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Ecological Modelling 150 (2002) 45 53

A mathematical model for the control of diseases in wildlife

populations: culling, vaccination and fertility control
G.C. Smith *, C.L. Cheeseman
Central Science Laboratory, Sand Hutton, York, YO41 1LZ, UK

Received 19 February 2001; received in revised form 18 September 2001; accepted 18 October 2001


Recent advances have permitted the red fox (Vulpes 6ulpes) to be vaccinated against rabies in order to control the
European epidemic. Vaccination is also the preferred long-term strategy for controlling bovine tuberculosis (My-
cobacterium bo6is) (TB) in the European badger (Meles meles) in England. We discuss a model to compare the
efficacy of various disease control strategies, including temporary and permanent sterilisation. By using rabies and TB
as examples of acute and chronic diseases, the model shows that lethal control can be more effective at disease
eradication in an isolated population than vaccination. This is due to the birth of larger numbers of susceptible
individuals during a vaccination campaign, which makes it harder to keep the population below the critical threshold
density. This difference was very marked for the progressive disease of tuberculosis. The inclusion of an abortifacient
increased the chances of disease control to levels close to that of lethal control. If the abortifacient is replaced by a
permanent contraceptive then the chances of disease eradication and population extinction were very similar to that
of lethal control, since the birth of susceptibles is now much reduced. These results are also of relevance in the control
of wildlife diseases in threatened populations or species. 2002 Elsevier Science B.V. All rights reserved.

Keywords: Fox; Rabies; Badger; Bovine TB; Disease control; Vaccination

1. Introduction scale vaccination has caused the number of cases

of rabies to significantly decline in recent years
Following decades of control by gun and fumi- (WHO, 1990 2001). The subsequent recovery of
the fox populations in Europe has resulted in
gation (Aubert, 1994), recent advances have per-
higher density populations which, ironically, may
mitted the red fox (Vulpes 6ulpes) to be vaccinated
be more susceptible to further rabies outbreaks
against rabies in order to control this modern
which are harder to eradicate (Muller, 1995;
epidemic (Brochier et al., 1991; Flamand et al., Suppo et al., 2000). The same is true of the high
1992; Winkler and Bogel, 1992). In Europe, large- density rabies-naive populations in the UK, where
modelling work has suggested that a combined
* Corresponding author. Tel.: + 44-1904-462-056; fax: + strategy of central poison baiting, with a ring of
44-1904-462-111. vaccine bait can successfully eradicate an out-
E-mail address: (G.C. Smith). break of the disease (Smith, 1995), although

0304-3800/02/$ - see front matter 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 3 0 4 - 3 8 0 0 ( 0 1 ) 0 0 4 7 1 - 9
46 G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553

targeting vaccine baits around natal dens may dX X

= b(X+ Y) d(N) iIX pX, (1)
help redress the situation (Vuillaume et al., 1997). dt N
The control of bovine tuberculosis (Mycobac-
terium bo6is), TB, in the European badger (Meles where the change in the number of healthy ani-
meles) in the UK has relied on various forms of mals, X, is due to births, b, from both healthy and
lethal control since its inception in 1975. How- infected (X + Y) animals, density-dependent death
ever, vaccination has become the preferred future (d(N)X/N see below), infection of healthy ani-
control strategy (Newell and Hewinson, 1995; mals, iIX, and culling, pX;
Krebs et al., 1997) although there are some reser- dY Y
vations as to its eventual effectiveness (Neal and =iIX d(N) |Y pY, (2)
dt N
Cheeseman, 1996). Unlike rabies, TB is not neces-
sarily fatal and some individuals may remain in- where the change in the number of infected, or
fectious for a number of years (Cheeseman et al., latent, animals, Y, is due to newly infected ani-
1988; Wilkinson et al., 2000). mals, iIX, density-dependent death (d(N)Y/N),
Recently there has been an interest in con- animals becoming infectious (1/| equals the incu-
trolling populations by reducing their fertility by bation period), and culling, pY;
using suitable baits (Caughley et al., 1992) or viral dI I
agents (Barlow, 1994). Two approaches are cur- = |Y d(N) hI pI, (3)
dt N
rently being studied in foxes: chemical compounds
which act as an abortifacient (Marks et al., 1996) where the change in the number of infectious
and immunocontraceptives capable of rendering animals, I, is due to new infection, |Y, density-de-
females permanently sterile (Pech et al., 1995; pendent deaths (d(N)I/N), disease-induced mor-
Bradley et al., 1997). The success of this approach tality hI and culling, pI. The per capita death rate,
will also depend upon the mating system (Barlow d(N), was density-dependent and depended upon
et al., 1997), although this is not considered here. the total population size, N. Thus, the density-de-
A model was developed to investigate the ef- pendent death rate of healthy animals is a fraction
fects of each of these control methods on two X/N of the population rate d(N).
zoonotic infections. Rabies and TB are chosen as If there is no incubation period, and infectious
examples of wildlife diseases because of the simi- animals can reproduce, then Eq. (1) and Eq. (3)
larities of their host species, and the differences of become:
the disease epidemiology. Rabies is acute and
fatal (Anderson et al., 1981), while TB is chronic dX X
=b(X+ I)d(N) iIX pX, (4)
and disease-induced mortality is limited (Smith et dt N
al., 1995; Swinton et al., 1997; Wilkinson et al., and
2000). These diseases were chosen to represent
different ends of a spectrum, and should not be dI I
= iIX d(N) hI pI. (5)
interpreted as pertaining only to rabies or TB. dt N

2.2. Vaccination
2. Model
For vaccination Eq. (1) becomes:
2.1. Culling
dX X
= b(X+ Y+ V) d(N) iIX 6X (6)
A set of differential equations was developed to dt N
investigate the effects of disease control by and Eq. (4) becomes,
culling. The population was represented by three
equations if there was an incubation period and dX X
= b(X+ I+ V) d(N) iIX 6X, (7)
infectious animals cannot reproduce: dt N
G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553 47

since the rate of culling, p, will be 0.00. The other finite population size such that I had the
equations remain the same, but vaccinated ani- boundary conditions I{0.5, N}, which forces
mals, V, are described by: disease extinction when at very low levels. The
results were not qualitatively different with con-
dV V
=6X d(N) , (8) tinuous control, but with discrete control the re-
dt N
sults were easier to interpret.
where 6 is the per capita rate of vaccination with
life-long immunity. We assume that vaccination
prevents infection and thus has no affect on incu- 3. Parameterisation and results
bating (infected) animals.
3.1. Rabies
2.3. Fertility control
Rabies is a fatal disease where the incubation
If the vaccine bait includes an immunocontra- period in the fox, approximately 1 month (Steck
ceptive, then we assume that all vaccinated indi- and Wandeler, 1980; Garnerin et al., 1986), is
viduals are incapable of breeding and the term V much longer than the infectious period. As a
is removed from Eqs. (6) and (7), the other equa- result, we used Eqs. (1)(3) for lethal control,
tions remaining unchanged. Eqs. (6), (2), (3) and (8) for vaccination and
If the vaccine bait includes an abortifacient, immunocontraception (with V removed from Eq.
then healthy animals become immune, V, and fail (6)), and Eqs. (6), (2), (3), (9) and (10) for vacci-
to breed for one season. Since we assume a con- nation with an abortifacient. The parameters were
tinuous birth process, all vaccinated individuals derived from data for urban foxes in Britain
either die or are transferred to class U where they wherever possible. The death rate was set to equal
are immune but capable of breeding. Therefore, the birth rate (d(N)=b) when N =1000, and the
all the above equations remain unchanged except finite annual survival rate was set to 68.5% when
for Eq. (8) which becomes: the population was at a minimum (Harris and
Smith, 1987). The contact rate, i, was initially
dV V
=6x+ 6U mV d(N) , (9) estimated from contact rate data (White et al.,
dt N
1995). These authors estimated that 0.8475 con-
which permits all breeding animals to be vacci- tacts were made with neighbouring foxes during
nated and all recently vaccinated animals to either the infectious phase of the disease, and a mini-
die or reach class U, at rate m, where they may mum of one contact within the same social group.
breed: If we assumed there were five neighbouring
dU U groups of two adult foxes each, in a total popula-
=mV d(N) 6U. (10) tion size of 1000 animals, then the per capita
dt N contact rate approximates:
Vaccinated and breeding animals in class U
1 0.847510
return to class V if they consume further bait + = 0.0095. (11)
1000 1000
(6U), and the rate, m, is assumed to be 1.0 for
simplicity. At this contact rate, an epidemic developed
To simulate the repeated application of baits as which burns itself out, leaving the fox population
seen in the field, population control was assumed just able to recover, which agrees with previous
to be performed by intermittent events occurring simulation models (Smith and Harris, 1991). To
continuously during alternate (odd) time intervals, mimic an endemic situation, it was necessary to
for n occasions. During the intervening (even) reduce i to 0.0025 where damped oscillations of
time intervals all control rates (p and 6) are set to the disease occurred with a mean periodicity of 39
0.0. These equations have therefore been solved months; within the limits of cycles of rabies inci-
numerically rather than analytically, and have a dence seen in Europe (Zimen, 1980). A sensitivity
48 G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553

analysis of the model is given in the Appendix A. Table 2

Parameters used in the models to define endemic bovine
By using the parameters in Table 1 (given as tuberculosis in a badger population, using an annual timescale
instantaneous rates) we estimated the effectiveness
of lethal control. This suggested that a single Symbol Parameter Source
application rate of 0.6, or numerous applications
b Average per 0.29 per year (Rogers et al.,
of 0.2, eradicated the disease in an isolated popu-
capita birth rate 1997)
lation (Fig. 1). Only with repeated applications at d Average per 0.200.33 per year;
a high rate will the population become extinct. capita death rate density-dependent
With a vaccination strategy the results were i Transmission rate 0.00132 (see text)
h Disease induced 0.05 per year (Smith, 1995)
similar, but on average required an application
mortality rate
rate 0.1 higher to achieve disease eradication and
there was no possibility of population extinction The value of i was chosen to maintain endemic tuberculosis in
the population.
Table 1
Parameters used in the models to define endemic rabies in a
fox population, using a monthly timescale due to control. The inclusion of an abortifacient
gave an intermediate chance of successful disease
Symbol Parameter Source control with no possibility of population extinc-
tion. The inclusion of an immunocontraceptive
b Average per capita 0.11 per month (Harris
birth rate and Smith, 1987)
further improved the chances of disease control to
d Average per capita 0.0310.130 per month; be almost identical to that of lethal control, but
death rate density-dependent population extinction again became possible.
i Transmission rate 0.0025 (see text)
| 1/| is the average 0.9 per month
3.2. Tuberculosis
incubation period
h Disease induced 10.0 per month
mortality rate Badgers with TB show intermittent bacterial
excretion (Clifton-Hadley et al., 1993), sometimes
The level of | permits some individuals to incubate the disease for tens of months (Cheeseman et al., 1988;
for more than 1 month and the level of h to ensure infectious
Clifton-Hadley et al., 1993). Although some mod-
individuals survive only a few days. The level of i was chosen
to give oscillations in the incidence of rabies as seen in the els of TB in the badger utilised an incubating
wild. stage (Anderson and Trewhella, 1985; Bentil and
Murray, 1993; Smith et al., 1995) some analyses
have shown that stage hard to find, and it is
possible to successfully model TB without it
(Swinton et al., 1997). To maintain simplicity we
ignored any latent phase. Eqs. (4) and (5) were
used for control by culling, Eqs. (6), (5) and (8)
for vaccination or vaccine with an immunocontra-
ceptive (with V removed from Eq. (6)), and Eqs.
(6), (5), (9) and (10) for vaccine with an abortifa-
cient. The parameters were derived from a single
long-term study of a high density population in
the south-west of England (Table 2). This popula-
tion had a finite annual birth rate of 0.29 and a
Fig. 1. The effect of the number of applications and the level death rate of 0.20 for adults (Rogers et al., 1997).
of culling on the prevalence of rabies in a fox population. The
results show no effect (area 1), eradication of rabies within the
Mortality was density-dependent with minimum
population (area 2) and the extinction of the fox population finite annual rate of 0.20, 0.29 at carrying capacity
(area 3). and 0.33 when above carrying capacity. Some
G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553 49

studies have suggested that disease-induced mor- this prevalence (0.00132). Sensitivity of the model
tality was high (Anderson and Trewhella, 1985; to these parameters is given in the Appendix A.
White and Harris, 1995a), but field data did not A single application of lethal control reduced
support this (Wilkinson et al., 2000), so we as- the prevalence of TB for short periods, but we are
sumed that h = 0.05. The prevalence of TB within concerned here with the comparative effect of
this population has been independently calculated different control strategies. Thus, only three long-
between 0.10 and 0.18 (Smith et al., 1995; Swin- term responses to control were possible: no effect,
ton et al., 1997). We thus chose a level of 0.14, disease eradication, or population extinction. The
and derived a value of i which maintained TB at category of no effect therefore includes all simu-
lations where TB remained extant. The effect of
increasing the number of applications of lethal
control, against increasing rate of each control
episode is given in Fig. 2a. These results were
similar to the control of rabies, but the risk of
population extinction was slightly greater due to
the reduced fecundity of badgers. Unlike the pre-
vious scenario, the application of vaccination
showed a much reduced chance of disease control
but without the possibility of population extinc-
tion (Fig. 2b). Infectious animals persisted in the
population for a number of years, and it was this
persistence which made vaccination less effective
than culling. The inclusion of an abortifacient led
to only a small improvement over pure vaccine
bait, with no possibility of population extinction
even with high application rates. If the bait con-
tained an immunocontraceptive (Fig. 2c), the
probability of disease eradication became very
close to the original culling strategy, but with a
reduced possibility of population extinction.

4. Discussion

A set of differential equations was produced to

examine the control of an acute fatal disease
(rabies in foxes) and a more chronic, less fatal,
disease (TB in badgers). The equations separated
natality from mortality, which was density-depen-
dent. The effect of density-dependent mortality,
natality or both, has been examined elsewhere for
these diseases (Barlow 1996). These models ig-
nored spatial aspects of the biology of the hosts,
Fig. 2. The effect of the number of applications and the level but such non-spatial models have been usefully
of: (a) culling; (b) vaccination; and (c) vaccination with perma- applied previously (Anderson et al., 1981; Ander-
nent sterility, on the prevalence of bovine tuberculosis in a
badger population. The results show no effect (area 1), eradi-
son and Trewhella, 1985; Murray et al., 1986;
cation of TB within the population (area 2) and the extinction Murray and Seward, 1992; Bentil and Murray,
of the badger population (area 3). 1993; Ruxton, 1996; Selhorst and Muller 1999).
50 G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553

Most previous models were developed to study For bovine tuberculosis the consequences of
the disease dynamics and possible control through control were more variable. This simple model
culling. Vaccination has also been modelled for shows that vaccination will not have a marked
the fox (Anderson et al., 1981; Murray and Se- effect in the short term, and that many repeated
ward, 1992). Sterilisation, vaccination and culling applications will be required to control the dis-
have been considered for both species (Barlow, ease, which agrees with more complicated models
1996; White et al., 1997; Suppo et al., 2000) but (White and Harris, 1995b; Smith et al., 2001). All
the combination of vaccination with fertility con- forms of lethal control may increase contact rates
trol has received little attention (Suppo et al., through social perturbation which can, in extreme
2000), and the division of fertility control into cases, more than counterbalance the predicted
temporary and permanent techniques has not reduction in prevalence (Swinton et al., 1997).
been considered in detail. However, vaccination will not increase the contact
We are to some extent less concerned with the rate between individuals, as it is not socially dis-
exact parameterisation for these two diseases, ruptive. Given that not all female badgers breed
since they are being used as typical zoonotic successfully each year, it is possible that some
examples. One aspect that deserves greater re- forms of contraception may have social conse-
search is the possible consequences of social per- quences such that any sows that remain fertile
turbation following lethal control, or sterilisation. become dominant and breed successfully. Between
These models have ignored any effects of such 58 and 90% of females in the study site did not
breed each year (Rogers et al., 1997), so there
perturbation, which may act to increase the total
would be no effect if these females were sterilised.
number of infected animals, even though culling
An abortifacient, if ethically acceptable, could
reduces the total population size (Swinton et al.,
well act too late in the breeding season to effect
1997). Since perturbation is a spatial response, we
the dominance of affected females and the breed-
would encourage this aspect to be modelling in
ing failure of unaffected females.
spatially explicit models.
Each of the methods of control simulated here
For rabies, the four methods of control resulted
had a roughly equivalent effect where an acute
in similar probabilities of disease eradication,
fatal disease, such as rabies, was concerned, al-
given an endemic scenario. This may appear to be though our consideration was limited to endemic
at odds with the findings in Europe where culling rabies. Previous models (Smith and Harris, 1991;
as a means of rabies control had only limited Smith, 1995) have suggested that at high fox
success (Smith and Harris, 1989; Aubert, 1994), densities, differences can be seen between these
however the synchronisation and inter-country methods of control when applied to the source of
co-operation of the vaccination campaigns must an outbreak. In such scenarios simulation models
have had a marked effect on the consistency and are more appropriate, since the primary concern
efficacy of control, although the effects of social is a spatial one: to stop the spread of the out-
perturbation following lethal control cannot be break. Further work with spatial models is neces-
discounted. The risk of re-infection, particularly sary to support the relative effectiveness of each
from the unvaccinated areas of eastern Europe, is of the control options presented here. The general
now increased due to the increased fox density implication is that for acute, fatal, wildlife dis-
following the eradication of rabies. In these situa- eases; lethal control, vaccination and vaccine
tions, control with a vaccine and contraceptive combined with contraception may all have a
bait could not only eradicate rabies from the local roughly equivalent probability of successful dis-
population, but could help maintain that popula- ease eradication. For a chronic wildlife disease,
tion at a reduced level to inhibit re-infection. This for example bovine tuberculosis, lethal control
would most usefully be used as a cordon sanitaire appears more effective than vaccination, which
at the boundary of a rabies free area and needs to agrees with previous work (White and Harris,
be evaluated more fully. 1995b; Barlow, 1996), although the inclusion of a
G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553 51

contraceptive in the vaccine bait can redress the previously been shown that the inclusion of sea-
situation. However, for diseases such as tubercu- sonality and stochasticity do not necessarily im-
losis it may be a more effective strategy to reduce prove model predictions of this type, and that
the excretion of the infective organism and thus spatially explicit models are required to permit
the effective contact rate. further considerations on the specifics of control
These results not only have implications for the options (Ruxton, 1996). Spatially explicit models
widespread diseases considered here, but perhaps exist for rabies (David et al., 1982; Voigt et al.,
more importantly, for diseases in isolated popula- 1985; Smith, 1995) and bovine tuberculosis (Smith
tions or threatened species, where the possibility et al., 1995; White and Harris, 1995a,b), but a
of population extinction, either through the dis- single spatial model cannot easily consider both
ease itself, or as a result of attempting to control diseases in different species. We recommend that
the disease, must be avoided. any management decision on disease control
The objective of each control policy is to reduce should be based on a more specific model of the
the population of susceptible individuals to below disease and vector in question (e.g. Smith, 1995;
some critical threshold density (Anderson et al., Selhorst, 2000 for rabies).
1981). Since vaccinated animals can reproduce,
the total number of new susceptible individuals
will be greater in a vaccinated population than in Acknowledgements
a culled population. Thus, it appears that vaccina-
tion becomes less effective than lethal control for The authors thank J. Swinton, J. Nokes, D.G.
chronic diseases, since infected animals can sur- Newall, D. Wilkinson and M. Aubert for helpful
vive and reproduce for a long time. We have comments on an earlier draft.
demonstrated here that this difference is due to
births, since if vaccinated animals cannot breed
the effectiveness of lethal control and vaccination Appendix A
appear similar. Further, if culling is more effective
than vaccination, then given the same efficacy of A.1. Rabies
control, there must be host densities where vacci-
nation will fail, while culling will lead to disease The sensitivity of the models to variation in the
eradication. input variables can be determined explicitly. Each
of the models may perform differently with re-
spect to each parameter. However, changes to the
5. Conclusion birth or death rates will have little effect due to
density-dependence. For the disease transmission
For the two diseases studied here, vaccination rate, i, this can be demonstrated by examining
was always less successful than culling, but this the effect of increasing i for a particular control
was only significant for the chronic disease (tuber- strategy. In the absence of control, changes to the
culosis). The inclusions of fertility control re- transmission rate qualitatively change the out-
dressed the situation for both diseases such that come of disease. Below i= 0.0014 the disease dies
vaccine and fertility control was equivalent to, but out due to boundary conditions (i.e. there would
not better than culling. be less than one infected individual); up to i=
Again we stress the simplicity of the approach 0.0015 the disease prevalence reaches a steady
used here for considering these diseases. The in- state; between i= 0.0016 and 0.0029 disease cy-
clusion of density-dependent demographic cles occur with duration and amplitude increasing
parameters may have an effect on the optimum as i increases. Above this level a short epidemic
control policy (Barlow, 1996), but the lack of occurs resulting in a population crash and subse-
demonstrated density-dependence in disease con- quent disease extinction due to boundary condi-
tact rates remains a problem (Smith, 2001). It has tions. The sensitivity of the different disease
52 G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553

control models can be identified by taking a par- References

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