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. 2013 Jul 20;245(2):188–205. doi: 10.1016/j.mbs.2013.07.001

On the dynamics of SEIRS epidemic model with transport-related infection

Adisak Denphedtnong a,b,c, Settapat Chinviriyasit a, Wirawan Chinviriyasit a,
PMCID: PMC7094751  PMID: 23876843

Highlights

  • We formulate an SEIRS epidemic model for studying the effect of transportrelated infection on disease spread.

  • We derive the basic reproduction number of the formulated model.

  • The movement without transport-relate infection will cause the disease dynamics and break infection out.

  • The transport-related infection is effected to the number of infected individuals and the duration of outbreak.

Keywords: SEIRS epidemic model, Transport-related infection, Stability, Reproduction number

Abstract

Transportation amongst cities is found as one of the main factors which affect the outbreak of diseases. To understand the effect of transport-related infection on disease spread, an SEIRS (Susceptible, Exposed, Infectious, Recovered) epidemic model for two cities is formulated and analyzed. The epidemiological threshold, known as the basic reproduction number, of the model is derived. If the basic reproduction number is below unity, the disease-free equilibrium is locally asymptotically stable. Thus, the disease can be eradicated from the community. There exists an endemic equilibrium which is locally asymptotically stable if the reproduction number is larger than unity. This means that the disease will persist within the community. The results show that transportation among regions will change the disease dynamics and break infection out even if infectious diseases will go to extinction in each isolated region without transport-related infection. In addition, the result shows that transport-related infection intensifies the disease spread if infectious diseases break out to cause an endemic situation in each region, in the sense of that both the absolute and relative size of patients increase. Further, the formulated model is applied to the real data of SARS outbreak in 2003 to study the transmission of disease during the movement between two regions. The results show that the transport-related infection is effected to the number of infected individuals and the duration of outbreak in such the way that the disease becomes more endemic due to the movement between two cities. This study can be helpful in providing the information to public health authorities and policy maker to reduce spreading disease when its occurs.

1. Introduction

The spread of infectious diseases between discrete geographic regions (or cities) is a phenomenon that involves many different compartments. To control the spread of an infectious disease, one has to understand how the growth and spread of the disease affect its outbreak. There are many factors that lead to the dynamics of an infectious disease of humans. They include such human behaviors as population dislocations, living styles, sexual practices and rising international travel. In current, population dispersal by human transportation plays an important role in the spread of infectious disease around the world. SARS (severe acute respiratory syndrome) spread along the routes of international air travel and infection was carried to many places [33], [34]. Khan et al. [14] pointed out a correlation between inter-regional spread of a novel influenza A (H1N1) virus and travelers. From these observations a number of authors have proposed epidemic models describing disease transmission dynamics among multiple locations due to the population dispersal (see [3], [4], [10], [23], [24], [25], [26], [29], [30], [31], [32] and the references therein). Recently, Cui et al. [7] have proposed a SIS epidemic model to understand the effect of transport related infection on disease spread. Takeuchi et al. [27] proved the global dynamics of model in [7]. They found that the global stabilities of equilibria disease-free and endemic equilibriums, still required additional condition besides the condition for their existence. Considering entry screening and exit screening to detect infected individuals, Liu and Takeuchi [20] proposed an SIQS model to study the effect of transport-related infection and entry screening. Subsequently, Liu and Zhou [21] analyzed global stability of an SIRS epidemic model with transport-related infection. Their results shown transport-related infection can make the disease endemic even if both the isolated regions are disease free. Obviously, the models in [7], [20], [27] assumed that a susceptible individual becomes infectious immediately after infected. However, for many diseases, a host stays in a latent period before becoming infectious after infected, Wan and Cui [29] formulated an SEIS epidemic model to describe the transmission of infectious diseases related by transports. When the individuals have immunity to the disease after recover, the SEIR or SEIRS models are more general than the SEI or SEIS types depending on whether the acquired immunity is permanent or otherwise. These kinds of models have These kinds of models have been studied to gain insights into the transmission dynamics of disease in community. For example, Greenhalgh [11] considered an SEIR model that incorporates density dependence in the death rate. Cooke and Driessche [6] introduced and analyzed the SEIRS model with two delays. Greenhalgh [12] studied Hopf bifurcations in the SEIRS type models with density dependent contact rate and death rate. Li and Muldowney [16] and Li et al. [17] studied the global dynamics of the SEIR models with a non-linear incidence rate as well as standard incidence rate. Li et al. [18] analyzed the global dynamics of the SEIR model with vertical transmission and a bilinear incidence. Recently, Zhang and Ma [36] analyzed the global dynamics of the SEIR model with saturating contact rate. However, those models have not applied to real data of outbreak to investigate the effect of transport-related infection when individuals travel among two cities.

The aim of this paper is to formulate an SEIRS epidemic model to describe the transmission of infectious diseases related by transports. The formulated model is applied to real data of SARS outbreak in 2003 in order to investigate the transmission of disease when individuals in a population suffer from diseases and possibly become infected during the movement between two cities.

This paper is organized as follows. An SEIRS model with transport-related infection is formulated in Section 2. In Section 3, the basic reproduction number of the formulated model is derived and the local stability of the model is analyzed to verify that the equilibria of the model are locally asymptotically stable under the condition of the basic reproduction number. Simulation results are presented in Section 4 to illustrate the effect of transport-related infection on its outbreak and the final size of all individuals for the populations. The SEIRS model and SEIRS model with transport-related infection are applied to predict the SARS outbreak within a city and if there is the movement of population between two cities, respectively.

2. Model formulation

The epidemic model for transmission of a communicable disease with population travel between two cities is based on monitoring the dynamics of the sub–populations (susceptible; Si(t), exposed (latent); Ei(t), infected; Ii(t), and recovered; Ri(t), in the city i, i=1,2 at time t). Thus, the total population in city i at time t is given by Ni=Si(t)+Ei(t)+Ii(t)+Ri(t) for i=1,2. It is assumed that both cities are identical, i.e. the demographic parameters are the same for each city.

The population of susceptible individuals is increased by the recruitment of individuals which are all newborn into the population at the rate a and the loss of infection–acquired immunity among recovered individuals at the rate α2 and by the susceptible individuals of city j leave to city i (ji,i=1,2) at the rate α1. In the other hand, it is decreased when the susceptible individuals in city i leave to city j at the rate α1 and by natural death at the rate b. It is assumed that susceptible individuals can acquire exposed individuals via effective contacts with infected individuals. The disease is transmitted horizontally within and between cities according to standard the incidence rate (that is, the number of new cases of infection per unit time)

βSiIiNi,fori=1,2,

where β is the transmission rate within a city. This population is further decreased when the individuals in city j travel to city i, and the disease is transmitted with the incidence rate

γ(α1Sj)(α1Ij)(α1Sj+α1Ej+α1Ij+α1Ri)=γα1SjIjNj,forj=1,2,

where γ is the transport-related transmission rate. Thus, the rate of change of population of susceptible class is given by

dSidt=a-bSi-βSiIiNi+α2Ri-α1Si+α1Sj-γα1SjIjNj. (2.1)

The population of exposed individuals is generated by the infected of susceptible individuals at the rate βSiIiNi and at the rate γα1SjIjNj when the individuals in city j travel to city i. It is reduced by progression to symptoms development at the rate c, travel to city j at the rate α1 and natural death at the rate b. Thus

dEidt=βSiIiNi-b+c+α1Ei+α1Ej+γα1SjIjNj. (2.2)

The population of infected individuals in city i is generated when exposed individuals develop symptoms at the rate c, and when infected individuals of city j leave to city i at the rate α1. It is decreased by progression to the recovered class at the rate d, natural death and disease induced mortality at the rate e, and when infected individuals of city i move to city j at the rate α1. Thus,

dIidt=cEi-e+d+α1Ii+α1Ii. (2.3)

The population of recovered individuals is generated when infected individuals recover and move to the recovered class at the rate d, and when recovered individuals of city j leave to city i. It is decreased by the loss of infection–acquired immunity at the rate α2, by natural death at the rate b, and when recovered individuals of city i move to city j at the rate α1. Thus,

dRidt=dIi-b+α1+α2Ri+α1Rj. (2.4)

It is assumed that the individuals have no infectious force in the latent period and the exposed individuals cannot recover to susceptible individuals. The individuals who are travelling do not give birth and do not take die. Infected individuals do not recover during travel. Thus, An SEIRS with transport-related infection consists of the following system of non–linear differential equations:

dS1dt=a-bS1-βS1I1N1+α2R1-α1S1+α1S2-γα1S2I2N2,dE1dt=βS1I1N1-b+c+α1E1+α1E2+γα1S2I2N2,dI1dt=cE1-e+d+α1I1+α1I2,dR1dt=dI1-b+α1+α2R1+α1R2,dS2dt=a-bS2-βS2I2N2+α2R2-α1S2+α1S1-γα1S1I1N1,dE2dt=βS2I2N2-b+c+α1E2+α1E1+γα1S1I1N1,dI2dt=cE2-e+d+α1I2+α1I1,dR2dt=dI2-b+α1+α2R2+α1R1. (2.5)

A flow diagram of the model is depicted in Fig. 1 . The standard incidence is used in the model. If initial conditions are set as Si(0)0, Ei(0)0, Ii(0)0 and Ri(0)0, it is easy to check that all solutions of (2.5) are nonnegative (that is Si(0)0, Ei(0)0, Ii(0)0 and Ri(0)0 for t>0, i=1,2) under the assumption 0γ1. Note that the last two terms in the first and fifth equations of (2.5) satisfy that

α1Si-γα1SiIiNi0(i=1,2),

for any Si0, Ei0, Ii0 and Ri0 when 0γ1. This is reasonable from a biological point of view, since the first term α1Si represents the susceptible individuals leaving city i and the second term γα1SiIiNi denotes individuals in α1Si becoming infected during travel from city i to j. Hence, the difference between these two numbers should be nonnegative. It is supposed that 0γ1.

Fig. 1.

Fig. 1

Schematic diagram of the SEIRS model for the transmission of communicable disease during the movement of population between two cities.

3. Analysis of the model

In this section, the model (2.5) is analyzed for stability of its associated equilibrium at some different cases. In particular, the Routh–Hurwitz theorem in [1], reproduced below for convenience, will be used for the kind of the following matrix J:

J=a11a12a13a14a21a22a23a240a32a33000a43aa44. (3.1)

Lemma 3.1

A1=-tr(J) , A2=J1+J2+J3 , A3=Q1+Q2+Q3 , A4=det(J) , where J1=a44a33+a44a22+a44a11+a33a11 , J2=a33a22-a32a23 , J3=a22a11-a21a12 , Q1=-a44(J2+J3) , Q2=-a33(J2) , Q3=-(a32(a21a13+a43a24)+a11(a44a33-a32a23)). Then J is stable (i.e. each eigenvalue of J has negative real part) if and only if the following conditions hold:

  • (i)

    Ai>0,

  • (ii)

    A1A2-A3>0,

  • (iii)

    A1A2A3-A32-A12A4>0.

Remark 3.1

The characteristic polynomial of matrix J in (3.1) is

λ4+A1λ3+A2λ2+A3λ+A4=0.

3.1. No individual travel

The movement of individuals is neglected, this case α1=0, then model (2.5) reduces to the SEIRS model:

dSdt=a-βSIN-bS+α2R,dEdt=βSIN-b+cE,dIdt=cE-e+dI,dRdt=dI-b+α2R. (3.2)

From biological considerations, we study (3.2) in the closed set

D={(S,E,I,R)R+4|S0,E0,I0,R0,S+E+I+Ra/b},

where R+4 denotes the non–negative cone of R4 including its lower dimensional faces. It can be verified that D is positively invariant with respect to (3.2).

The disease-free equilibrium, obtained by setting the right–hand sides of equations in (3.2) to zero, is given by

P0(S0,0,0,0)=ab,0,0,0. (3.3)

The linear stability of P0 can be established using the next generation method [8], [10] by writing the right hand sides of second and third equation in (3.2) in term of two matrices F and V, where F is a matrix consisting of all term with β and V is M-matrix consisting of the remaining transition term in two equations (it should be recalled that a matrix A is an M-matrix if and only if every off-diagonal entry of A is non-positive and the diagonal entries are all non-negative). That is, for the model (3.2), the next generation matrices F and V are given by

F=0β00andV=b+c0-ce+d.

Using the next generation method, the local stability of disease-free equilibrium, P0, is based on whether or not ρ(FV-1)<1, where ρ is the spectral radius. If ρ(FV-1)<1, then all eigenvalues of the linearized model have negative real parts, so that the disease-free equilibrium is locally asymptotically stable (LAS). For ρ(FV-1)>1, at least one of the eigenvalues of the linearization has positive real part, thus, the disease-free equilibrium is unstable in this case. Let R0=ρ(FV-1), it is easy to show that

R0=βce+db+c. (3.4)

Consequently, using Theorem 2 of [28], the following results is established.

Theorem 3.1

The disease-free equilibrium (DFE), P0 , of the system ( 3.2 ) is locally asymptotically stable (LAS) if R0<1 and unstable if R0>1 .

The quantity R0 in (3.4) is called the basic reproduction number of infection [2]. It is generally known that if R0<1, then the disease-free equilibrium is locally asymptotically stable (and the disease will be eradicate from the community if the initial sizes of the four state variables are within the vicinity of P0). Therefore, in the event of an epidemic, the theoretical determination of conditions that can make R0 less than unity is of great public health interest. If R0>1, the system (3.2) has an endemic equilibrium P(S,E,I,R), where

S*=ab+α2(c+d+e)+cdΩ,E*=aR0-1b+α2e+dΩ, (3.5)
I*=acR0-1b+α2Ω,R=acdR0-1b+α2Ω, (3.6)

with Ω=R0b(be+cd+dα2+eα2+bd)+c(b+α2)((R0-1)e+b), and N*=S+E+I+R=R0S.

Evaluating the Jacobian of (3.2) at P gives

J(P)=-b-ψ1ψ2-ψ3ψ2+α2ψ1-b-c-ψ2ψ3-ψ20c-e-d000d-b-α2, (3.7)

where

ψ1=βI(N-S)N2=βcR0-12b+α2R02(b+α2)(c+d+e)+cd,ψ2=βSIN2=βcR0-1b+α2R02(b+α2)(c+d+e)+cd,ψ3=βS(N-I)N2=(βc+βR0(d+e))(b+α2)+βcdR0R02(b+α2)(c+d+e)+cd. (3.8)

Note that Jacobian matrix (3.7) has the form as (3.1), using Lemma 3.1 (see Appendix A), we have the following result:

Theorem 3.2

If R0>1 , the endemic equilibrium, P , is LAS.

3.2. Only susceptible and exposed individuals travel

When the infected and recovered individuals are inhibited from traveling to another city, that is α1=γ=0, the model (2.5) becomes

dS1dt=a-bS1-βS1I1N1+α2R1-α1S1+α1S2,dE1dt=βS1I1N1-b+c+α1E1+α1E2,dI1dt=cE1-e+dI1,dR1dt=dI1-b+α2R1,dS2dt=a-bS2-βS2I2N2+α2R2-α1S2+α1S1,dE2dt=βS2I2N2-b+c+α1E2+α1E1,dI2dt=cE2-e+dI2,dR2dt=dI2-b+α2R2. (3.9)

From calculations, there are possible two steady states for model (3.9); namely, disease-free equilibrium, P1(ab,0,0,0,ab,0,0,0) and endemic equilibrium, P2(S,E,I,R,S,E,I,R), respectively. Here S,E,I,R,R0 are given by Eqs. (3.5), (3.6).

According to the concept of next generation matrix [8] and reproduction number presented in van den Driessche and Watmough [28], the matrices F and V are given by

F=0β00000000β00000andV=b+c+α10-α10-ce+d00-α10b+c+α1000-ce+d,respectively.

Therefore, the basic reproduction number of model (3.9) is given by

R0=ρ(FV-1)=βce+db+c. (3.10)

Note that the basic reproduction numbers of (3.2), (3.9) are identical.

The Jacobian matrix of the model (3.9) at equilibrium point, P, is given by

J(P)=A1BBA2 (3.11)

where, for i=1,2,

Ai=-b-α1-βIi(Ni-Si)Ni2βSiIiNi2-βSi(Ni-Ii)Ni2βSiIiNi2+α2βIi(Ni-Si)Ni2-b-c-α1-βSiIiNi2βSi(Ni-Ii)Ni2-βSiIiNi20c-e-d000d-b-α2

and B=α10000α10000000000. From calculations in Appendix B, the following result is established:

Theorem 3.3

(i) If R0<1 , then P1 is LAS. (ii) If R0>1 , then P2 is LAS.

Remark 3.2

There is, from Theorem 3.3, some import implications. First, if the disease have appeared in both cities then the travel of susceptible and exposed individuals does not change the dynamics of disease spreading, and the final size of susceptible, exposed, infected and recovered individuals does not change, see Fig. 4. Second, if a disease has appeared only in city 1 with E1(0)>0, I1(0)>0, E2(0)=0, I2(0)=0 and R0>1 (see Figs. 4(b)–(c)), the traveling of exposed individuals will bring the disease to city 2 and the disease will break out later in city 2 (see Figs. 4(f)–(g)). On the contrary, if R0<1, there is not the possibility for disease spreading in both cities, as shown in Figs. 4(b)–(c)), and Figs. 3(f)–(g).

Fig. 4.

Fig. 4

Simulations of the model (3.9) showing the number of all individuals in two cities as a function of time using the parameter values in Table 1 with β=0.95 and R0=1.14>1: (a)–(d) the profiles of all populations in city 1; (e)–(h) the profiles of all populations in city 2.

Fig. 3.

Fig. 3

Simulations of the model (3.9) showing the number of all individuals in two cities as a function of time using the parameter values in Table 1 with β=0.6 and R0=0.72<1: (a)–(d) the profiles of all populations in city 1; (e)–(h) the profiles of all populations in city 2.

3.3. All individuals travel between two cities

In this section, the full model (2.5) is explored to study the effect of transport-related infection when all individuals can travel between two cities. The extended model (2.5) has a disease-free equilibrium, given by P1(ab,0,0,0,ab,0,0,0). Here, the next generation matrices, F and V, are given by

F=0β0γα100000γα10β0000andV=b+c+α10-α10-ce+d+α10-α1-α10b+c+α100-α1-ce+d+α1.

It follows that, using the next generation approach, the basic reproduction number of the model (2.5), denoted by R0γ, is

R0γ=R0+γα1c(b+c)(d+e). (3.12)

Consequently, using Theorem 2 of [28], the following result is established.

Lemma 3.2

The disease-free equilibrium, P1 , of the model (2.5) is LAS if R0γ<1 , and unstable if R0γ>1.

The model (2.5) has a unique coexistence endemic equilibrium denoted by Pγ(Sγ,Eγ,Iγ,Rγ,Sγ,Eγ,Iγ,Rγ),

Sγ*=ab+α2(c+d+e)+cdΩγ,Eγ*=aR0γ-1b+α2e+dΩγ, (3.13)
Iγ*=acR0γ-1b+α2Ωγ,Rγ*=acdR0γ-1b+α2Ωγ, (3.14)

with Ωγ=R0γb(be+cd+dα2+eα2+bd)+c(b+α2)((R0γ-1)e+b).

The local stability of the coexistence endemic equilibrium is now explored. The Jacobian matrix of system (2.5) at the equilibrium point, P, is given by

J(P)=A1B2B1A2, (3.15)

where, for i=1,2, Ni=Si+Ei+Ii+Ri,

Ai=-b-α1-βIi(Ni-Si)Ni2βSiIiNi2-βSi(Ni-Ii)Ni2βSiIiNi2+α2βIi(Ni-Si)Ni2-b-c-α1-βSiIiNi2βSi(Ni-Ii)Ni2-βSiIiNi20c-e-d-α1000d-b-α1-α2

and

Bi=α1-γα1Ii(Ni-Si)Ni2γα1SiIiNi2-γα1Si(Ni-Ii)Ni2γα1SiIiNi2γα1Ii(Ni-Si)Ni2α1-γα1SiIiNi2γα1Si(Ni-Ii)Ni2-γα1SiIiNi200α10000α1.

From calculations in Appendix C, we have the following results:

Theorem 3.4

The endemic equilibrium, Pγ , of (2.5) is LAS if R0γ>1.

From Theorem 3.4, the disease eradication is possible for a sufficient small parameter γ when the both cities are disease-free without traveling (that is, R0γ<1 for small γ when R0<1). Comparing R0γ with R0, on the other hand, we find that even a small transmission rate γ is unfavorable or harmful to disease eradication since R0γ>R0 for γ>0. In fact, if γ=0 and R0<1 hold, then infectious disease should disappear in both cities from (3.12) (see Fig. 5, Fig. 6). Further, if infected individuals can travel and there is transport-related infection such that R0γ>1 then the endemic steady state Pγ(Sγ,Eγ,Iγ,Rγ,Sγ,Eγ,Iγ,Rγ) appears in two cities to become stable. This situation is illustrated in Fig. 7, Fig. 8.

Fig. 5.

Fig. 5

Simulations of the model (2.5) showing the number of all individuals in two cities as a function of time using the parameter values in Table 1 with β=0.6, γ=0.09, R0=0.72<1 and R0γ=0.82<1: (a)–(d) the profiles of all populations in city 1; (e)–(h) the profiles of all populations in city 2.

Fig. 6.

Fig. 6

Simulations of the model (2.5) showing the number of all individuals in two cities as a function of time using the parameter values in Table 1 with β=0.6, γ=0.2, R0=0.72<1 and R0γ=0.936<1: (a)–(d) the profiles of all populations in city 1; (e)–(h) the profiles of all populations in city 2.

Fig. 7.

Fig. 7

Simulations of the model (2.5) showing the number of all individuals in two cities as a function of time using the parameter values in Table 1 with β=0.6, γ=1, R0=0.72<1 and R0γ=1.8>1: (a)–(d) the profiles of all populations in city 1; (e)–(h) the profiles of all populations in city 2.

Fig. 8.

Fig. 8

Simulations of the model (2.5) showing the number of all individuals in two cities as a function of time using the parameter values in Table 1 with β=0.95, γ=1, R0=1.14>1 and R0γ=2.22>1: (a)–(d) the profiles of all populations in city 1; (e)–(h) the profiles of all populations in city 2.

As above results, it can be concluded that if the disease is endemic in both isolated cities, then transport-related infection will surely lead to the disease becoming endemic. When the two isolated cities are disease-free, transport-related infection may also have the possibility to lead to the disease becoming endemic. In addition, to see clearly the effect of transport-related infection, the relations among two reproduction number, R0 in (3.4) and R0γ in (3.12), are compared. It is found that R0γ>R0 for γ>0, and R0γ=R0 for γ=0. Since R0γγ=α1(b+c)(e+d)>0 for all γ>0, it implies that R0γ increases with the increase of γ. Consider the coexistence steady state Pγ(Sγ,Eγ,Iγ,Rγ,Sγ,Eγ,Iγ,Rγ) of the model (2.5) given by Eqs. (3.13), (3.14), it is clear that SγS, EγE, IγI, RγR as γ0. Comparing coexistence steady state values of susceptible, exposed, infected and recovered individuals in the case of γ=0 with those of γ>0, respectively, give Sγ<S, Eγ>E, Iγ>I and Rγ>R for γ>0 because of

Sγγ=-a[(b+α2)(c+d+e)+cd]R0γ/γΩγ2<0,Eγγ=aΛ(b+α2)(e+d)R0γ/γΩγ2>0,Iγγ=acΛ(b+α2)R0γ/γΩγ2>0,Rγγ=acΛ(b+α2)R0γ/γΩγ2>0,

with Λ=b(bc+cα2+be+cd+dα2+eα2+bd). It is also found that Sγ=S, Eγ=E, Iγ=I and Rγ=R when γ=0. This implies that, at steady–state, the total number of susceptible individuals in the both cities decreases with the increase of γ, while the total number of exposed, infected and recovered individuals increase with the increase of γ.

Next, the effect of transport-related infection to the final size of population is discussed. Note that

Nγ=Sγ+Eγ+Iγ+Rγ=a[(b+α2)(c+d+e)+cd]Δ+, (3.16)

where Δ=b(be+cd+dα2+eα2+bd+ce)+ceα2 and =c(b+α2)(b-e)(e+d)(b+c)β+γα1.

The partial derivative of Nγ with respect to γ is given by

Nγγ=-a[(b+α2)(c+d+e)+cd](Δ+)2γ

with

γ=cα1(b+α2)(e-b)(e+d)(b+c)(β+γα1)2.

Since e>b then γ>0. It follows that Nγγ<0. Therefore, Nγ<N for γ>0 and Nγ=N for γ=0. This implies that the final size of populations decreases with the increase of γ.

By the way, it is found that

γEγ+Iγ+RγNγ=1Nγ2(Eγ+Iγ+Rγ)γSγ-Sγγ(Eγ+Iγ+Rγ)>0,γSγNγ=1Nγ2Sγγ(Eγ+Iγ+Rγ)-Sγ(Eγ+Iγ+Rγ)γ<0,

since Sγγ<0. These imply that the proportion of the total number of exposed, infected and recovered individuals (i.e. the total number of individuals affected by the disease) increases with the increase of γ. On the contrary, the proportion of the susceptible individuals decreases with the increase of γ. Therefore, as above described, it can be suggested that transport-related infection will cause an endemic disease more seriously on spreading disease. Moreover, from these epidemiological implications, it is very essential to strengthen restrictions of passengers once when an infectious disease appears.

4. Numerical experiments

The models (2.5), (3.2), (3.9) are solved by using fourth–order Runge kutta method with the parameter values/ranges in Table 1 . The results are shown in two experiments. Experiment 1 presents the various theoretical results under the conditions of the basic reproduction numbers, R0 and R0γ, in order to illustrate the effect of transport-related infection on its outbreak. Experiment 2 shows the SEIRS model (3.2) is applied to study the outbreak of SARS in a city and the SEIRS model with transport-related infection (2.5) is applied to study the SARS outbreak during the movement between two cities.

Table 1.

Description and parameter values for the models (2.5), (3.2), (3.9).

Parameters Descriptions Values References
a Recruitment rate 1 [29]
(by birth and by immigration)
b Natural death rate 0.2 [29]
c Rate that exposed individuals 0.3 [29]
become infected individuals
d Transfer rate from infected 0.1 [22]
individuals to recovered individuals
e Mortality rate for infected individuals 0.4 [29]
α2 Rate that recovered individuals 0.03 [22]
become susceptible individuals
α1 Rate that individuals of city i leave 0.9 [29]
to city j(ji)
β Transmission rate 0β1 Assumed
γ Transport-related transmission rate 0γ1 Assumed

4.1. Experiment 1: numerical simulations of the models

Firstly, the dynamics of model (3.2) which neglects the movement of individuals are investigated by setting the transmission rate within a city, β=0.6, 0.95 due to give R0=0.72<1 and R0=1.14>1, respectively. The typical behaviors of all individuals at steady-states as a function of R0 are shown in Fig. 2 . Figs. 2(a)–(d) verifies that the numerical solutions of the model (3.2) converge to disease-free equilibrium, P0(S0,0,0,0), whenever R0<1, and to endemic equilibrium in (3.5), (3.6), P(4.219,0.317,0.19,0.083), if R0>1, (see Figs. 2(e)–(h)), respectively. These results are in line with Theorem 3.1, Theorem 3.2, respectively.

Fig. 2.

Fig. 2

Time series plot of the model (3.2) with parameter values in Table 1 and initial conditions S(0)=2, E(0)=1, I(0)=1, R(0)=0: (a)–(d) profiles of all populations for β = 0.6, R0=0.72<1; (e)–(h) profiles of all populations for β = 0.95, R0=1.14>1.

Next, assume that only susceptible and exposed individuals travel to another city at the same rate α1 while the infected and recovered individuals are inhibited from traveling to another city. Thus, model (3.2) is extend to model (3.9). The model (3.9) is simulated with parameter values in Table<br/>1. For numerical simulation purposes, the transmission rate within a city, β, is set to be 0.6 and 0.95, respectively. The initial conditions are used: S1(0)=2, E1(0)=1, I1(0)=1, R1(0)=0, S2(0)=2, E2(0)=0, I2(0)=0 and R2(0)=0. The profiles of susceptible, exposed, infected and recovered individuals at steady–state are depicted in Fig. 3, Fig. 4 . Let β=0.6, then R0=0.72. It is seen that the obtained results convergence to the disease-free equilibrium P1=(S0,0,0,0,S0,0,0,0)=(5,0,0,0,5,0,0,0) if R0<1, as shown in Fig. 3. According to Theorem 3.3, the disease-free equilibrium P1 is locally asymptotically stable whenever R0<1. It interprets that the infected individuals in city 1 decrease while the infected individuals in city 2 appear to be pandemic initially, and are eventually extinct. Therefore, the disease die out separately in two cities if R0<1. When β=0.95, then R0=1.14. All solutions of the model (3.9) admit an endemic equilibrium P2=(S,E,I,R,S,E,I,R)=(4.219,0.317,0.19,0.083,4.219,0.317,0.19,0.083), see Fig. 4. This confirms that the endemic equilibrium, P2, is locally asymptotically stable whenever R0>1 (as guaranteed by Theorem 3.3).

Finally, two basic reproductions numbers, R0 and R0γ, are compared,

R0=βcb+ce+dandR0γ=R0+γα1c(b+c)(e+d). (4.17)

It is clear that, from (4.17), R0γ>R0, and R0γ depends on R0 and transport-related infection rate, γ. When β=0.6 and the other parameters b,c,d,e,α1 given in Table 1, it is found that R0<1 and R0γ<1 whenever 0<γ<7/27, and R0>1 and R0γ>1 whenever 7/27<γ1. Whereas β=0.95 then R0>1 and R0γ>1 for all γ>0. Thus, this experiment investigates the dynamics of disease transmission into two cases by solving model (2.5) with various values of β and γ: β=0.6,0.95 and γ=0.09,0.2,1, whilst retaining the same values of the other parameters. In all computations, the initial conditions are taken to be S1(0)=2, E1(0)=2, I1(0)=2, R1(0)=2, S2(0)=1, E2(0)=1, I2(0)=1, R2(0)=1.

  • Case 1.

    When R0<1 and R0γ<1, the parameters β and γ are chosen to be β=0.6 and γ=0.09,0.2, respectively. The profiles of susceptible, exposed, infected and recovered individuals, as depicted in Fig. 5, Fig. 6 , reveal that the numerical solutions of model (2.5) converge to disease-free equilibrium, P1, whenever R0γ<1 (as guaranteed by Lemma 3.2). This study suggests that the transport-related infection may not lead to the disease becoming endemic when R0<1 and R0γ<1 for small γ.

  • Case 2.

    Taking the values of γ=1, β=0.6 and γ=1, β=0.95 give R0=0.72, R0γ=1.8 and R0=1.14, R0γ=2.22, respectively. These lead to study the dynamics of model (2.5) in the cases R0<1<R0γ, and 1<R0<R0γ. All experiments are guaranteed by Theorem 3.4 in the way that the number of all individuals asymptotically approach to coexistence endemic equilibrium for R0γ>1, see Fig. 7, Fig. 8 . Therefore, the results suggest that if there is transport – related infection such that R0γ>1, then the disease is endemic in both two cities.

4.2. Experiment 2: effect of transport-related infection to SARS outbreak in Hongkong 2003

The SEIRS model (3.2) is first applied to study the SARS outbreak in Hongkong 2003 by adding the cumulative number of SARS cases [5] which is given by

C=kI, (4.18)

where C denotes cumulative number of SARS cases and k is the rate of progression from infective to diagnosed. Simulations are obtained by choosing the most proper parameters (base-case estimates) to SARS on 17 March 2003 to 26 April 2003 [35]:

a=3day-1,b=0.000034day-1,c=16.4day-1,d=14day-1,e=0.007934day-1,α2=0.001day-1andk=13day-1. (4.19)

The values of b, c and d correspond to life expectancy of 80 years [13], an average incubation period of 6.4 days and infectious period of approximately 4 days [9], respectively. The rate of SARS induced mortality is 0.0079 day-1 [13]. The rate k is progression from infective to diagnosed and is set to be 1/3 day-1 [5]. The natural death rate is 0.000034 day-1 [13], then the rate e is 0.007934 day-1 (summation of natural death rate and SARS induced mortality rate). The basic reproduction number (R0) values for SARS is in the range 2.2 to 3.7 [19], then R0 is selected as 2.7 [19]. Substituting R0=2.7 in (3.4) give the transmission rate

β=0.679day-1. (4.20)

For numerical simulations, the initial conditions are assumed to be S(0)=1,100, E(0)=95, I(0), R(0)=0 and C(0)=95. For I(0)=95 corresponds to number of infectious cases on 17 March 2003. The numerical results of model (3.2), (4.18) are shown in Fig. 9, Fig. 10 . Fig. 9 shows that the number of susceptible individuals decrease whereas the number of exposed, infected and recovered individuals increase. This means that when the disease spread occurs, the number of susceptible individuals decrease since the susceptible individuals contact with infected individuals. Thus, susceptible individuals can require exposed individuals. After 2–10 days [9], the exposed individuals is progression to symptoms development, therefore, exposed individual is called infected individuals. After that infected individuals is hospitalized about 3–5 days [9] and then infected individuals is becomes recovered individuals. It can be concluded that SARS is highly infectious base on the gradient of the susceptible curve. Fig. 10 shows the predicted total cases obtained by (4.18). The resulting curve for C fits very well with the observed total cases from 17 March 2003 to 26 April 2003 (totally 54 days). This implies that SEIRS model (3.2) can be used to predict the SARS transmission in Hongkong 2003.

Fig. 9.

Fig. 9

The number of all populations in a city produced by the model (3.2) with the parameter values: a=3day-1, b=0.000034day-1, c=16.4day-1, d=14day-1, e=0.007934day-1, α2=0.001day-1, k=13day-1 and β=0.679day-1.

Fig. 10.

Fig. 10

Comparison the cumulative numbers of SARS between actual data by WHO [35] (dotted lines) and predicted by SEIRS model(3.2) (solid lines).

Next, an SEIRS model with transport-related infection (2.5) is applied to study the dynamic of SARS during the movement among two cities. It is assumed that the all individuals can travel from one city to another city at the rate α1. It is also assumed that both cities are identical, i.e. the demographic are the same for each city. When the disease spread occurs, the disease is transmitted with transition rate γα1. Thus, the effect of transport-related infection, γ, is monitored to forecast the total number of infected individuals and duration of its outbreak. In this case the model (2.5) is simulated by using parameter values α1=0.9 and various values of γ: γ=0, γ=0.2 and γ=1, whilst retaining the same values of other parameters in the previous experiment. The initial conditions are used S1(0)=1,100, E1(0)=95, I1(0)=95, R1(0)=0, C1(0)=95, S2(0)=1,100, E2(0)=5, I2(0)=5, R2(0)=0, C2(0)=0. The cumulative number of cases and trajectory of infected individuals, in two cities, are shown in Fig. 11, Fig. 12 , respectively. The results show that the total number of SARS in both cities increases with increase of γ (see Fig. 11). It is also seen that the maximum number of infected individuals are 130, 150, 240 and the outbreak reached its peak about 22 days, 20 days, 10 days as γ increase, γ=0, γ=0.2, γ=1, respectively (see Fig. 12). This confirms that the size and duration of an outbreak can be influenced by transport-related infection. Thus, to reduction and to prevention the spread of SARS, it should have the control measure of the traveling of individual from one city to another city.

Fig. 11.

Fig. 11

The cumulative number of SARS cases obtained by the model (2.5) with various of γ: γ=0, γ=0.2, γ=1: (a) the cumulative number of SARS cases in city 1; (b) the cumulative number of SARS cases in city 2.

Fig. 12.

Fig. 12

The trajectory of infected individuals of the model (2.5) with various of γ and other parameter values: a=3day-1, b=0.000034day-1, c=16.4day-1, d=14day-1, e=0.007934day-1, α2=0.001day-1, k=13day-1, β=0.679day-1, and α1=0.9day-1.

5. Conclusions

This paper presents an SEIRS with transport-related infection for studying the spreading disease during the movement between two cities. The model was rigorously analyzed into three cases in order to gain insights into their qualitative dynamics. The following results are obtained:

  • (i)

    Each of the three models considered in this study has a locally asymptotically stable if a certain threshold quantity, known as the basic reproduction number, is less than unity; indicating that the number of infectious individual in the community will be brought to zero if public health measures that make (and keep) the threshold to a value less than unity are carried out;

  • (ii)

    The basic reproduction number of the models (3.2), (3.9) are identical, then the traveling of susceptible and exposed (means exposed but not yet infectious) individuals does not change the dynamics of the corresponding epidemic model when the disease had appeared in both regions. But if the basic reproduction number is greater than unity, the traveling of the exposed individuals can bring the disease from one region to other regions according to Theorem 3.3;

  • (iii)

    If there is no restriction on the traveling of the exposed and infectious individuals, according to Theorem 3.7 and the discussion behind this theorem, then transport-related infection intensifies the disease spread in the sense of that both the absolute and relative size of patients increase when R0γ>1;

  • (iv)

    The result of the SEIRS model without transport related infections (3.2) is good agreement with the real data of SARS outbreak in Hongkong 2003. When there is the movement of exposed and infectious individuals between two cities, the SEIRS model with transport related infection (2.5) is used to investigate the outbreak of SARS when the individuals in one city travel to another city. The results show that the transport-related infection is effected to the number of infected individuals and the duration of outbreak in such the way that the disease becomes more endemic due to the movement between two cities. This study can be helpful in providing the information to public health authorities and policy maker to reduce spreading disease when its occurs. However, the results of the model (2.5) has not yet forecasted the real size of the SARS epidemics in two city and one can see that in the model (2.5), it is assumed that the two regions share an identical parameter set. It may be necessary to consider two different population sizes and different dispersal rates in order to discuss precisely the impact of the transport-related infection on the disease dynamics. Moreover, to make the model more realistic, gravity models introduced by Murray and Cliff [15] is applied. We leave these to future work.

Acknowledgements

This research are (partially) supported by the Center of Excellence in Mathematics, the Commission on Higher Education, Thailand, and the Higher Education Research Promotion and National Research University Project of Thailand, Office of the Higher Education Commission (under NRU-CSEC Project). The authors would like to thank the anonymous referees for very helpful suggestions and comments which led to improvements of our original manuscript.

Appendix A. Proof of Theorem 3.2

Proof

From Jacobian matrix (3.7) has the form as (3.1), it suffices to check (3.7) satisfy in Lemma 3.1 to stability of P. We check for J(P) as following steps.

  • (i)

    A1>0. Obviously, ψi>0 for i=1,2,3 when R0>1, and aii<0 for i=1,2,3,4. Thus, A1=-(a11+a22+a33+a44)>0.

  • (ii)

    A2=J1+J2+J3 where J1=a44a33+a44a22+a44a11+a33a11, J2=ψ2(e+d+c) and J3=ψ2b+(b+c)(ψ1+b). Obviously, J2>0, J3>0 and J1>0 since aii<0 for i=1,2,3,4. Thus, A2=J1+J2+J3>0.

  • (iii)

    A3=Q1+Q2+Q3 where Q1=-a44(J2+J3), Q2=-a33J3, Q3=ψ2c(b+d)+(e+d)[ψ1(b+α2)+bα2]-cb(e+d). Since -a33>0, -a44>0, J2>0 and J3>0, then Q1>0 and Q2>0. Furthermore, Q2+Q3=ψ2c(b+d)+(e+d)[ψ1(b+α2)+bα2+b(b+ψ1)+ψ1c+ψ2b]>0. Thus, A3=Q1+Q2+Q3>0.

  • (iv)
    A4=det(J(P))=L1+L2+L3 where L1=(b+α2)(e+d)J3, L2=dc(bψ2-ψ1α2), and L3=-(b+α2)cψ3b. Since a33<0, a44<0 and J3>0, it is found that
    A4=b(e+d)(b+α2)(ψ1+ψ2)+cbψ2(b+α2+cd)+bψ1(e+d)(b+α2+c)+cα2eψ1>0.
  • (v)
    A1A2-A3>0. Since aii<0 for i=1,2,3,4, and Ji>0 for i=1,2,3, it follows that
    A1A2-A3=-a11(J2+J3)-a22(J1+J3)-a33(J1+J2)-a44J1-a11(a44a22+a44a11+a33a11)+(b+ψ2)J2+cψ2(e+c)+bcψ3>0.
  • (vi)
    Finally, it can be shown that A1A2A3-A32-A12A4>0. We have A4=L1+L2+L3, then
    A1A2A3-A32-A12A4=(A1A2-A3)A3-A12L1+A12(-L2-L3).
    It is revealed that A1A2A3-A32-A12A4>0 since
    -L2-L3=cdψ1α2+cb(b+α2)(βc+βR0(e+d))(b+α2)+βcdR02(b+α2)(c+d+e)+cd>0
    and
    (A1A2-A3)A3-A12L1=(-(a11+a33)J2+(b+ψ2)J2+cψ2(e+c)+bcψ3)A3+ca112a332a44-(a22+a33+a44)(J1A3-L1A1)-(a11+a22)(J3A3-a11L1)+a11a44(-(a11+a22)A3-L1)+a11a33(-a11A3-ca11a33a44-L1)>(b+ψ1)(e+d)Γ1+(2b+c+ψ1+ψ2)Γ4+(b+ψ1)(b+α2)Γ6+(2b+c+ψ2+e+d+α2)Γ7>0
    where
    Γ1=ψ2(b+α2)[ψ1(e+d)+c(b+ψ1)]+(b+ψ1)(b+α2)J3+(b+ψ1)[ψ2c(b+d)+(e+d)(ψ1(b+α2)+ψ1(b+c)+ψ2b)]>0,Γ2=Q1+ψ2c(b+d)+(e+d)[ψ1(b+α2)+ψ1(b+c)+ψ2b]>0,Γ3=Q1+ψ2c(b+d)+(e+d)[ψ1(b+c)+ψ2b]>0,Γ4=J3Γ3>0,Γ5=(e+d)[(b+α2)J2+Q2+Q3]>0,Γ6=bA3+(b+ψ1+ψ2)Γ2+Γ3>0,Γ7=(b+ψ1)Γ5+(b+c+e+d+ψ2)(b+α2)(Q1+Q3)+(b+α2)Γ1>0.

Hence, by Lemma 3.1, all eigenvalues of J(P) have negative real part when R0>1. Thus, P is LAS.

Appendix B. Proof of Theorem 3.3

Proof of Theorem 3.3 (i). Evaluating (3.11) at P1 gives

J(P1)=ABBA,

where

A=-b-α10-βα20-b-c-α1β00c-e-d000d-b-α2

and

B=α10000α10000000000.

By Cui et al. [7], the eigenvalues of J(P1) are identical to those of A+B and A-B, where

A+B=-b0-βα20-b-cβ00c-e-d000d-b-α2,

and

A-B=-b-2α10-βα20-b-c-2α1β00c-e-d000d-b-α2.

It is found that the eigenvalues of A+B and A-B are the roots of equations

fA+B(λ)=(λ+b)(λ+b+α2)(λ2+a1λ+a2)=0,fA-B(λ)=(λ+b+2α1)(λ+b+α2)(λ2+a3λ+a4)=0,

respectively, where a1=b+c+d+e, a2=(b+c)(d+e)(1-R0), a3=(b+c+d+e+2α1), a4=(e+d)(b+c+2α1)1-βc(d+e)(b+c+2α1). It is easy to see that a1>0, a3>0 and a2>1 when R0<1. Since βc(d+e)(b+c+2α1)<R0<1 then a4>0. These imply that, using the Routh–Hurwitz criterion, all eigenvalues of A+B and A-B have negative real part. Hence P1 is LAS if R0<1.

Proof of Theorem 3.3 (ii). Evaluating (3.11) at P2 yields

J(P2)=ABBA,

where

A=-b-α1-ψ1ψ2-ψ3ψ2+α2ψ1-b-c-α1-ψ2ψ3-ψ20c-e-d000d-b-α2

and

B=α10000α10000000000.

Since A+B=J(P), by the proof of Theorem 3.2, A+B is stable if R0>1. For the matrix A-B, we have

A-B=-b-2α1-ψ1ψ2-ψ3ψ2+α2ψ1-b-c-2α1-ψ2ψ3-ψ20c-e-d000d-b-α2.

It suffices to check that matrix A-B satisfies the conditions in Lemma 3.1 as following six steps. For simplification, the entries of A-B is denoted by aij for i,j=1,2,3,4. It is obvious that aii<0 for i=1,2,3,4. Since R0=R0, ψi(i=1,2,3) give in (3.8) are positive when R0>1.

  • (i)

    A1=-(a11+a22+a33+a44)>0.

  • (ii)

    A2=J1+J2+J3>0 where J1=a44a33+a44a22+a44a11+a33a11>0, J2=(ψ2+2α1)(e+d)+cψ2>0, and J3=ψ2(b+2α1)+(b+c+2α1)(ψ1+b+2α1)>0. Thus, A2>0.

  • (iii)
    A3=Q1+Q2+Q3. Since J2>0, J3>0 and a33<0, a44<0, these yield Q1=-a44(J2+J3)>0 and Q2=-a33J3>0. For Q3=dcψ2+(b+2α1)cψ2+(e+d)[ψ1(b+α2)+α2(b+2α1)]-c(b+2α1)(e+d), it can be verified that
    Q2+Q3=cψ2(b+d+2α1)+(e+d)[ψ1(b+α2)+α2(b+2α1)]+(e+d)[ψ2(b+2α1)+ψ1(b+c+2α1)+(b+2α1)2]>0.
    Thus, A3=Q1+Q2+Q3>0.
  • (iv)

    A4=det(A-B)=(b+α2)(e+d)(b+2α1)(ψ1+ψ2)+cψ2(b+2α1)(b+α2+cd)+ψ1(b+2α1)(e+d)(b+α2+c)+cα2eψ1>0.

  • (v)
    A1A2-A3>0. Since Ji>0 for i=1,2,3, and aii<0 for i=1,2,3,4,
    A1A2-A3=-a11(J2+J3)-a22(J1+J3)-a33(J1+J2)-a44J1-a11(a44a22+a44a11+a33a11)+(b+ψ2+2α1)J2+ce(ψ2+2α1)+c2ψ2+(b+2α1)cψ3>0.
  • (vi)

    Finally, A1A2A3-A32-A12A4=(A1A2-A3)A3-A12L1+A12(-L2-L3) where L1=(b+α2)(e+d)J3, L2=dc(ψ2(b+2α1)-ψ1α2), L3=-(b+α2)(b+2α1)cψ3.

    Since
    -L2-L3=cdψ1α2+c(b+2α1)(b+α2)(βc+βR0(e+d))(b+α2)+βcdR02(b+α2)(c+d+e)+cd>0,
    and
    (A1A2-A3)A3-A12L1(b+2α1+ψ1)(e+d)Γ1+(2b+2α1+c+ψ1+ψ2)Γ4+(b+2α1+ψ1)(b+α2)Γ6+(2b+2α1+c+ψ2+e+d+α2)Γ7>0,
    where
    Γ1=(b+α2)[(e+d)(ψ1ψ2+2α1(b+2α1+ψ1))+cψ2(b+2α1+ψ1)](b+2α1+ψ1)(b+α2)J3+(b+2α1+ψ1)(cψ2(b+d+2α1))+(b+2α1+ψ1)(e+d)[ψ1(b+α2)+ψ1(b+c+2α1)]+(b+2α1+ψ1)(e+d)[ψ2(b+2α1)+2α1(b+2α1)]>0,
    Γ2=(e+d)[ψ1(b+α2)+ψ1(b+c+2α1)+ψ2(b+2α1)+2α1(b+2α1)]+Q1+cψ2(b+d+2α1)>0,
    Γ3=(e+d)[ψ1(b+c+2α1)+ψ2(b+2α1)+2α1(b+2α1)]+Q1+cψ2(b+d+2α1)>0,
    Γ4=J3Γ3>0,Γ5=(e+d)[(b+α2)J2+Q2+Q3]>0,Γ6=(b+2α1)A3+(b+2α1+ψ1+ψ2)Γ2+cΓ3>0,Γ7=(b+2α1+ψ1)Γ5+(b+c+e+d+ψ2+2α1)(b+α2)(Q1+Q3)+(b+α2)Γ1>0.

From (i)–(vi), all the eigenvalues of A-B have negative real part. Since all the eigenvalues of A-B and A+B have negative real part whenever R0>1, P2 is LAS.

Appendix C. Proof of Theorem 3.4

Proof

Evaluating the Jacobian matrix of (2.5) at Pγ gives

J(Pγ)=ABBA,

where

A=-b-α1-ψ1ψ2-ψ3ψ2+α2ψ1-b-c-α1-ψ2ψ3-ψ20c-e-d-α1000d-b-α1-α2,

and B=α1-μ1μ2-μ3μ2μ1α1-μ2μ3-μ200α10000α1, with

ψ1=βIγ(Nγ-Sγ)Nγ2=βcR0γ-12b+α2R0γ2(b+α2)(c+d+e)+cd,ψ2=βSγIγNγ2=βcR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cd,ψ3=βSγ(Nγ-Iγ)Nγ2=(βc+βR0γ(d+e))(b+α2)+βcdR0γR0γ2(b+α2)(c+d+e)+cd,μ1=γα1Iγ(Nγ-Sγ)Nγ2=γα1cR0γ-12b+α2R0γ2(b+α2)(c+d+e)+cd,
μ2=γα1SγIγNγ2=γα1cR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cd,μ3=γα1Sγ(Nγ-Iγ)Nγ2=(γα1c+γα1R0γ(d+e))(b+α2)+γα1cdR0γR0γ2(b+α2)(c+d+e)+cd,

and Nγ=Sγ+Eγ+Iγ+Rγ. The eigenvalues of J(Pγ) are equivalent to calculate the eigenvalues of A+B and A-B as in the following. First, according to Lemma 3.1, the matrix A+B:

A+B=-b-θ1θ2-θ3θ2+α2θ1-b-c-θ2θ3-θ20c-e-d000d-b-α2,

where θ1=ψ1+μ1, θ2=ψ2+μ2, θ3=ψ3+μ3, is checked into six step. For simplification, the entries of A+B are denoted by aij for i,j=1,2,3,4. It is clear that aii<0 for i=1,2,3,4.

  • (i)

    A1=-(a11+a22+a33+a44)>0.

  • (ii)

    A2=J1+J2+J3>0 since J1=a44a33+a44a22+a44a11+a33a11>0, J2=θ2(e+d+c)>0 and J3=(b+c)(b+θ1)+bθ2>0. It follows that A2=J1+J2+J3>0.

  • (iii)

    Obviously, Q1=-a44(J2+J3)>0 and Q2=-a33J3>0. Let Q3=θ2c(b+d)+(e+d)[θ1(b+α2)+bα2]-cb(e+d), it follows that Q2+Q3=θ2c(b+d)+(e+d)[θ1(b+α2)+bα2+b(b+θ1)+θ1c+θ2b]>0. Thus, A3=Q1+Q2+Q3>0.

  • (iv)

    A4=det(J)=b(e+d)(b+α2)(θ1+θ2)+cbθ2(b+α2+cd)+bθ1(e+d)(b+α2+c)+cα2eθ1>0.

  • (v)
    From (i)–(iii), it can be seen that
    A1A2-A3=-a11(J2+J3)-a22(J1+J3)-a33(J1+J2)-a44J1-a11(a44a22+a44a11+a33a11)+(b+θ2)J2+cθ2(e+c)+bcθ3>0.
  • (vi)
    Finally, from (i)-(v), it is see that
    A1A2A3-A32-A12A4=(A1A2-A3)A3-A12L1+A12(-L2-L3)
    where L1=(b+α2)(e+d)J3, L2=dc(bθ2-θ1α2), L3=-(b+α2)cθ3b and
    -L2-L3=cdθ1α2+cb((b+α2)θ3-dθ2)>cb(b+α2)2(β+γα1)c+R0γ(β+γα1)(e+d)R0γ2(b+α2)(c+d+e)+cd+cb(b+α2)(β+γα1)cdR0γ2(b+α2)(c+d+e)+cd>0,
    and
    (A1A2-A3)A3-A12L1>(b+θ1)(e+d)Γ1+(2b+c+θ1+θ2)Γ4+(b+θ1)(b+α2)Γ6+(2b+c+θ2+e+d+α2)Γ7>0,
    where
    Γ1=(b+α2)θ2(θ1(e+d)+c(b+θ1)+(b+θ1)(b+α2)J3+(b+θ1)[θ2c(b+d)+(e+d)(θ1(b+α2)+θ1(b+c)+θ2b)]>0,Γ2=Q1+θ2c(b+d)+(e+d)[θ1(b+α2)+θ1(b+c)+θ2b]>0,Γ3=Q1+θ2c(b+d)+(e+d)[θ1(b+c)+θ2b]>0,Γ4=J3Γ3>0,Γ5=(e+d)[(b+α2)J2+Q2+Q3]>0,Γ6=bA3+(b+θ1+θ2)Γ2+cΓ3>0,Γ7=(b+θ1)Γ5+(b+c+e+d+θ2)(b+θ2)(Q1+Q3)+(b+α2)Γ1>0.

By Lemma 3.1, all eigenvalues of A+B have negative real part when R0γ>1.

Next, the matrix A-B is given by

A-B=a11ϕ2-ϕ3ϕ2+α2ϕ1a22ϕ3-ϕ20ca33000da44

where ϕ1=ψ1-μ1, ϕ2=ψ2-μ2, ϕ3=ψ3-μ3, a11=-b-2α1-ϕ1, a22=-b-c-2α1-ϕ2, a33=-e-d-2α1 and a44=-b-2α1-α2. The eigenvalues of A-B are evaluated.

  • (i)
    Obviously, aii<0 for i=3,4. For 0γ1 and 0<R0γ-1<R0γ<R0γ2 when R0γ>1, it is found that
    a11=-b-ψ1-22-γcR0γ-12b+α2R0γ2(b+α2)(c+d+e)+cdα1<0
    and
    a22=-b-c-ψ2-2-γcR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cdα1<0,respectively.
    Hence, A1=-(a11+a22+a33+a44)>0.
  • (ii)

    A2=J1+J2+J3 where J1=a44a33+a44a22+a44a11+a33a11>0, J2=(e+d+2α1)(b+2α1+c)+(e+d+2α1)(β-γα1)SγIγNγ2-(β-γα1)cSγ(Nγ-Iγ)Nγ2 and J3=(b+c+2α1)(α1+ϕ1)+(b+2α1)(b+α1+ϕ2)+c(b+α1). Clearly, aii<0 for i=1,2,3,4, then J1>0. There is two cases for testing J2>0.

    Case 1: βγα1,
    J2=J2=(e+d+2α1)(b+2α1+c)+(e+d+2α1)(β-γα1)SγIγNγ2-(β-γα1)cSγ(Nγ-Iγ)Nγ2(e+d+2α1)(b+2α1+c)-(β-γα1)cSγ(Nγ-Iγ)Nγ2(e+d+2α1)(b+2α1+c)-(β+γα1)cSγ(Nγ-Iγ)Nγ2(b+c)(e+d)-(β+γα1)cSγ(Nγ-Iγ)Nγ2(β+γα1)c1R0γ-SγNγ+SγIγNγ2(β+γα1)cSγIγNγ2>0.
    Case 2: β<γα1,
    J2=(e+d+2α1)(b+2α1+c)+(e+d+2α1)(β-γα1)SγIγNγ2+(γα1-β)cSγ(Nγ-Iγ)Nγ2(e+d+2α1)(b+2α1+c)+(e+d+2α1)(β-γα1)SγIγNγ2
    (e+d)(b+c)+4α12-(e+d+2α1)(γα1)SγIγNγ22α122-γcR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cd,+(e+d)c1-γα1R0γ-1b+α2R0γ2(b+α2)(c+d+e)+cd>0.
    From case 1 and case 2, therefore, J2>0. When 0γ1 and R0γ>1, it is clear that
    α1+ϕ1=1-γcR0γ-12b+α2R0γ2(b+α2)(c+d+e)+cdα1>0,(A)andα1+ϕ2=1-γcR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cdα1>0.(B)
    Hence, J3>0.
  • (iii)
    A3=Q1+Q2+Q3 where Q1=-a44(J2+J3), Q2=-a33J3 and Q3=cd(α1+ϕ2)+(b+2α1+ϕ1)(b+2α1+α2)(e+d+2α1)-(b+2α1)cϕ3-cdα1. It can be shown that
    A3=Q1+Q2+Q3>(b+2α1)(b+c)(e+d)-c(β-γα1)Sγ(Nγ-Iγ)Nγ2>0,
    as the following two cases.
    Case 1: βγα1,
    A3(b+2α1)(b+c)(e+d)-c(β+γα1)Sγ(Nγ-Iγ)Nγ2(b+2α1)(β+γα1)cSγIγNγ2>0.
    Case 2: β<γα1,
    A3(b+2α1)(b+c)(e+d)+c(γα1-β)Sγ(Nγ-Iγ)Nγ2>0.
    From case 1 and case 2, it is clear that A3>0.
  • (iv)

    A4=det(A-B)=L1+L2+L3>0, where L1=(b+α2+2α1)(e+d+2α1)J3, L2=dc[ϕ2(b+2α1)-ϕ1α2] and L3=-(b+α2+2α1)(b+2α1)cϕ3.

    Furthermore,
    L1+L2+L3=(b+α2+2α1)(e+2α1)J3+c(b+2α1)(β-γα1)Sγ(Nγ-Iγ)Nγ2+d(b+2α1)(J2-cα1)+dα2(J3-cϕ1)>(b+2α2+2α1)(e+2α1)J3-cγα1Sγ(Nγ-Iγ)Nγ2+d(b+2α1)(J2-cα1)+dα2(J3-cϕ1)
    with
    J3+cϕ3>J3-cγα1Sγ(Nγ-Iγ)Nγ2>c(b+α1)-cγα1Sγ(Nγ-Iγ)Nγ2>cb+cα11-γα1Sγ(Nγ-Iγ)Nγ2>cb+cα11-γR0γ>0,(C)J2-cα1=(e+d+α1)(b+c+ϕ2+2α1)+α1(b+ϕ2+2α1)-cϕ3>0,J3-cϕ1=(b+2α1)(ϕ1+α1)+cα1+(b+2α1)(b+α1+ϕ2)+c(b+α1)>0.
    Thus, A4>0.
  • (v)
    From (i)–(iii), Ji>0 for i=1,2,3 and aii<0 for i=1,2,3,4. It is found that
    A1A2-A3=-(a11+a22)(J1+J2+J3)-a33(J1+J2)-a44J1-Q3>-(a11+a22)J3-a11J1-a22-Q3>-(a11+a22)J3-a11[J1-a33a44]-a11a33a44+(-a22-c)J2+cJ2-Q3>-a11a33a44-(a11+a22)J3+cJ2-Q3>c(J2-ϕ2d)+(2b+c+2α1+(ϕ1+α1)+(ϕ2+α1))J3+(b+2α1)cϕ3>c(J2-ϕ2d)+(b+2α1)(J3+cϕ3)>c(J2-ϕ2d)+(b+2α1)J3-cγα1S(N-I)N2>c(J2-ϕ2d)+(b+2α1)1-γR0γ>0,
    where
    J2-ϕ2d>(e+d+2α1)(ϕ2+α1)-ϕ2d>(e+2α1)(ϕ2+α1)+dα1>0.
    Thus, A1A2-A3>0.
  • (vi)
    Finally, it is shown that A1A2A3-A32-A12A4>0. Here,
    ϕ1=(β-γα1)cR0γ-12b+α2R0γ2(b+α2)(c+d+e)+cd,ϕ2=(β-γα1)cR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cd,ϕ3=(β-γα1)[(c+R0γ(d+e))(b+α2)+cdR0γ]R0γ2(b+α2)(c+d+e)+cd,
    it can be shown that A1A2A3-A32-A12A4>0 as the following two cases. Case 1, if β>γα1 then ϕ1>0, ϕ2>0 and ϕ3>0. It can be seen that
    A1A2A3-A32-A12A4=(A1A2-A3)A3-A12L1+A12(-L2-L3)>0,
    since
    -L2-L3>cb(b+α2)2(β-γα1)c+R0γ(β-γα1)(e+d)R0γ2(b+α2)(c+d+e)+cd+cb(b+α2)(β-γα1)cdR0γ2(b+α2)(c+d+e)+cd>0,
    and
    (A1A2-A3)A3-A12L1(b+2α1+ϕ1)(e+d+2α1)Γ1+(2b+4α1+c+ϕ1+ϕ2)Γ4+(b+2α1+ϕ1)(b+2α1+α2)Γ6+(2b+6α1+c+ϕ2+e+d+α2)Γ7>0,
    with
    Γ1=(b+α2+2α1)[(e+d+2α1)(ϕ1ϕ2+2α1(b+2α1+ϕ1))+cϕ2(b+2α1+ϕ1)]+(b+2α1+ϕ1)[(b+α2+2α1)J3+cϕ2(b+d+2α1)]+(b+2α1+ϕ1)(e+d+2α1)[ϕ1(2b+α2+c+4α1)+(ϕ2+2α1)(b+2α1)]>0,Γ2=Q1+cϕ2(b+d+2α1)+(e+d+2α1)(ϕ1(b+2α1+α2)+ϕ2(b+2α1))+(e+d+2α1)(b+c+2α1)ϕ1>0,
    Γ3=Q1+cϕ2(b+d+2α1)+(e+d+2α1)(ϕ1(b+2α1+α2)+ϕ2(b+2α1)),Γ4=J3Γ3>0,Γ5=(e+d+2α1)[(b+α2+2α1)J2+Q2+Q3]>0,Γ6=(b+2α1)A3+(b+2α1+ϕ1+ϕ2)Γ2+cΓ3>0,Γ7=(b+2α1+ϕ1)Γ5+(b+c+e+d+ϕ2+4α1)(b+α2+2α1)(Q1+Q3)+(b+α2+2α1)Γ1>0,
    Case 2, if β<γα1,
    ϕ1=-(γα1-β)cR0γ-12b+α2R0γ2(b+α2)(c+d+e)+cd<0,ϕ2=-(γα1-β)cR0γ-1b+α2R0γ2(b+α2)(c+d+e)+cd<0,andϕ3=-(γα1-β)[(c+R0γ(d+e))(b+α2)+cdR0γ]R0γ2(b+α2)(c+d+e)+cd<0.
    From (A) – (C), it is revealed that ϕ1+α1>0, ϕ2+α1>0 and J3+cϕ3>0, respectively. Next, the inequality
    A1A2A3-A32-A12A4=(A1A2-A3)A3-A12(L1+L2+L3)(D)
    is proved as follows. Calculating L2+L3, J2-J3, give
    L2+L3=dc[ϕ2(b+2α1)-(ϕ1+α1)α2]-(J3+cϕ3)(b+α2+2α1)(b+2α1)+dcα1α2+J3(b+α2+2α1)(b+2α1)=η+ν,J2-J3=(e+d+2α1)(b+c+ϕ2+2α1)-(b+c+2α1)(b+2α1)-ϕ1(b+c+2α1)-ϕ2(b+2α1)-cϕ3=(b+c+2α1)(e-b)+d(b+c+2α1+ϕ2)-ϕ1(b+c+2α1)-ϕ2b-ϕ3c>0,
    where η=dc[ϕ2(b+2α1)-(ϕ1+α1)α2]-(J3+cϕ3)(b+α2+2α1)(b+2α1)<0and ν=dcα1α2+J3(b+α2+2α1)(b+2α1)>0.Substituting L2+L3 into (D) yields
    (A1A2-A3)A3-A12(L1+ν+η)(b+2α1+ϕ1)(e+d+2α1)Γ1+(2b+4α1+c+ϕ1+ϕ2)Γ4+(b+2α1+ϕ1)(b+2α1+α2)Γ6+(2b+6α1+c+ϕ2+e+d+α2)Γ7>0,
    where
    Γ1=(b+2α1+ϕ1)A3+c(b+2α1+ϕ1)(e+d+2α1)(b+2α1+α2)-(b+α2+2α1)(e+d+2α1)J3+(ϕ1+α1)dcα2+(J3+cϕ3)(b+α2+2α1)(b+2α1)-dcϕ2(b+2α1)-dcα1α2-J3(b+α2+2α1)(b+2α1)>(b+α2+2α1)[(e+d+2α1)ϕ1ϕ2+(b+ϕ1+2α1)(2α1(e+d+2α1)+cϕ2)]+(ϕ1+α1)(b+ϕ1+α1)(e+d+2α1)(b+α2+2α1+c)+(b+2α1)(ϕ1+ϕ2+2α1)(b+ϕ1+α1)(e+d+2α1)+(ϕ1+α1)(b+α2+2α1)J3>0,Γ2=(b+2α1+α2)[J2+J3-(b+2α1)(e+d+2α1)]+(e+d+2α1)J3+Q3>(b+2α1+α2)[2α1(b+c)+(b+c+2α1)(α1+ϕ1)+(b+2α1)(b+α1+ϕ2)]+c(b+α1)(b+2α1+α2)>0,
    Γ3=Γ2+c(γα1-β)R0γ-12b+α2(e+d+2α1)(b+2α1+α2)R0γ2(b+α2)(c+d+e)+cd>0,Γ4=J3Γ3>0,Γ5=(e+d+2α1)[(b+α2+2α1)J2+Q2+Q3]+(ϕ1+α1)dcα2+(J3+cϕ3)(b+α2+2α1)(b+2α1)-dcϕ2(b+2α1)-dcα1α2-J3(b+α2+2α1)(b+2α1)>(b+α2+2α1)(e+2α1)(J2-J3)+(e+d+2α1)(Q2+Q3)+dc2(γα1-β)R0γ-1b+α2(b+2α1)R0γ2(b+α2)(c+d+e)+cd>0,Γ6=(b+2α1)A3+(b+2α1+ϕ1+ϕ2)Γ2+cΓ3+(ϕ1+α1)dcα2+(J3+cϕ3)(b+α2+2α1)(b+2α1)-dcϕ2(b+2α1)-dcα1α2-J3(b+α2+2α1)(b+2α1)>(b+2α1)((b+α2+2α1)J2+Q2+Q3)+(b+2α1+ϕ1+ϕ2)Γ2+cΓ3>0,Γ7=(b+c+e+d+ϕ2+4α1)[(b+α2+2α1)(Q1+Q3)-ν-η]+(b+2α1+ϕ1)Γ5+(b+α2+2α1)Γ1>(b+c+e+d+ϕ2+4α1)(b+α2+2α1)α2J3>0.

Thus, A1A2A3-A32-A12A4>0. By Lemma 3.1, all the eigenvalues of A-B have negative real part. Therefore, it can be concluded that all the eigenvalues of A+B and A-B have negative real part. These imply that Pγ isLAS when R0γ>1.

References

  • 1.Allen L.J.S. Pearson Education Ltd.; USA: 2007. An Introduction to Mathematical Biology. [Google Scholar]
  • 2.Anderson R.M., May R.M. Oxford University Press; London, NewYork: 1991. Infectious Diseases of Humans, Dynamics and Control. [Google Scholar]
  • 3.J. Arino, Diseases in metapopulations, in: Modeling and Dynamics of Infectious Diseases, in: Ser. Contemp. Appl. Math. CAM, vol. 11, Higher Ed. Press, Beijing, 2009, pp. 64–122.
  • 4.Arino J., van den Driessche P. A multi–city epidemic model. Math. Popul. Stud. 2003;10:175. [Google Scholar]
  • 5.Chowella G., Fenimorea P.W., Castillo-Garsowc M.A., Castillo-Chavez C. SARS outbreaks in Ontario, Hong Kong and Singapore: the role of diagnosis and isolation as a control mechanism. J. Theor. Biol. 2003;224:1. doi: 10.1016/S0022-5193(03)00228-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Cooke K., van den Driessche P. Analysis of an SEIRS epidemic model with two Delays. J. Math. Biol. 1990;35:240. doi: 10.1007/s002850050051. [DOI] [PubMed] [Google Scholar]
  • 7.J. Cui, Y. Takeuchi, Y. Saito, Spreading disease with transport-related infection, J. Theor. Biol. 239 (206) 376–390. [DOI] [PubMed]
  • 8.Diekmann O., Metz J.A.J., Heesterbeek J.A.P. On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. J. Math. Biol. 1990;28:365. doi: 10.1007/BF00178324. [DOI] [PubMed] [Google Scholar]
  • 9.C.A. Donnelly et al., Epidemiological determinants of spread of cusal agent of severe acute respiratory syndrome in Hong Kong, Lancet, 2003, http://image.thelancet.com/extras/03art4453-web.pdf [DOI] [PMC free article] [PubMed]
  • 10.Fulford G.R., Roberts M.G., Heesterbeek J.A.P. The metapopulation dynamics of an infectious disease: tuberculosis in possums. J. Theor. Biol. 2002;61:15. doi: 10.1006/tpbi.2001.1553. [DOI] [PubMed] [Google Scholar]
  • 11.Grenhalgh D. Some results for an SEIR epidemic model with density dependence in the death rate. IMA J. Math. Appl. Med. Biol. 1992;9:67. doi: 10.1093/imammb/9.2.67. [DOI] [PubMed] [Google Scholar]
  • 12.Greenhalgh D. Hopf bifurcation in epidemic models with a latent period and nonpermanent immunity. Math. Comput. Model. 1997;25:85. [Google Scholar]
  • 13.Gumel A.B. Modelling strategies for controlling SARS outbreaks. Proc. Roy. Soc. B. 2004;271:2223. doi: 10.1098/rspb.2004.2800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Khan K., Arino J., Hu W., Raposo P., Sears J., Calderon F., Heidebrecht C., Macdonald M., Liauw J., Chan A., Gardam M. Spread of a novel influenza a (H1N1) virus via global airline transportation. N. Engl. J. Med. 2009;361(2):212. doi: 10.1056/NEJMc0904559. [DOI] [PubMed] [Google Scholar]
  • 15.Murray G.D., Cliff A.D. A stochastic model for measles epidemics in a multi–region setting. Inst. Br. Geog. 1975;2:158. [Google Scholar]
  • 16.Li M.Y., Muldoweney J.S. Global stability for SEIR modle in epidemiology. Math. Biosci. 1995;125:155. doi: 10.1016/0025-5564(95)92756-5. [DOI] [PubMed] [Google Scholar]
  • 17.Li M.Y., Muldoweney J.S. Global stability of a SEIR epidemic model with vertical transmission. SIAM J. Appl. Math. 2001;62:58. [Google Scholar]
  • 18.Li M.Y., Muldoweney J.S., Wang L.C., Karsai J. Global dynamics of an SEIR epidemic model with a varying total population size. Math. Biosci. 1999;160:191. doi: 10.1016/s0025-5564(99)00030-9. [DOI] [PubMed] [Google Scholar]
  • 19.Lipsitch M. Transmission dynamics and control of severe acute respiratory syndrome. Science. 2003;300:1966. doi: 10.1126/science.1086616. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Liu X., Takeuchi Y. Spread of disease with transport-related infection and entry screening. J. Theor. Biol. 2006;242:517. doi: 10.1016/j.jtbi.2006.03.018. [DOI] [PubMed] [Google Scholar]
  • 21.Liu J., Zhou Y. Global stability of an SIRS epidemic model with transport-related infection. Chaos, Solitons & Fractals. 2009;40:145. [Google Scholar]
  • 22.Liu J., Zhou Y. Global stability of an SIRS epidemic model with transport-related infection. Chaos, Solitons & Fractals. 2009;40:145. [Google Scholar]
  • 23.Longini I. A mathematical model for predicting the geographic spread of new infectious agents. Math. Biosci. 1988;90:367. [Google Scholar]
  • 24.Ruan S., Wang W., Levin S.A. The effect of global travel on the spread of SARS. Math. Biosci. Eng. 2006;3(1):205. doi: 10.3934/mbe.2006.3.205. [DOI] [PubMed] [Google Scholar]
  • 25.Rvachev L., Longini I. A mathematical model for the global spread of influenza. Math. Biosci. 1985;75:3. [Google Scholar]
  • 26.Sattenspiel L., Dietz K. A structured epidemic model incorporating geographic mobility among cities. Math. Biosci. 1995;128:71. doi: 10.1016/0025-5564(94)00068-b. [DOI] [PubMed] [Google Scholar]
  • 27.Takeuchi Y., Liu X., Cui J. Global dynamics of SIS models with transport-related infection. J. Math. Anal. Appl. 2007;329:1460. [Google Scholar]
  • 28.Van den Driessche P., Watmough J. Reproduction numbers and sub–threshold endemic equilibria for compartmental models of disease transmission. Math. Biosci. 2002;180:29. doi: 10.1016/s0025-5564(02)00108-6. [DOI] [PubMed] [Google Scholar]
  • 29.Wan H., Cui J. An SEIS epidemic model with transport-related infection. J. Theor. Biol. 2007;247:507. doi: 10.1016/j.jtbi.2007.03.032. [DOI] [PubMed] [Google Scholar]
  • 30.Wang W., Zhao X.-Q. An epidemic model in a patchy environment. Math. Biosci. 2004;190(1):97. doi: 10.1016/j.mbs.2002.11.001. [DOI] [PubMed] [Google Scholar]
  • 31.Wang W., Mulone G. Threshold of disease transmission in a patch environment. J. Math. Anal. Appl. 2003;285:321. [Google Scholar]
  • 32.Wang W., Ruan S. Simulating the SARS outbreak in Beijing with limited data. J. Theor. Biol. 2004;227:369. doi: 10.1016/j.jtbi.2003.11.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.A. Wilder-Smith, The severe acute respiraltory syndrome: impact on travel and tourism, Travel Med. Infect. Dis. 4 (2006) 53–60. [DOI] [PMC free article] [PubMed]
  • 34.World Health Organization, Severe acute respiratory syndrome (SARS): status of the outbreak and lessons for the immediate future, Geneva, May 20, 2003.
  • 35.World Health Organization, Severe acute respiratory syndrome (SARS): status of the outbreak and lessons for the immediate future, Geneva, May 20, 2003.
  • 36.Zhang J., Ma Z. Global stability of SEIR model with saturating contact rate. Math. Biosci. 2003;185:15. doi: 10.1016/s0025-5564(03)00087-7. [DOI] [PubMed] [Google Scholar]

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