Ecological Modelling 150 (2002) 45 53

www.elsevier.com/locate/ecolmodel

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

Abstract

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

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

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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
since the rate of culling, p, will be 0.00. The other
equations remain the same, but vaccinated ani-
mals, V, are described by:
dV V
=6X d(N) , (8)
dt N
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-
bating (infected) animals.
2.3. Fertility control
If the vaccine bait includes an immunocontra-
ceptive, then we assume that all vaccinated indi-
viduals are incapable of breeding and the term V
is removed from Eqs. (6) and (7), the other equa-
tions remaining unchanged.
If the vaccine bait includes an abortifacient,
then healthy animals become immune, V, and fail
to breed for one season. Since we assume a con-
tinuous birth process, all vaccinated individuals
either die or are transferred to class U where they
are immune but capable of breeding. Therefore,
all the above equations remain unchanged except
for Eq. (8) which becomes:
dV V
=6x+ 6U mV d(N) , (9)
dt N
which permits all breeding animals to be vacci-
nated and all recently vaccinated animals to either
die or reach class U, at rate m, where they may
breed:
dU U groups of two adult foxes each, in a total popula-
=mV d(N) 6U. (10)
dt N contact rate approximates:
Vaccinated and breeding animals in class U
return to class V if they consume further bait
(6U), and the rate, m, is assumed to be 1.0 for
simplicity.
To simulate the repeated application of baits as
seen in the field, population control was assumed
to be performed by intermittent events occurring
continuously during alternate (odd) time intervals,
for n occasions. During the intervening (even)
time intervals all control rates (p and 6) are set to
0.0. These equations have therefore been solved
numerically rather than analytically, and have a
47
finite population size such that I had the
boundary conditions I{0.5, N}, which forces
disease extinction when at very low levels. The
results were not qualitatively different with con-
tinuous control, but with discrete control the re-
sults were easier to interpret.
3. Parameterisation and results
3.1. Rabies
Rabies is a fatal disease where the incubation
period in the fox, approximately 1 month (Steck
and Wandeler, 1980; Garnerin et al., 1986), is
much longer than the infectious period. As a
result, we used Eqs. (1)(3) for lethal control,
Eqs. (6), (2), (3) and (8) for vaccination and
immunocontraception (with V removed from Eq.
(6)), and Eqs. (6), (2), (3), (9) and (10) for vacci-
nation with an abortifacient. The parameters were
derived from data for urban foxes in Britain
wherever possible. The death rate was set to equal
the birth rate (d(N)=b) when N =1000, and the
finite annual survival rate was set to 68.5% when
the population was at a minimum (Harris and
Smith, 1987). The contact rate, i, was initially
estimated from contact rate data (White et al.,
1995). These authors estimated that 0.8475 con-
tacts were made with neighbouring foxes during
the infectious phase of the disease, and a mini-
mum of one contact within the same social group.
If we assumed there were five neighbouring
tion size of 1000 animals, then the per capita
1 0.847510
+ = 0.0095. (11)
1000 1000
At this contact rate, an epidemic developed
which burns itself out, leaving the fox population
just able to recover, which agrees with previous
simulation models (Smith and Harris, 1991). To
mimic an endemic situation, it was necessary to
reduce i to 0.0025 where damped oscillations of
the disease occurred with a mean periodicity of 39
months; within the limits of cycles of rabies inci-
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
studies have suggested that disease-induced mor-
tality was high (Anderson and Trewhella, 1985;
White and Harris, 1995a), but field data did not
support this (Wilkinson et al., 2000), so we as-
sumed that h = 0.05. The prevalence of TB within
this population has been independently calculated
between 0.10 and 0.18 (Smith et al., 1995; Swin-
ton et al., 1997). We thus chose a level of 0.14,
and derived a value of i which maintained TB at
Fig. 2. The effect of the number of applications and the level
of: (a) culling; (b) vaccination; and (c) vaccination with perma-
nent sterility, on the prevalence of bovine tuberculosis in a
badger population. The results show no effect (area 1), eradi-
cation of TB within the population (area 2) and the extinction
of the badger population (area 3).
49
this prevalence (0.00132). Sensitivity of the model
to these parameters is given in the Appendix A.
A single application of lethal control reduced
the prevalence of TB for short periods, but we are
concerned here with the comparative effect of
different control strategies. Thus, only three long-
term responses to control were possible: no effect,
disease eradication, or population extinction. The
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,
but such non-spatial models have been usefully
applied previously (Anderson et al., 1981; Ander-
son and Trewhella, 1985; Murray et al., 1986;
Murray and Seward, 1992; Bentil and Murray,
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
the disease dynamics and possible control through
culling. Vaccination has also been modelled for
the fox (Anderson et al., 1981; Murray and Se-
ward, 1992). Sterilisation, vaccination and culling
have been considered for both species (Barlow,
1996; White et al., 1997; Suppo et al., 2000) but
the combination of vaccination with fertility con-
trol has received little attention (Suppo et al.,
2000), and the division of fertility control into
temporary and permanent techniques has not
been considered in detail.
We are to some extent less concerned with the
exact parameterisation for these two diseases,
since they are being used as typical zoonotic
examples. One aspect that deserves greater re-
search is the possible consequences of social per-
turbation following lethal control, or sterilisation.
These models have ignored any effects of such
perturbation, which may act to increase the total
number of infected animals, even though culling
reduces the total population size (Swinton et al.,
1997). Since perturbation is a spatial response, we
would encourage this aspect to be modelling in
spatially explicit models.
For rabies, the four methods of control resulted
in similar probabilities of disease eradication,
given an endemic scenario. This may appear to be
at odds with the findings in Europe where culling
as a means of rabies control had only limited
success (Smith and Harris, 1989; Aubert, 1994),
however the synchronisation and inter-country
co-operation of the vaccination campaigns must
have had a marked effect on the consistency and
efficacy of control, although the effects of social
perturbation following lethal control cannot be
discounted. The risk of re-infection, particularly
from the unvaccinated areas of eastern Europe, is
now increased due to the increased fox density
following the eradication of rabies. In these situa-
tions, control with a vaccine and contraceptive
bait could not only eradicate rabies from the local
population, but could help maintain that popula-
tion at a reduced level to inhibit re-infection. This
would most usefully be used as a cordon sanitaire
at the boundary of a rabies free area and needs to
be evaluated more fully.
For bovine tuberculosis the consequences of
control were more variable. This simple model
shows that vaccination will not have a marked
effect in the short term, and that many repeated
applications will be required to control the dis-
ease, which agrees with more complicated models
(White and Harris, 1995b; Smith et al., 2001). All
forms of lethal control may increase contact rates
through social perturbation which can, in extreme
cases, more than counterbalance the predicted
reduction in prevalence (Swinton et al., 1997).
However, vaccination will not increase the contact
rate between individuals, as it is not socially dis-
ruptive. Given that not all female badgers breed
successfully each year, it is possible that some
forms of contraception may have social conse-
quences such that any sows that remain fertile
become dominant and breed successfully. Between
58 and 90% of females in the study site did not
breed each year (Rogers et al., 1997), so there
would be no effect if these females were sterilised.
An abortifacient, if ethically acceptable, could
well act too late in the breeding season to effect
the dominance of affected females and the breed-
ing failure of unaffected females.
Each of the methods of control simulated here
had a roughly equivalent effect where an acute
fatal disease, such as rabies, was concerned, al-
though our consideration was limited to endemic
rabies. Previous models (Smith and Harris, 1991;
Smith, 1995) have suggested that at high fox
densities, differences can be seen between these
methods of control when applied to the source of
an outbreak. In such scenarios simulation models
are more appropriate, since the primary concern
is a spatial one: to stop the spread of the out-
break. Further work with spatial models is neces-
sary to support the relative effectiveness of each
of the control options presented here. The general
implication is that for acute, fatal, wildlife dis-
eases; lethal control, vaccination and vaccine
combined with contraception may all have a
roughly equivalent probability of successful dis-
ease eradication. For a chronic wildlife disease,
for example bovine tuberculosis, lethal control
appears more effective than vaccination, which
agrees with previous work (White and Harris,
1995b; Barlow, 1996), although the inclusion of a
 G.C. Smith, C.L. Cheeseman / Ecological Modelling 150 (2002) 4553
contraceptive in the vaccine bait can redress the
situation. However, for diseases such as tubercu-
losis it may be a more effective strategy to reduce
the excretion of the infective organism and thus
the effective contact rate.
These results not only have implications for the
widespread diseases considered here, but perhaps
more importantly, for diseases in isolated popula-
tions or threatened species, where the possibility
of population extinction, either through the dis-
ease itself, or as a result of attempting to control
the disease, must be avoided.
The objective of each control policy is to reduce
the population of susceptible individuals to below
some critical threshold density (Anderson et al.,
1981). Since vaccinated animals can reproduce,
the total number of new susceptible individuals
will be greater in a vaccinated population than in
a culled population. Thus, it appears that vaccina-
tion becomes less effective than lethal control for
chronic diseases, since infected animals can sur-
vive and reproduce for a long time. We have
demonstrated here that this difference is due to
births, since if vaccinated animals cannot breed
the effectiveness of lethal control and vaccination
appear similar. Further, if culling is more effective
than vaccination, then given the same efficacy of
control, there must be host densities where vacci-
nation will fail, while culling will lead to disease
eradication.
5. Conclusion
For the two diseases studied here, vaccination
was always less successful than culling, but this
was only significant for the chronic disease (tuber-
culosis). The inclusions of fertility control re-
dressed the situation for both diseases such that
vaccine and fertility control was equivalent to, but
not better than culling.
Again we stress the simplicity of the approach
used here for considering these diseases. The in-
clusion of density-dependent demographic
parameters may have an effect on the optimum
control policy (Barlow, 1996), but the lack of
demonstrated density-dependence in disease con-
tact rates remains a problem (Smith, 2001). It has
51
previously been shown that the inclusion of sea-
sonality and stochasticity do not necessarily im-
prove model predictions of this type, and that
spatially explicit models are required to permit
further considerations on the specifics of control
options (Ruxton, 1996). Spatially explicit models
exist for rabies (David et al., 1982; Voigt et al.,
1985; Smith, 1995) and bovine tuberculosis (Smith
et al., 1995; White and Harris, 1995a,b), but a
single spatial model cannot easily consider both
diseases in different species. We recommend that
any management decision on disease control
should be based on a more specific model of the
disease and vector in question (e.g. Smith, 1995;
Selhorst, 2000 for rabies).
Acknowledgements
The authors thank J. Swinton, J. Nokes, D.G.
Newall, D. Wilkinson and M. Aubert for helpful
comments on an earlier draft.
Appendix A
A.1. Rabies
The sensitivity of the models to variation in the
input variables can be determined explicitly. Each
of the models may perform differently with re-
spect to each parameter. However, changes to the
birth or death rates will have little effect due to
density-dependence. For the disease transmission
rate, i, this can be demonstrated by examining
the effect of increasing i for a particular control
strategy. In the absence of control, changes to the
transmission rate qualitatively change the out-
come of disease. Below i= 0.0014 the disease dies
out due to boundary conditions (i.e. there would
be less than one infected individual); up to i=
0.0015 the disease prevalence reaches a steady
state; between i= 0.0016 and 0.0029 disease cy-
cles occur with duration and amplitude increasing
as i increases. Above this level a short epidemic
occurs resulting in a population crash and subse-
quent disease extinction due to boundary condi-
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-
ticular control frequency and determining the in-
teraction between the transmission rate, the
application frequency and the outcome. For vac-
cination with a permanent immunocontraceptive,
the transmission parameter, i, may be increased
markedly without failure to control the disease:
high levels of i led to population extinction. For
culling, a similar result occurs with population
extinction occurring at slightly lower levels of i.
For the remaining strategies the value of i at
which a particular application level fails can be
plotted and the slope of the curve, m calculated.
In effect this measures increase in the transmis-
sion rate, which is required for disease control to
fail as the culling or application rate, is increased.
Control strategies, which are more tolerant to
changes in the transmission rate, will have a
higher slope. The model sensitivities to i are as
follows:
Vaccine+ abortifacient m =0.0158
Vaccine only m =0.00818
These models are therefore more sensitive to vari-
ation in the transmission rate, particularly the
vaccine only policy.
A.2. Tuberculosis
In the absence of control, changes to the trans-
mission rate result in different asymptotic levels of
prevalence, but do not change the qualitative
outcome. At low levels (i=0.0011) the disease
fails to establish due to boundary conditions,
while at high levels (i =0.054) the prevalence
reaches 1.0.The model sensitivities to i are as
follows:
Culling only m =0.267
Vaccine +immunosterilant m = 0.00152
Vaccine+abortifacient m = 0.000546
Vaccine only m =0.000212
Thus, culling is very insensitive to the exact level
of the transmission rate when compared to the
other techniques.
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