical regions were chosen as the domain of the analysis (Fig. 3). The inner sphere represents the diseased tissue. MNPs are present in the tumor with radius that act as sources of heat generation when an alternating magnetic field is applied. Fig. 4 shows the 2-D projection of discretized domain and computational boundary nodes (filled circles) for a spherical boundary of radius 7.5 lattice units. The outer sphere represents the healthy tissue. According to Pennes BHE, (16) and (17) define the transient heat transport in the diseased and healthy tissues, respectively [4]. (16) (17) (22) (23) , , , , , , , , , , In the above equations , , , are tumor radius, healthy tissue radius, radius, specific heat capacity, tissue thermal conductivity, blood thermal conductivity, density, metabolism heat generation, energy dissipation of MNPs in an alternating magnetic field, time, temperature, initial temperature, blood perfusion, and subscripts are diseased tissue, healthy tissue, and blood respectively. In this study the properties of the tissue are taken as , , , , where is volume fraction, , for fcc FePt MNPs, , for magnetite MNPs, , , LAHONIAN AND GOLNESHAN: NUMERICAL STUDY OF TEMPERATURE DISTRIBUTION 265 Power dissipation of MNPs in an alternating magnetic field is expressed as [35], [36] (24) where is the permeability of free space, is the equilibrium susceptibility, and are the amplitude and frequency of the alternating magnetic field, and is the effective relaxation time, given by (25) Fig. 5. History of temperature at the center of the tumor for the cases of 9-nm and 19-nm magnetite fcc FePt MNPs. and are the Néel relaxation and the Brownian rewhere laxation time, respectively. and are written as (26) (26) (27) Fig. 6. Temperature distributions in the tissue at for the cases of and 19-nm magnetite 9-nm fcc FePt MNPs. , , [4], [6]. , , , For the LBM simulation, we use lattices and the lattice size is . Therefore . In a magnetic field with fixed amplitude and frequency at 50 mT and 300 kHz and a volume fraction , 9-nm fcc FePt and 19-nm magnetite MNPs can dissipate , respectively [4], [6]. Fig. 5 shows the history of temperature at the center of the tumor for the cases of 9-nm fcc FePt and 19-nm magnetite MNPs. In accordance with the results shown in Fig. 5, the temperature distribution has become steady at . Also, Fig. 6 shows the temperature distributions in the tissue at for the cases of 9-nm fcc FePt and 19-nm magnetite MNPs. It is observed that the results of the present work, match well with those given in the literature [4]. The temperature that can be achieved in the tissue strongly depends on the power dissipation of the MNPs, thermophysical properties of the blood and the tissue, the blood perfusion in the tissue and the duration of application of the magnetic field. Also, the power dissipation of the MNPs depends on the properties of the magnetic material used, the frequency and the strength of the applied magnetic field. Therefore, carefully chosen parameters and the means to monitor the real-time temperature are required [3], [5], [33], [34]. where the shorter time constant tends to dominate in determining the effective relaxation time for any given size of particle. is the average relaxation time in response to a thermal fluctuation, is the viscosity of medium, is the hydrodynamic volume of MNP, is the Boltzmann constant, , and is the temperature. Here, where is the magnetocrystalline anisotropy constantn and is the volume of MNPs. The MNPs volume and the hydrodynamic volume including the ligand layer are written as (28) (29) where is the diameter of MNP and is the ligand layer thickness. The equilibrium susceptibility is assumed to be the chord susceptibility corresponding to the Langevin equation , and expressed as (30) where , , , and is the volume fraction of MNPs. Here, and are the domain and saturation magnetization, respectively. The initial susceptibility is given by (31) Based on the above-mentioned theory, we calculated the power dissipation for aqueous dispersion of mono-dispersed equiatomic fcc FePt MNPs varying the diameter of MNP in adiabatic condition. In Table I, physical properties of fcc FePt and magnetite are shown. Fig. 7 shows the dependence of power dissipation on induction of applied magnetic field, for fixed . Note that is varied as 30, 50, and 80 mT. Increasing earns a raise for power dissipation. Also, Fig. 8 shows the dependence 266 IEEE TRANSACTIONS ON NANOBIOSCIENCE, VOL. 10, NO. 4, DECEMBER 2011 TABLE I PHYSICAL PROPERTIES OF FCC FEPT AND MAGNETITE MNPS [6] Fig. 10. Steady state temperature distribution for 19-nm magnetite MNPs in an alternating magnetic field. Fig. 7. Dependence of power dissipation on . the human tissue [1]. The super-paramagnetic particles (10–40 nm) are recommended in clinical application as they are able to generate substantial heat within low magnetic field strength and frequency [37]. The typical magnetite dosage is magnetite MNPs per gram of tumor that has been reported in clinical studies [38], [39]. Therefore, homogenous volume fraction is (32) Here, we consider three cases for the distribution of a constant amount of magnetite MNPs inside the tumor. For each case, the volume fraction as a function of distance from the center of the tumor can be modeled as follows: (33) Fig. 8. Dependence of power dissipation on . (34) (35) Fig. 9. Dependence of power dissipation on . of power dissipation on when is fixed in 50 mT. Note that is varied as 100, 200, and 300 kHz. Increasing earns a raise and a gradual decrease, respectively, in the power dissipation and . Fig. 9 shows the dependence of power dissipation on the volume fraction, . The power dissipation increases with increasing . No change in is observed. Iron oxides magnetite nanoparticles are the most studied to date due to their biocompatibility, when injected in Now the effect of diffusion of MNPs on temperature distribution inside the tissue will be studied after applying an alternating magnetic field. Generally, the practical range of frequency and amplitudes are often described as 50–1200 kHz and 0–15 kA/m [40]. Fig. 10 shows the temperature distribution for 19-nm magnetite MNPs in an alternating magnetic field with amplitude of 10 kA/m and frequency of 100 kHz for constant , linear and parabolic distributions of MNPs inside the tumor. As shown in Fig. 10, the temperature in the healthy tissue are the same for three cases but the temperature in the tumor is the highest for linear distribution and the lowest for homogenous distribution. As a result, 19-nm magnetite MNPs are able to raise the temperature of the tumor above in the magnetic field of amplitude of 10 kA/m and frequency 100 kHz with the dose of 10 mg magnetite MNPs per gram of tumor. Fig. 11 shows the effect of different factors such as the blood perfusion, thermal conductivity of the tumor, frequency and amplitude of the magnetic field on temperature distribution inside LAHONIAN AND GOLNESHAN: NUMERICAL STUDY OF TEMPERATURE DISTRIBUTION 267 Fig. 11. Temperature distribution inside the tumor and its surrounding healthy tissue under different conditions. the tumor and its surrounding healthy tissue, for linear distribution of MNPs case. Results show increasing the blood perfusion decreases the temperature inside the tumor and its surrounding healthy tissue [Fig. 11(a)]. Also, increasing thermal conductivity of the tumor decreases the temperature only in the tumor area [Fig. 11(b)]. Furthermore, increasing amplitude and frequency of the magnetic field increases the temperature of both the tumor and the healthy tissue [Figs. 11(c) and 11(d)]. that increasing of the blood perfusion decreases the temperature inside the tumor and its surrounding healthy tissue. Also, increasing thermal conductivity of the tumor only decreases the temperature inside the tumor. In addition, increasing of amplitude and frequency of the magnetic field increases the temperature all over the tissue. Results show that the LBM has good accuracy to solve the bio-heat transfer problems. REFERENCES VI. CONCLUSION We have applied a three-dimensional LBM for solving the Pennes BHE to predict the temperature distribution in spherical tissue in MFH treatment. The effects of the blood perfusion, the metabolism and the magnetic nanoparticles (MNPs) heat sources were introduced. To validation, the results were compared with those reported in the literature [4]. To show the effect of MNPs dispersion on temperature distribution, firstly, the effect of different parameters such as induction and frequency of the magnetic field and the MNPs volume fraction was studied. Then, effect of MNPs dispersion for homogenous, parabolic and linear distribution was investigated. As a result, 19-nm magnetite MNPs are able to rise the temperature of the tumor above in the magnetic field of amplitude of 10 kA/m and frequency 100 kHz with the dose of 10 mg magnetite MNPs per gram of tumor. 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