# An intuitive formulation for the reproductive number for the spread of diseases in heterogeneous populations

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2 66 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 disease is introduced into the population. The threshold conditions are characterized by the socalled reproductive number, the reproduction number, the reproductive ratio, basic reproductive value, basic reproductive rate, or contact number, commonly denoted by R in mathematical epidemiology [5,1,17,19±21,23,29,35,39,43]. The concept of R, introduced by Ross in 199 [39], is de ned in epidemiological modeling such that if R < 1, the modeled disease dies out, and if R > 1, the disease spreads in the population. There have been intensive studies in the literature to calculate R for a wide class of epidemiological models of infectious diseases [6,8,9,12,17,18,25,26,28,3,32±34,41]. In mathematical models, the reproductive number is determined by the spectral radius of the next-generation operator in continuous models and, in particular, is determined by the dominant eigenvalue of the Jacobian matrix at the infection-free equilibrium for models in a nite-dimensional space [8,9,24,27]. It can also be obtained, in certain models, by suitable Lyapunov functions [28,41]. The biological meaning of the reproductive number is the average number of secondary cases produced by one infected individual during the infected individual's entire infectious period when the disease is rst introduced. Let r be the average number of contacts per unit of time per individual, b be the probability of transmitting the infection per contact, and s be the mean duration of the infectious period. Then the reproductive number can be estimated by the following intuitive formula: R ˆ rbs: 1:1 This formula can give insight into the transmission dynamics of infectious diseases for various relatively simple epidemiological models [3±5,7,4]. For simple homogeneous models, it is easy to de ne r, b, and s. For example, consider a simple homogeneous AIDS model governed by the following system of ordinary di erential equations: ds dt ˆ l S S t k t S t ; di ˆ k t S t l m I t ; dt da dt ˆ mi t da t ; where S, I, and A denote the individuals susceptible to infection, the infected individuals, and the AIDS cases, respectively; ls is the input ow into the susceptible group; l the removal rate; m the rate of contracting AIDS; d the removal rate due to the death from AIDS or other reasons; and k is the rate of infection given by I t k t ˆbr S t I t : Here, b is the transmission probability per contact and r is the average number of contacts per individual per unit of time. We assume here that transmission by the AIDS cases is neglected. To focus our attention on the issues we will address, we assume, for simplicity, that the mixing is proportional for this model and other models in this paper. The system has the infection-free equilibrium S ;. The stability of S ; determines the reproductive number as

3 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 67 R ˆ rb l m : Formula (1.1) then holds when we de ne the duration of infection as s ḓef 1= l m. (We will use the symbol ḓef to indicate that the equation is the de nition of a quantity.) However, as more heterogeneous structures or subgroups for the infected population are included in an epidemiological model, the calculation of R becomes more complicated, and it is di cult to nd an explicit formula for R. Even when an explicit formula can be obtained, it is not always clear whether it is appropriate to de ne a mean contact rate, a mean duration of infection, and a mean transmission probability so that the reproductive number can still be estimated by formula (1.1). Furthermore, even if it can be claimed that such an estimate is adequate, a deep understanding of the model is absolutely necessary so that those means can be well de ned. Moreover, for models of the diseases for which di erentiation of the contact rates or the partner acquisition rates must be addressed, such as sexually transmitted disease (STD) models, not only the mean but also the second moment or the variance about the mean must be taken into account. Then, formula (1.1) can no longer be applied. For certain simple models, a more accurate formula for the reproductive number is R ˆ r r2 bs; 1:2 r where r is the mean number of contacts per individual and r is the variance or standard deviation of the mean number of contacts [1±3,5,8,28,36]. Formula (1.2) is an e ective formulation for providing insight into the transmission dynamics of diseases. Unfortunately, as more heterogeneities are considered, it becomes impracticable to de ne the variance or the standard deviation, and expression (1.2) becomes inadequate. For risk-group models, Hethcote and Yorke [23] rst introduced and Jacquez et al. [28,29] speci ed the idea of de ning a mean reproductive number as the average number of infected individuals generated per infected individual over the duration of the infected state. They de ned a reproductive number for each subgroup and then express the mean reproductive number as a weighted mean of those group reproductive numbers. In this paper, we use the models in [26] as a basis and formulate new heterogeneous models to demonstrate how di erent cases can be treated so that an appropriate reproductive number can be estimated. We show that for models with no risk structure, that is, the models with a homogeneous susceptible population in the contact rates, it is still possible to de ne the mean quantities and to apply formula (1.1). We show, however, for susceptible populations with heterogeneous structure such as risk structure and age structure, it is more appropriate to de ne a reproductive number for each subgroup or each cohort and then express the reproductive number for the whole population as the weighted average of those reproductive numbers for the subgroups or cohorts. 2. Models without risk structure We rst consider the models in which the risk level is assumed to be uniform for all the susceptible individuals. The susceptible population may still be divided into subgroups, but they are not based on the risk level, that is, the number of partners, or the number of contacts.

4 68 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65± Di erential infectivity models There is evidence that HIV serum and plasma levels or individual variations a ect transmission, that infected individuals have di erent levels of virus after the acute phase, and that those with high levels progress to AIDS more rapidly than those with low levels in clinical studies. As a result, a hypothesis that some individuals are highly infectious over long periods of time and a new model that accounts only for di erences between infected individuals, referred to as a di erential infectivity (DI) HIV model, were proposed in [26]. In that DI model, it is assumed that individuals enter a speci c group when they become infected and stay in that group until they are no longer involved in transmitting the disease. Their infectivity and progression rates to AIDS are assumed to depend upon which group they are in; the susceptible population is assumed to be homogeneous; and variations in susceptibility, risk behavior, and many other factors associated with the dynamics of the spread of HIV are neglected. In this section, we use the simple DI model formulated in [26] and generalize it to a model in which the risk level of infected individuals depends on the group to which they belong. We demonstrate how a mean number of contacts, a mean transmission probability, and a mean duration of infection can be de ned so that formula (1.1) can be used to obtain the reproductive number. The following DI model with homogeneous contact rate was formulated for HIV transmission in [26] ds dt ˆ l S S ks; di i dt ˆ p iks l m i I i ; i ˆ 1;...; n; 2:1 da dt ˆ Xn m j I j da; where the infected population is subdivided into n subgroups, I 1 ; I 2 ;...; I n. Upon infection, an individual enters subgroup i with probability p i and stays in this group until becoming inactive in transmission, where P n p i ˆ 1. The variable A denotes the group of individuals removed from the population due to end stage disease or behavioral changes. Individuals in A are assumed to die at a rate d P l. The rate m i of leaving the infected population because of behavioral changes induced by either HIV-related illnesses or testing positive for HIV (presumably changing behavior so as not to transmit infection) depends on the subgroups. The rate of infection k depends on the transmission probability per contact of individuals in subgroup i, b i, the proportion of individuals in the subgroup, I i =N, and the number of contacts of an individual per unit of time r, so that k t ˆr Xn b i I i t N t ; where N t ˆS t P n I j t.

5 The reproductive number for this model is R ˆ r Xn p i b i : l m i By de ning the mean duration of infectiousness for infected individuals and the mean probability of transmission as Xn ḓef s p i ; ḓef 1 X n b l m i s p i b i l m i ; respectively, the reproductive number can be expressed as the product of the number of contacts and these two means R ˆ rbs: Now we generalize the DI model (2.1) by assuming that the number of contacts per individual per unit of time depends on the subgroups, because people may change their behavior according to how ill they are. Let r i be the average number of contacts per individual per unit of time in subgroup i. Then the rate of infection is generalized to k t ˆr Xn r i I i t b i rs t P n r ji j t ; where r is the contact rate of the susceptible individuals and r i is the contact rate of infected individuals in subgroup. We refer to model (2.1) with the generalized infection rate as a general DI model. Similarly as in [26], a simple stability analysis for the infection-free equilibrium gives the reproductive number for the general DI model as R ˆ Xn p i r i b i : l m i The mean duration of infectiousness for infected individuals in this general DI model is the same as for model (2.1). Since r i = l m i is the average number of contacts per individual in group i made during the whole infection period, the total average number of contacts per infected individual during the whole infection period is r total ḓef Xn p i r i ; l m i and hence the mean number of contacts per infected individual per unit time for the general DI model, denoted by r, is r ḓef r total s ˆ 1 X n s J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 69 p i r i l m i : The total transmission probability through all contacts with infected individuals in subgroup i during the entire time period when they are infected is

6 7 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 b total i ḓef b i r i l m i : Hence, the mean probability per contact per unit of time for the general DI model, denoted by b, is Xn ḓef b p i b total i rs ˆ 1 X n rs p i r i b i l m i : Therefore, R ˆ r bs: 2.2. The staged progression models A common mathematical model for the spread of AIDS assumes that infected individuals pass through several stages, being highly infectious in the rst few weeks after becoming infected, then having low infectivity for many years, and nally becoming gradually more infectious as their immune systems break down, and they progress to AIDS, with the rates of progression to AIDS being also very low in the rst few years after infection. Based on this hypothesis, epidemiological models that we refer to as staged progression (SP) models have been studied by many researchers (see the references in [26]) The general discrete SP model The following SP model with a homogeneous contact rate is studied in [26]. It assumes that the susceptible population is homogeneous and is maintained by the same type of in ow. It assumes that the population of infected individuals is subdivided into subgroups I 1 ; I 2 ;...; I n with di erent infection stages such that infected susceptible individuals enter the rst subgroup I 1 and then gradually progress from this subgroup to subgroup I n. Let c i be the average rate of progression from subgroup i to subgroup i 1, for i ˆ 1;...; n 1, and let c n be the rate at which infected individuals in subgroup I n become sexually inactive or no longer infectious due to end-stage disease or behavioral changes. The dynamics of the transmission are governed by the following system: ds dt ˆ l S S ks; di 1 dt ˆ ks c 1 l I 1 ; di i dt ˆ c i 1I i 1 c i l I i ; 2 6 i 6 n; 2:2 da dt ˆ c ni n da; where the infection rate k is given by

7 k ˆ r Xn b i I i N : Here, r is the average number of contacts per individual per unit time, b i the transmission probability per contact with an individual in subgroup i, d P l the removal rate of individuals in group A, and N ˆ S P n I. Notice again that the transmission by the A group is neglected just as it was in model (2.1). The reproductive number for model (2.2) with (2.3) is de ned by R ˆ r Xn b i q i ; l c i where q i ḓef Yi 1 c j l c j : The mean duration of infection is de ned by Xn ḓef s q i l c i ; and the mean probability of transmission per partner from an infected individual during the course of infection is de ned by b ḓef 1 X n s b i q i c i l : Then, the reproductive number is again expressed as R ˆ r bs: (See [26] for details.) Instead of assuming that the all infected individuals have the same contact rate, we now assume that infected individuals with di erent stages may have di erent rates of contacts because of possible changes in behavior. Then the infection rate is given by k ˆ r Xn r i I i b i rs P n r : 2:4 ji j Here, r is the average number of contacts per susceptible individual per unit of time, r i the average number of contacts per infected individual with stage i per unit of time, b i the transmission probability per contact with an infected individual in subgroup i, and d is the removal rate of individuals in group A. The reproductive number for the general SP model given by (2.2) and (2.4) can be de ned as R ˆ Xn r i b i q i : l c i J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65± :3 The mean duration of infection for this model is the same as that for the SP model (2.2) with (2.3).

8 72 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 The term r i q i = l c i is the number of contacts per infected individual during the individual's infection period in subgroup i. Then the total number of contacts that an infected individual makes during all of the individual's infection period is X n r i q i ḓef r total : l c i Hence, the average number of contacts per infected individual per unit of time is r ḓef r total s ; so that r total ḓef rs. The transmission probability through all contacts with an infected individual in subgroup i is b i r i q i = l c i. Then the total transmission probability from all contacts with an infected individual during the individual's entire infection period, denoted by b total, can be de ned as b total ḓef Xn b i r i q i : l c i Hence, the average transmission probability per contact is b ḓef b total ˆ 1 X n b i r i q i ; r total rs l c i and the reproductive number can be expressed as R ˆ r bs: The continuous SP model In this section, we consider a simple SIR (susceptible±infected±removed) STD model with continuous infection stages (see [25,42] for further references). Let u be the infection age, and denote the distribution functions of susceptible, infected, and removed individuals by S t, I t; u, and R t, respectively. We again neglect the transmission by the group of removed individuals, assuming that they are a small portion of the infected population and that they are less active in transmitting the disease. We also neglect migration between populations and assume that the only recruitment into the population is a constant in ow of susceptible individuals and that all infected individuals are infectious and will eventually be removed. Under these assumptions, the dynamics of the population are governed by the following system of equations and associated boundary conditions: ds dt ˆ l S S k t S; oi ot oi ˆ l c u I; ou I t; ˆk t S;

9 I ; u ˆW u ; dr dt ˆ dr c s I t; u du; where l is the attrition rate caused by natural death or movement out of the sexually active population, k the infection rate, ls the rate at which individuals migrate into the population, c the removal rate of infected individuals, d the death rate of individuals in the removed group, and W is the initial distribution of the infected population. We consider the infection rate that can be represented as I t; u k t ˆr b u r u r S t R 1 du: 2:6 r v I t; v dv Here we assume that the individuals at di erent infection ages have di erent activity levels such that r u is the number of contacts that an infected individual with infection age u has, r the number of contacts that a susceptible individual has, and b u is the probability that an infected partner with infection age u will infect a susceptible partner. By linearizing S t and I t; u about S ; and assuming the solutions initially change exponentially, a characteristic equation can be obtained. Analyzing the characteristic equation to locate the eigenvalues of the equation in the left-half complex plane yields the following formula for the reproductive number for the model governed by (2.5) and (2.6): Z u R ˆ r u b u exp lu c w dw du: 2:7 (Details of the derivation of formula (2.7) can be found in Appendix A.) It is similar to the discrete SP models that the mean duration of infection is Z u s ḓef exp lu c w dw du; the total contact rate is r total ḓef r u exp lu the mean number of contacts is r ḓef r total s ˆ 1 s r u exp Z u lu the total transmission probability is r u b u exp lu b total ḓef c w dw du; Z u Z u and then the mean probability of transmission is b ḓef b total ˆ 1 r u b u exp lu r total rs J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 73 c w dw du; c w dw du; Z u c w dw du: 2:5

10 74 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 Therefore, the reproductive number can be again expressed as R ˆ r bs: 2.3. The di erential susceptibility model We have shown in Section 2.1 that for the DI model and the SP models, in so far as we assume a homogeneous susceptible population such that there is one group of susceptible individuals, the mean number of contacts, the mean transmission probability, and the mean duration of infection can be de ned so that the reproductive number can be always given as the product of these three means. In this section, we consider a simple di erential susceptibility (DS) model in which the infected population is homogeneous, but the susceptible population is divided into n groups according to their susceptibilities. The model equations are given by ds i dt ˆ l S i S i k i S i ; di dt ˆ Xn kˆ1 k k S k l c I; da ˆ ci da: dt The rate of infection is k i ˆ rbi N a i; i ˆ 1;...; n; 2:9 where a i is the susceptibility of susceptible individuals in subgroup i, b the infectious rate of infected individuals, r the average number of contacts per sexually active individual, and N ˆ Pn S i I. By the local stability analysis of the infection-free equilibrium, the reproductive number for model (2.8) with (2.9) can be de ned as R ˆ rb P n a isi l c P n : S i Since there is only one group of infected individuals, the mean duration is s ḓef 1= l c. The biological de nition of the reproductive number is the number of secondary cases produced when a primary case is introduced into a totally susceptible population. Hence, the mean susceptibility of susceptible individuals in all the groups, denoted by a, should be weighted by all susceptible groups at the infection-free equilibrium. That is, 2:8 P n a ḓef a isi P n S i ; and hence the total mean infectivity is b ḓef ba. With these notations, the reproductive number can be rewritten as R ˆ rbs:

11 2.4. The combined DS and DI models We showed in Section 2.3 that even if the susceptible population is divided into subgroups, whereas there is a homogeneous infected population, we can still de ne the mean infectivity, and the reproductive number can be given by the compact and intuitive formula. Now if the infected population is divided into subgroups based on their di erent infectivities and the average numbers of contacts of infected individuals in the infected subgroups are distinct, can those means be well de ned and the reproductive number still be the product of those means? We combine the DS and DI models and derive the formula of the reproductive number as follows. Divide the susceptible population into n groups according to their susceptibilities and the infected population into m groups based on their infectivities and how ill they are. Then we have the following system of equations: ds i dt ˆ l S i S i k i S i ; i ˆ 1;...; n; di j dt ˆ Xn p kj k k S k l m j I j ; j ˆ 1;...; m; 2:1 kˆ1 da dt ˆ Xm kˆ1 m k I k da; where the fractions satisfy P m p kj ˆ 1, k ˆ 1;...; n. The rate of infection is k i ˆ ra i X m b j J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 75 r j I j r P n lˆ1 S l P m kˆ1 r ; ki k 2:11 where r is the mean number of contacts per susceptible individual, r j the average number of contacts per infected individual in subgroup j, a i the susceptibility of the susceptible individuals in subgroup i, and b j is the infectiousness of the infected individuals in subgroup j. By investigating the stability of the infection-free equilibrium, the reproductive number for the model given by (2.1) and (2.11) can be de ned by R ˆ Xm X n kˆ1 p kj a k Sk r jb j l m j P n : 2:12 lˆ1 S l (The detailed proof of formula (2.12) is given in Appendix B.) The infected individuals in each subgroup are infected from all susceptible subgroups. Their mean duration of infection needs to be weighed by the fractions and the sizes of susceptibles at the infection-free equilibrium. Denote the mean duration of infection by s. Then Xn ḓef s 1 l m j P m kˆ1 p kjs k P n lˆ1 S l : The term r j = l m j is the number of contacts per infected individual in group j during the whole duration of infection. Then,

12 76 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 X n kˆ1 r j p kj Sk P l m j n lˆ1 S l is the average number of contacts per infected individual in subgroup j during the whole infection period with susceptible individuals that induce the transmission of infection. Summing them over and dividing by the mean duration of infection gives the mean number of contacts per infected individual over all infected subgroups per unit of time r. That is, r ḓef 1 s X m X n kˆ1 r j p kj Sk P l m j n : lˆ1 S l The term r j b j = l m j is the total infectivity per infected individual in subgroup j through all contacts during the whole infection period. Since transmission of a disease results from the infectivity of infected individuals and the susceptibility of susceptible individuals, the probability of transmission per contact from an infected individual in subgroup j with all susceptible individuals during the whole infection period is r j b j l m j X n kˆ1 p kj a k Sk P n : lˆ1 S l Again, summing over all subgroups of infected individuals and dividing by the mean number of contacts and the mean duration of infection yields the mean probability of transmission b ḓef 1 X m r j b j X n p kj a k Sk P sr l m n ˆ 1 j kˆ1 lˆ1 S l sr R : Therefore, the reproductive number can be rewritten as R ˆ r bs: 3. The segregated risk DI model In this section, we consider a segregated risk DI model. We divide the susceptible population into n groups based on their risk behavior. Then, each risk-based infected population group is further subdivided into m subgroups. Upon infection, a susceptible individual in the risk-group S i enters infected subgroup Ij i with probability p j and stay in this subgroup until becoming inactive in transmission, where P m p j ˆ 1. The rate at which infected individuals are removed from subgroup Ij i to the group of removed individuals, R, ismi j. Again, we assume that individuals in group R are no longer actively transmitting disease. The model is then de ned by the following system: ds i dt ˆ l S i S i k i S i ; i ˆ 1;...; n; di i j dt ˆ p jk i S i l m i j I i j ; j ˆ 1;...; m; 3:1 dr dt ˆ Xn X m m i j Ii j dr;

13 where l is the removal rate, including the natural death rate and other rates at which people leave the investigated population, lsi the recruitment of new susceptible individuals into the population with risk i, and d is the death rate of individuals in group R. The rate of infection for the individuals with risk i, k i, for proportional mixing, is de ned by P m k i ˆ r b P n j r iij i i P n kˆ1 r k S k P m ; 3:2 lˆ1 Ik l where b j is the infectivity of the individuals in the infected subgroup Ij i and is assumed to be independent of their risk level. The reproductive number for model (3.1) with (3.2) can be de ned by R ˆ Xn r 2 i S i P n lˆ1 r ls l X m p j b j : 3:3 l m i j (We give a complete derivation of formula (3.3) in Appendix C.) Note that if the removal rates m i j ˆ m j are independent of risk level, then the reproductive number becomes R ˆ Xm p j b j l m j X n J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 77 ri 2S i P n lˆ1 r : 3:4 lsl The term P m p jb j = l m j is the product of the mean duration of infection and the mean transmission probability. This R in (3.4) involves the second mean of the risk level P n r2 i S i.as Diekmann et al. pointed out in [8], P n r2 i S i P n lˆ1 r ˆ mean variance lsl mean : Hence, (3.4) is consistent with the results in [8,11,37]. However, if the removal rates are not risk-level independent, it is unclear how to de ne the mean duration of infection and the mean transmission probability. Here we provide an alternative way to make the formula of the reproductive number more intuitive. De ne the mean duration of infectivity for infected individuals with risk level i by s i ḓef Xm p j ; l m i j the mean probability of transmission per partner from those infected individuals by ḓef 1 X b m p j b j i ; s i l m i j and the reproductive number for the subgroup with risk level i by R i ḓef r i bi s i : Then the reproductive number can be rewritten as

14 78 J.M. Hyman, J. Li / Mathematical Biosciences 167 (2) 65±86 R ˆ Xm r i Si P m lˆ1 r R i lsl : Here, r i Si is the total number of contacts of an individual in the group with risk level i. Then the reproductive number for the whole population is equal to the mean reproductive numbers of the risk groups weighted by their risks. 4. A simple age-structured model We consider a simple SIR model with age structure in this section (see [33]). Denote the distribution functions of susceptible, infected, and removed individuals by S t; a, I t; a, and R t; a, respectively, where t is the time and a is the age. We neglect transmission of the virus by group R. We also neglect migration between populations and assume that the only recruitment into the population is a constant in ow of susceptible individuals. Under these assumptions, the dynamics of the population are governed by the following system of equations and associated boundary conditions: os ot os ˆ K a l a k t; a S; oa S t; a ˆB; S ; a ˆU a ; oi ot oi ˆ l a c a I k t; a S; oa I t; a ˆ; I ; a ˆW a ; or ot or ˆ d a R c a I; oa R t; a ˆ; R ; a ˆ; 4:1 where l is the attrition rate due to natural death or movement out of the sexually active population, k the infection rate, B the number of individuals in the susceptible class at age a, K the rate at which individuals ow into the population at ages greater than a, c the removal rate, d is the death rate in group R, and U and W are the initial distributions of the susceptible and infected populations. We consider the infection rate that can be represented as k t; a ˆ a b a; a p t; a; a I t; a N t; a da ;

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