Dog population characteristics and rabies
vaccination coverage at the wildlife interface
in the Mpumalanga Province of South Africa.
Thesis
J.A.C. Geerdes
April 2014
Faculty of Veterinary Science
Acknowledgements
I would like to express my appreciation to all the householders in Athol, Dixie, and Utah. Many thanks
to the Environmental Monitors (especially Godfrey Tsela) whom accompanied me to the study sites
and assisted with interviews and translations. This study received support from the Faculty of
Veterinary Science of the University of Pretoria (UP) and the Hluvukani Animal Health Centre. I would
finally like to thank Prof. Dr. F. Jongejan for his supervision from The Netherlands, Prof. D.L. Knobel at
UP for his comments on earlier drafts of this manuscript and Dr A. Conan for her practical support in
the field and her contribution to data analysis.
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | i
Abstract
Rabies is a zoonotic, rapidly progressive, fatal virus which targets the central nervous system and is
mainly transmitted by bites and scratches from domestic dogs (Canis lupus familiaris) acting as the
main reservoir of disease. Not only dogs and humans play a role in the dynamics of rabies, it is also
known as a disease that is of conservation interest. Wild carnivore populations have been affected by
rabies virus over the past 20 years. The design and success of long-term rabies control programs
aimed at domestic dogs in developing countries may be affected by many factors such as high density
populations and high turnover rates.
The objective of this study was to collect data through a household-level census in three rural
communities in the sub-district of Bushbuckridge, Mpumalanga Province of South Africa, bordering a
large privately-owned conservation area. With this data we aim to assess rabies-vaccination coverage
and other factors that might influence the success of the on-going vaccination campaign in the study
areas. A descriptive analysis of household characteristics, dog demographics, and contraception
demand was performed.
A total of 1086 households were interviewed representing a total of 5115 persons and 413
dogs. Dog densities were found to be 169 dogs/km2, 128 dogs/km2, and 133 dogs/km2. We found
that the dog:human ratio is 1:11 and 1:15 in the three studied communities. Of all the households
included in this study 227 (21%) were DOHH and 863 (79%) of them NOHH.
More than 60% of the dogs were found to be free roaming in all three communities. The dog
populations were comprised principally of adults (>1 year of age) which made up 52 - 69% of the dog
populations in the three communities. The sex ratio of the dog population in all three communities is
skewed towards males. The average number of litters in the past twelve months ranged from 1,0-1,3
litter(s), the mean size of the litter was 5,0-5,2 pups and the mortality in the first week after birth 045,9%. Neutered dogs (<12%) are not a common finding in any of the three communities. Owners
were willing to pay an average of $8 for the 2-year contraception injection.
The vaccination coverage range in each of the three communities was 48.6%-57.3%, 68.7%77.4% and 53.3%-77.8%. We did not detect any significance between confinement characteristics and
the vaccination status of dogs in the three communities. Our results show that over 85% of dogs in all
three communities were vaccinated during a vaccination campaign where house-to-house visits were
carried out.
Veterinarians, medical practitioners, and health authorities have the responsibility to apply
intersectoral collaboration under the motto of ‘One Health’. We need to strive for a high level of risk
perception among dog owners and an increased belief in the benefits of vaccination through public
education activities. Proactive and sustainable vaccination programs in the Western World have
proven their efficacy in the eradication of domestic dog rabies; this should provide a motivation and a
model for South Africa in the fight against rabies.
Dog population characteristics and rabies vaccination coverage
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Content
Acknowledgements ...................................................................................................................................................................... i
Abstract ............................................................................................................................................................................................ ii
Content ............................................................................................................................................................................................ iii
1
Introduction .......................................................................................................................................................................... 1
2
Materials & Methods ........................................................................................................................................................ 6
3
2.1
Study area ................................................................................................................................................................... 6
2.2
Study populations .................................................................................................................................................... 6
2.3
Questionnaire ............................................................................................................................................................ 7
2.4
Demographic parameters ..................................................................................................................................... 7
2.5
Photo database ......................................................................................................................................................... 8
Statistical analysis ............................................................................................................................................................... 9
3.1
Household characteristics ..................................................................................................................................... 9
Human population dynamics ........................................................................................................................................ 9
Dog ownership patterns .................................................................................................................................................. 9
3.2
Dog demographics .................................................................................................................................................. 9
Dog population dynamics .............................................................................................................................................. 9
Sex and age distribution.................................................................................................................................................. 9
Female reproduction ......................................................................................................................................................... 9
4
3.3
Contraception demand .......................................................................................................................................... 9
3.4
Vaccination coverage ............................................................................................................................................. 9
3.5
Significance of sex and confinement on vaccination status .................................................................10
3.6
Ethical clearance .....................................................................................................................................................10
Results...................................................................................................................................................................................11
4.1
Household characteristics ...................................................................................................................................11
Human population dynamics ......................................................................................................................................11
Dog ownership patterns ................................................................................................................................................11
4.2
Dog demographics ................................................................................................................................................12
Dog population dynamics ............................................................................................................................................12
Sex and age distribution................................................................................................................................................12
Female reproduction .......................................................................................................................................................13
4.3
Contraception demand ........................................................................................................................................14
4.4
Vaccination coverage ...........................................................................................................................................15
General information regarding vaccination coverage .......................................................................................15
Dog population characteristics and rabies vaccination coverage
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Overall vaccination coverage sampled population ............................................................................................15
Significance of sex and confinement on vaccination status ...........................................................................18
5
Discussion............................................................................................................................................................................20
6
Conclusion...........................................................................................................................................................................25
7
References ...........................................................................................................................................................................26
Dog population characteristics and rabies vaccination coverage
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1 Introduction
South Africa had its first known rabies outbreak in domestic dogs (Canis lupus familiaris) confirmed in
1893. Outbreaks were sporadic, and rabies appeared not to be able to establish itself [1]. National
records of South Africa show that Limpopo Province had its first invasive form of dog rabies confirmed
in 1950. From there the disease spread to Zimbabwe, through Mozambique in 1952 to KwaZulu-Natal
where the first dog rabies case was diagnosed in 1961, and despite control measures it reappeared in
1976. From that moment on rabies moved to the southern part (Nkomazi District) of Mpumalanga
Province where the disease then spread primarily in domestic dogs in densely populated rural areas
and became endemic in many of these areas [2, 3].
Rabies is caused by members of the Lyssavirus genus in the Rhabdoviridae family that targets
the central nervous system. The disease is a zoonotic, acute, rapidly progressive, fatal viral encephalitis
transmitted through contact (mainly bites and scratches) with an infectious host animal, both
domestic and wild [4, 5]. Human rabies is a major public health concern and is considered a neglected
disease worldwide by the World Health Organization [6, 7]. It is an endemic disease throughout most
African and Asian countries, and domestic dogs are the main reservoir of the virus, able to ensure
persistence of the disease. Dogs are also primarily responsible, in 95% of cases, for the transmission of
the virus to humans. Once symptoms appear, human rabies is almost inevitably fatal [8, 9].
More than 99% of all human deaths from rabies occur in the developing world and it remains a
neglected disease throughout most of these countries. The WHO estimated the rabies burden in
Africa in 2010 to be 23 800 human deaths per year [6] which accounts for 44% of the total number of
deaths per year worldwide, particularly in rural areas [5, 10]. The worldwide administration of post
exposure prophylaxis (PEP) amounts to an estimated annual cost of US$ 583.5 million [5]. PEP consists
of wound washing, passive immunization with rabies immune globulin, and a series of rabies vaccine
doses [7]. Rabies in humans can be prevented with the appropriate PEP but unfortunately this is a
treatment of which victims are often unaware. PEP is not always available, and often needs to be
administered to patients who least can afford to pay [5]. Poor households may experience substantial
delays in receiving PEP due to difficulties acquiring funds. Another financial burden for these families
is the need for bite victims to travel to multiple hospitals or clinics to obtain treatment due to a
frequent shortage of PEP throughout most of Africa [11]. It could therefore be said that both human
health and public health finances could benefit substantially from a reduction in dog rabies incidence.
Although rabies is a notifiable disease in South Africa, the surveillance of rabies cases in dogs by
veterinary services and collection of data on dog bite injuries by local clinics and district hospitals
could be improved in some areas. In the sub-district of Bushbuckridge, Mpumalanga Province, there
were a total of 702 dog bite cases reported in 2012, with an average of 14 dog bites per week. In 2013
there were 784 reported cases of dog bites from January 2013 through September 2013, with an
average of 20 per week. The Mpumalanga Department of Health reports 17 confirmed human rabies
cases between 2006 and 2013 [12]. Laboratory records of animal-bite injuries compiled from
Mpumalanga Province show only eight fatal cases of rabies infection between 2001 and 2013 [13]. Six
of the latter cases were reported as dog-bite injuries, two others as unknown. Five of the victims were
under the age of 15 years. It is estimated that, on average, 30-50% of rabies deaths concern children
under 15 years of age [14]. Young children enjoy playing with dogs, are unable to discern abnormal
animal behavior and are often bitten on the head and arms where virus entry is in close proximity to
the central nervous system thus elevating the risk of contracting rabies [12, 15]. Modeling approaches,
using these incidences of dog-bite injuries and availability of PEP, indicate that official data on rabies
Dog population characteristics and rabies vaccination coverage
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deaths submitted to the WHO greatly under-estimate the incidence of disease in Africa by as much as
100-fold [15, 16]. The reasons for lower estimates are extensive and include: victims are considered to
be the victims of bewitchment, victims are too ill to travel to hospital or die before arrival, families
recognize the futility of medical treatment, or cases do not receive laboratory confirmation [11, 14,
17]. Hospital-diagnosed cases are rarely reported or clinical signs may be mistaken for other diseases
such as malaria or meningitis. More often rabies cases remain undetected because victims die at
home not aware what first-aid to administer, after receiving inappropriate PEP care or because the
biological necessities are not available [18]. This could suggest an increase in the number of rabies
deaths without the authorities being alerted.
Dogs play a significant role as reservoirs and vectors of disease, transferring disease to humans and
livestock because of their intimate contact with other animals and people. With many diseases the
reservoir needs to be targeted to eliminate infection and so is the case with rabies [11]. Vaccination of
dogs not only leads to a decline in dog rabies but also to a rapid reduction in the demand for PEP
[15]. Vaccination of dogs includes a single dose of an inactivated (killed) parenteral rabies vaccine with
3-year duration of immunity (DOI) [19]. In many parts of the world, such as Europe and central and
South America, large-scale mass dog vaccination on a continual basis have proven successful in
bringing canine rabies under control [11]. Dog-transmitted human rabies control programs in
resource-poor or under-served communities involve the promotion of annual or biannual canine mass
vaccination campaigns, usually without additional costs for the communities [7]. Studies in Tanzania
have shown that dog vaccination of 60%-70% of the population over annual vaccination campaigns
can reduce the incidence of dog rabies by over 90% [15, 20].
However, the design and success rate of long-term rabies control programs in developing
countries may be affected by many factors such as poverty, geographical and environmental
limitations, social, cultural, political and economic variables. First, prevention of epidemics or
elimination of a dog disease poses a challenge with a high density of susceptible hosts and a high
population turnover rate, which is often the case in rural settlements in Africa where turnover rates are
often high [21]. Rates of disease transmission depend on the density of the dog population and social
behavior that determines the extent of contact. Research in the Serengeti found that rabies appears to
persist endemically in higher-density domestic dog populations (>5/km2) and less in lower-density
populations [22, 23]. Data on rabies persistence in rural Kenya suggests 4,5 dogs/km2 as the density
threshold for rabies persistence [24]. The indicated rabies vaccination coverage of 70% [6, 25] by the
WHO, which would prevent coverage falling below the critical proportion of the population that must
be protected in order to eliminate infection, could also prove insufficient in these higher density
populations or in populations with a high turnover rate [15]. Yet, the vaccination coverage of a
population can only be identified with a precise assessment of the dog population size prior to
vaccination programs. Under-estimation of the size of dog populations could cause the achieved
vaccination coverage to be overestimated, when in reality it may be below the target of 70% [15, 26].
Secondly, different vaccine delivery strategies, for example house-to-house, oral vaccination or
centralized strategies, could also determine the (cost-) effectiveness of a vaccination campaign
because the attitude of owners towards the handling of dogs can affect the dogs’ accessibility to
vaccination campaigns. Furthermore, accessibility of owned dogs for vaccination is not always
guaranteed because owners of dogs often have misconceptions regarding dog vaccination where they
believe that dogs die or have reduced vigor after vaccination [26].
Dog population characteristics and rabies vaccination coverage
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Finally, dependent on demographic data of the target area, the critical vaccination coverage
threshold may not be reached with an annual campaign if the turnover is too rapid. In these areas, to
maintain population level coverage above the critical threshold until the next campaign one year later,
reasonable vaccination coverage of 70% may be inadequate and vaccinations may need to be
repeated within the same year to prevent or eliminate rabies [15]. Studies performed in Kenya, South
Africa and Zimbabwe support that if vaccination coverage in not maintained, rabies can re-establish
extremely rapidly [20, 27]. When the number of human cases has been reduced and dog vaccination
no longer seems necessary inadequate maintenance of vaccination coverage will likely lead to reemergence of the disease [28].
Not only dogs and humans play a role in the dynamics of rabies, it is also known as a disease that is of
conservation interest [29]. Wild carnivore populations have been affected by rabies virus over the past
20 years [30, 31]. Complex reservoir systems pose a challenge when trying to understand the
maintenance and transmission of infectious canine diseases and risks for wildlife. In communities
comprising multiple hosts it is important to identify maintenance populations and sources of infection
which transmit rabies to ‘spill-over’ hosts (e.g. humans, endangered wildlife and livestock). However,
the exact role of wildlife in rabies in the context of particular ecosystems and host communities needs
to be addressed [22]. Although a wide range of mammals can be infected by and transmit rabies virus,
only species within the orders Carnivora (e.g. dogs, raccoons, skunks, foxes, jackals, and mongooses)
and Chiroptera (bats; only in North and South America) have been identified as reservoirs for the
disease [7, 11, 15]. Studies have reported species of wild carnivore in southern Africa, such as the
yellow and slender mongooses, bat-eared fox and the side-striped and black-backed jackal [32] as
independent maintenance hosts of rabies [1, 22, 33]. A recent publication strongly supports the
maintenance, under certain circumstances, of an independent rabies virus cycle in Namibian kudu
(Tragelaphus strepsiceros), unusual in that kudus are herbivores [34].
Research done in the Serengeti found rabies outbreaks in domestic dogs coincided with
sporadic rabies cases in wildlife, although the estimated transmission between species was less than
expected [22]. Also, the number of cases detected in wildlife in the Serengeti was much lower than the
number of cases detected in domestic dogs in proximity to the park which could be evidence that
wildlife is not able to maintain rabies cycles and that rabies does not occur in the absence of dog
rabies [23]. Low transmission rates in wildlife populations could be caused by factors such as absence
of other hosts with which to interact, high diversity of species coexisting within the same area, failure
to induce biting behavior and inefficient salivary shedding [33, 35]. Furthermore, carnivore populations
are often low-density populations and rabies is therefore less likely to persist endemically [20]. Shortlived pathogenic infections are much more likely to be maintained in large neighboring populations
rather than small (endangered) populations in which contact between infected and susceptible
individuals is too low and infection will eventually fade out [22, 30].
Despite this, conservationists and veterinarians have their concerns about rabies in African wild
dog (Lycaon pictus) populations [36] which have been affected by rabies outbreaks in the late 1980s
and early 1990s in the Serengeti-Mara Ecosystem [11, 23, 30]. This period of pack losses suggests the
potential for disease to act as a local extinction threat. Recent study results by Hofmeyr et al. [37] in
South Africa demonstrate a protective benefit of rabies vaccination in South African wild dog
populations where vaccinated adults survived a rabies outbreak and unvaccinated pups did not [20,
30]. Recent trials in the Bale Mountains’ population of Ethiopian wolves during a rabies epidemic
Dog population characteristics and rabies vaccination coverage
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showed that reactive vaccination limited the scale of the outbreak and prevented a decline in the
endangered population [20, 30, 38].
Theoretically, wildlife vectors can act as sources of infection for domestic animals, which may
complicate eradication of the disease [3]. Studies performed on dog rabies in Thailand, Kenya and the
Serengeti all detected a variant of virus from a range of wildlife species closely related to a canidassociated virus isolate which indicates transmission between domestic dogs and wildlife, with dogs
being the likely reservoir [23, 35]. Genetic analysis of brain samples from endangered Ethiopian wolves
(Canis simensis) in the Bale Mountains in Ethiopia identified the virus to be of canid type with an
overall identity of 96,2% for the N gene sequences [38]. Phylogenetic similarity was also found with
rabies viruses from dogs and jackals in Zimbabwe and South Africa. It is tempting to assume that
closely-related virus isolates from wildlife and domestic dogs indicate rabies control measures
targeted at domestic dog populations alone will often be sufficient for eradication of the disease [1,
22, 30, 39]. However, under certain circumstances rabies seems to be able to jump to wildlife host
communities, such as jackals and kudu, in which it can establish stable infection cycles independently
of dogs because of host-adapted variants of the virus [34]. This phenomenon may indicate the need
for new control and/or eradication strategies.
Conservation management faces the challenge of determining a strategy to control (or
eliminate) a disease threatening wildlife while it is maintained in a domestic animal reservoir.
Therapeutic tools for wildlife are limited and control measures are difficult to apply, while vaccination
of domestic animal reservoirs is often practically more feasible. Oral rabies vaccines for wildlife have
been very successful for the control of rabies in wildlife reservoirs in parts of Europe and North
America but these have not been widely used for endangered wild canids in southern Africa and will
need further testing [20].
Mobile clinics around Hwange National Park, Zimbabwe, vaccinated 800 local domestic dogs
against rabies and distemper as part of a wider conservation initiative coordinated by Wildlife Vets
International to protect the wild dog population in the park [39]. Such conservation-related activities
will gain more support by integrating wildlife expertise into disease control strategies.
Conservationists in a large privately-owned conservation area in South Africa have expressed ‘their
support towards activities for a better understanding of rabies in the communities bordering their
fences’ [pers. comm.]. Free roaming dogs that behave rabidly and are more likely to transmit disease
are regularly found within the parks’ boundaries. Therefore these conservationists could be providing
future funding for similar disease control strategies in their surroundings, such as dog rabies
vaccination campaigns or humane population management projects.
One of the activities that conservationists could support is the development and implementation of
nonsurgical methods of sterilization to control the population size. Neutering contributes to the
attainment of stable, vaccinated populations of dogs, but it is impractical, time consuming, invasive,
and expensive [40]. A very promising alternative is the use of immunocontraceptive vaccines such as
Gonacon (USDA, APHIS, Wildlife Services National Wildlife Research Center (NWRC), Fort Collins, CO,
USA). The gonadotropin-releasing hormone (GnRH) peptide in the vaccine stimulates the production
of antibodies that bind to circulating GnRH, thus preventing the release of LH and FSH. For application
in roaming dogs during mass campaigns the immunocontraceptive will have to 1) be effective with
one dose or in booster doses; 2) inhibit fertility for at least 1 year; 3) have zero to limited side-effects;
4) be safe and effective if administered during pregnancy; 5) be less expensive than surgical
sterilization; 6) inhibit female reproduction (preferably male reproduction as well); and 7) be stable
Dog population characteristics and rabies vaccination coverage
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under a wide variety of field conditions [41]. A study in cats in Combodia showed GonaCon to induce
fertility for 1 year in 93% of the cats treated with a single dose. The following 2 years after injection
reproduction was suppressed in 73% of cats [42]. Infertility of 1 year in male dogs and 2-3 times
longer in females than males has been demonstrated by others [43]. Recent studies have confirmed
prevention of ovulation and inhibition of estrous behavior with the use of GnRH peptide as an
immunocontraceptive in females [41]. Immunocontraceptive effects have also been confirmed in
males of different animal species [44]. Proof of a negative effect on existing pregnancies has not been
found [40]. Side-effects and/or social behavior changes have not been observed in the immunized
animals [45]. A helpful advantage of this intervention could be that with female dogs lacking estrous
behavior and male dogs no longer being attracted to the females, the number of bite rates among
dogs might also.
Controlling the breeding capability, in other words reducing population turnover rates, of a dog
population will result in maintenance of herd immunity [43]. A vaccination program could become
cost-effective by combining the two vaccines and the cost of fertility inhibitors could be lower than
the cost of surgical sterilization. The use of GonaCon does not seem to interfere with parenteral rabies
immunization in breeding age female dogs [40, 43]. Willingness of dog owners to pay for a
contraceptive vaccine would most likely increase if administered in tandem with a rabies vaccination.
Knowledge of the dynamics in the local dog population is needed to design, manage and assess the
impact of a fertility-control program.
The question remains if it is achievable to eliminate domestic dog rabies globally. Perhaps strategies
used in Europe and North America, most importantly continuous vaccination of the pet population as
animals are born into it, may not be practically feasible in a number of African countries where
(bi)annual vaccination campaigns by public veterinary services will be more effective if properly
applied. This question can only be answered by taking a closer look at domestic dog populations in
these countries including: dog demography, dog ecology patterns, extent of movement of virally
infected animals, rabies transmission dynamics, and the effectiveness of current vaccination strategies
[14, 46]. Current control measures could possibly be unsuccessful due to a lack of knowledge or
misunderstanding of the ecology of dog populations, or the insufficient identification of the sources
and routes of transmission from reservoirs to species of concern. In potentially complex reservoir
systems, such as rural communities in close proximity to conservation areas, control will depend on
understanding how rabies in maintained.
Human and animal rabies can be eliminated through
measures targeting the dog population in the case of domestic dogs being the sole maintenance
population. The real threat of a disease such as rabies can only be understood with epidemiological
and demographic data on dog populations.
The objective of this study was to collect data through a household-level census in communities
bordering a large privately-owned conservation area, during which we gathered information on
human:domestic dog ratios, contraception demand, pet ownership aspects and rabies vaccination
coverage achieved. With this data we aim to assess rabies-vaccination coverage and other factors that
might influence the success of the on-going vaccination campaign in the study areas. This study
involved collection of interview data only, without clinical intervention or sampling.
Dog population characteristics and rabies vaccination coverage
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2 Materials & Methods
2.1
Study area
The study was conducted in the north-eastern corner of the Bushbuckridge Local Municipality,
Mpumalanga Province of South Africa. The four settlements in which the census took place include
Athol, Utah A, Dixie and Utah B (Scheme). All four of these communities border the northern fence line
of a large privately-owned conservation area to the south (see map). The distances from the farthest
households of these communities to the Sabi Sand Game Reserve fence line are: Athol 1,4 km, Utah A
2,8 km, Dixie 2,2 km and Utah B (Scheme) 2,4 km. The area of each site was calculated by using the
borders of the stands on the outskirts of the community as the boundaries for calculation via Google
Maps. Athol covers an area of 1,51 km2, Utah 0,9 km2, and Dixie 0,34 km2. The closest medical clinics
are situated in Utah A and Hluvukani and the only Animal Health Center in the region is located in
Hluvukani. The study area comprises community land with rural settlements surrounded by bushveld
where cattle owners take their herds to graze.
2.2
Study populations
The census was designed as a census rather than a cluster sampling study to eliminate as many biases
as possible and assess the number of owned dogs and of dog-owning households within the study
wards. It is a common misperception in rural Africa that a large proportion of the dog population are
ownerless ‘stray’ dogs [15] but our impression from working in the field is that the majority of dogs in
the studied settlements are kept by local people and therefore these dogs are owned (or domestic)
dogs rather than stray dogs. The domestic dog in this area is to a greater or lesser extent dependent
on humans for survival but confinement to a particular household is not a general practice, rather dog
owners allow their pets to roam free. Dogs are kept for security purposes, to accompany grazing herds
Dog population characteristics and rabies vaccination coverage
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and occasionally for hunting practices. The majority of dog owners keep their dogs outdoors with no
or basic shelter.
In case the research team came across a roaming dog in the street, the team
managed to identify its household and collect information about the dog. It is not certain that there
are no unowned dogs in the research area but this study has not come across any dogs without a
reference household.
A map of each of the three study areas was printed using Google Earth to visualize all stands
within the community boundaries. Each household has been given a unique stand number by the
municipality consisting of 5 numbers which is shown on a white sign attached to the outside wall of
(most of) the houses. The communities are divided into sections based on the first number of that
unique stand number. The team of interviewees would write down the stand number on that specific
stand on the map. By looking at the map they could see which households had not been visited yet
and, once the whole community had been completed, whether no households had been forgotten.
Households that needed to be revisited were marked with a separate color on the map.
2.3
Questionnaire
To assess the number of owned dogs and dog-owning households within the four communities, a full
household-level census on dog ownership was carried out. A household questionnaire was designed
to gather information related to household- and dog characteristics (including vaccination coverage).
Each household was visited by the interviewer, accompanied by a research assistant to assist with
translations to and from Shangaan and for assistance with the collection of photos of all dogs. The
purpose of this study was explained to the head of each household visited. After obtaining the
participants’ verbal consent the questionnaire was read out loud to the participants over the age of 18
and the answers directly recorded on a tablet with Open Data Kit (ODK) software. Data were
downloaded in a Comma Separated Values format. Information was then automatically transferred to
a Microsoft Excel spreadsheet for analysis. Re-visits were conducted if no (adult) household member
could be interviewed at the first visit or if some of the required information was missing.
2.4
Demographic parameters
The questionnaire focused on household characteristics recording the location of each household
using a global positioning system (GPS) tool in ODK, the stand number, number of people
permanently living at the household and number of dogs currently owned. The dog demography
section of the questionnaire collected descriptive data about each dog and its management: (i) sex (ii)
age (iii) sterilization status (iv) degree of confinement (i.e. confined, at times, roams free, caged). The
age of dogs was determined not only by asking inhabitants both age and date of birth of the dog, but
also by appearance of the dog whenever the owner was not sure of the age of the dog. Estimation
was made to the nearest month for dogs younger than a year and to the nearest year for older dogs.
A separate section for questions specific to female dogs (reproductive history and contraception
preference) included: (v) reproductive history of females including number of litters in lifetime and
within the last 12 months and size of the latest litter (vi) fate of pups (i.e. kept, sold, given away or
died) (vii) reason for pups dying and (viii) current age of the pups. Information on achieved coverage
of vaccination was collected by asking dog owner (i) vaccination status (ii) with which vaccine (i.e.
rabies, 5-in-1, other or unknown) (iii) when the vaccination took place (i.e. <12 months ago, 12-24
months ago, 25-36 months ago, >36 months ago or unknown) (iv) where or by whom the dog was
Dog population characteristics and rabies vaccination coverage
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vaccinated (i.e. during a campaign, by the Hluvukani Animal Health Clinic, by a private veterinarian or
unknown) and finally (v) whether or not the owner could produce a certificate of dog vaccination.
A vaccination certificate is provided to dog owners for each dog vaccinated. In case of a bite
incident this certificate can be of great importance and it is therefore important for owners to keep
their dogs’ vaccination certificates. In order to assess dog vaccination coverage participants were
asked for a vaccination certificate as proof of dog vaccination. The current census was carried out
approximately 4-6 months after the annual vaccination campaign so the chance of dog owners losing
their certificates was plausible yet small. When a dog owner was unable to produce a certificate,
further questioning on the specific month of vaccination and the answer that was given – in relation to
the latest mass vaccination campaign date – would make the vaccination status of the dog more or
less trustworthy.
The final questions in the questionnaire, in case of ownership of a female dog, were related to
the dog owner’s demand for contraception. Questions included (i) if the owner would be interested in
a two-year contraceptive injection (GnRH-vaccine) for their dog (ii) reason for interest (i.e. to stop
litters, to stop estrus behavior or both) or reason for not being interested (i.e. want puppies, cultural/
social reason, do not care or other reason) (iii) preference for permanent or temporary contraception
(iv) whether or not owner is willing to pay for a two-year contraceptive injection and how much the
owner is maximum willing to pay for such an injection. The latter was evaluated by following the
recommendations from previous surveys in which the willingness to pay was evaluated [47, 48]. Dog
owners participating in our study were asked three close-ended yes-no questions: 1) if they would be
willing to pay for a contraceptive injection for their dog 2) if the answer to the first question is ’yes’ the
owner would then be asked whether they would purchase the product if it were offered at 100 Rand
($9) 3a) if the owner is willing to pay 100 Rand they are they are then asked if they would be willing to
pay 200 Rand ($18) 3b) if the participant refuses to pay 100 Rand or is unsure, he/she is asked if they
would be willing to pay 20 Rand ($2). The final open-ended question would then be what the highest
price is they would be willing to pay.
All interviews were conducted between July 3, 2013 and September 28, 2013. This study is the
first estimation of dog population size in the area.
2.5
Photo database
The database was compiled as a resource to investigate the utility of such a method (e.g. identifying
individual dogs using their natural markings) for mark-recapture studies to estimate dog population
size, and to identify unknown and possibly unowned dogs in the communal areas.
Our aim was to take a left side, right side and facial picture of all dogs. Dogs were photographed
while the owner handled the dog (without physically trapping them) or from a distance in case the
dog could not be approached. Photos were later sorted and entered into an online database
(www.geerdes.nl/DogiD) designed especially for this study. All dog photos were then tagged with
specific characteristics depending on the appearance of each individual dog in order to make it
possible to distinguish one dog from the other. With this combination of tags for each dog it is
possible to select certain characteristics according to the appearance of the dog that has been located
by the research team. If the right features have been entered the database will then show you the
photos of dogs that match the search criteria. The selection criteria include: sex, coat pattern, coat
color(s), coat length, posture, eye color, position of the ears, one or more distinct white socks on one
or more paws/lower legs, tail length and distinct features (including location) (e.g. ridge on the back,
scars, amputated leg, damaged ear or damaged eye).
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 8
3 Statistical analysis
3.1
Household characteristics
Human population dynamics
Descriptive analyses were performed for total number of households, total number of people, number
of people per household (average, median, range and IQR) and people per km2.
Dog ownership patterns
Interviewed households were divided in dog owning households (DOHH) and non-dog owning
households (NOHH) [29]. The human:dog ratio was estimated by summing the total number of people
and dividing by the total number of dogs per study site. In addition the number of dogs per
household and per DOHH (average, median and IQR) was estimated.
3.2
Dog demographics
Dog population dynamics
Calculations of total number of dogs, dog density and confinement statistics were performed on the
collected data. The dog population density in each site was obtained by dividing the dog population
by the area of the study site.
Sex and age distribution
Statistics on total male dogs, total female dogs, male/female ratio, age characteristics (e.g. mean,
median, mode and range) and neutered proportion.
Female reproduction
Data on female reproduction was used to calculate mean litter size, pup mortality, reasons for pups
dying, fate of the puppies, number of litters/female in lifetime and mean litter size/female which were
reported in the past 12 months.
3.3
Contraception demand
The number of female dog-owners interested in contraception by injection, reasons for interest,
preference for permanent or temporary contraception and willingness to pay were observed by
descriptive analyses of the collected data.
3.4
Vaccination coverage
The main outcome measure of the study was the overall vaccination coverage. This was calculated for
dogs >3 months old separately for each community by dividing the total number of vaccinated dogs
(in the past three years) by the overall population of dogs. Calculations are made twice, one for dogs
with and without certificates of proof (+/-) and one for dogs exclusively with a certificate of proof (+).
Dogs vaccinated more than three years ago are considered unvaccinated.
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 9
Additionally a vaccination coverage-range has been calculated which reflects a ‘worst case scenario’
and a ‘best case scenario’. In the worst case we assume that the dogs of which we do not know their
vaccination status have not been vaccinated against rabies and are therefore given the status
‘unvaccinated’. In the best case we assume that the dogs of which we do not know their vaccination
status have been vaccinated. The lower limit excludes the unknowns and the upper limit assumes that
all unknowns are vaccinated. Further focus lays on vaccination coverage in age classes and location
where vaccination took place.
3.5
Significance of sex and confinement on vaccination status
The chi-squared test for comparison of two groups and two outcomes in a 2x2 contingency table was
used to evaluate the association of the vaccination status of a dog with sex, and with degree of
confinement. The frequencies observed in Dixie were often less than 10 and therefore Fischer’s exact
test was used.
3.6
Ethical clearance
The study was approved by the University of Pretoria Animal Ethics Committee. Permission and
informed consent were obtained from the University of Pretoria and study participants.
Dog population characteristics and rabies vaccination coverage
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Page | 10
4 Results
Utah B (Scheme) was left out of the performed analyses because fieldwork revealed that this
settlement is solely a place where cattle farmers bring their cattle for the day. Farmers do not spend
the night at the site; the scarce number of buildings is only used for cattle owners to rest during the
day. Besides, there is a verbal agreement between all cattle owners that dogs are not allowed in this
settlement.
In all three communities there were a number of dogs of which we were not able to collect any
information (e.g. age, sex, confinement, reproductive history, sterilization status, vaccination status)
from the owner despite multiple visits to the household. This amounted to 12 dogs in Athol, 8 dogs in
Utah and 8 dogs in Dixie of which the details remain unknown. These missing data were taken into
account in the following results and calculations.
4.1
Household characteristics
Human population dynamics
A total of 1086 households were interviewed representing a total of 5115 persons. Summary of the
human population data obtained during the questionnaire surveys are shown in Table 1.
Variable
Households interviewed
Total people
Area in km2
People per household
Mean
Median
Range
IQR*
People per km2
Athol
571
2928
1,5
Utah
380
1703
0,9
Dixie
135
484
0,3
5,3
5
1-21
3-7
1952
4,5
4
1-13
3-6
1893
3,6
4
1-13
2,8-5
1424
Total
1086
5115
Table 1 Summary human population data collected from questionnaire surveys (* Interquartile Range – 25th and
75th percentile)
Dog ownership patterns
Of all the households included in this study 227 (21%) were DOHH and 863 (79%) of them NOHH. The
overall dog:human ratio was one owned dog for every twelve inhabitants (1:12). Table 2 gives an
overview of dog ownership information for each of the three communities.
Variable
Dog:human ratio
Dogs per household
DOHH (n)
NOHH (n)
Dogs per DOHH
Mean
Median
IQR
Athol
1:11
0,4
25,0% (143)
75,0% (428)
Utah
1:15
0,3
15,3% (58)
84,7% (322)
Dixie
1:11
0,3
19,3% (26)
80,7% (109)
1,7
1
1-2
2,0
1
1-2
1,7
1
1-2
Table 2 Summary of dog ownership information collected from questionnaire surveys
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 11
4.2
Dog demographics
Dog population dynamics
A total number of 413 dogs in three communities were recorded during the census. The majority of all
dogs in the three study wards are considered to be ‘free roaming’ dogs by their owner. A small
percentage of dogs is always confined to the household boundaries or leaves the household at times
when the owner leaves the premises. Table 3 and Figure 1 show more detailed data on dog
demographics and confinement characteristics.
Variable
Total dogs
Dogs per km2
Confinement
Always (n)
In part (n)
Roams free (n)
Caged (n)
Athol
253
169
Utah
115
128
Dixie
45
133
12,9% (31)
10,8% (26)
76,4% (184)
0% (0)
16,8% (18)
21,5% (23)
61,7% (66)
0% (0)
10,8% (4)
10,8% (4)
78,4% (29)
0% (0)
Table 3 Summary dog population data collected from questionnaire surveys
Sex and age distribution
Data on sex and neutering is summarized in Table 4. Age distribution by sex is shown in Table 5.
Figure 1 represents the age distribution as percentages of the total number of dogs per community.
Variable
No. female dogs (n)
No. male dogs (n)
Male:female ratio
Percentage neutered (n)
Athol
39,4% (95)
60,6% (146)
1:0,7
0% (0) of males
0% (0) of females
Utah
41,1% (44)
58,9% (63)
1:0,7
11,1% (7) of males
0% (0) of females
Dixie
35,1% (13)
64,9% (24)
1:0,5
5,4% (2) of males
2,7% (1) of females
Table 4 Summary sex distribution and neutering information collected from questionnaire survey
Variable
4-11 months
Male
Female
12-23 months
Male
Female
24-35 months
Male
Female
36-47 months
Male
Female
48-59 months
Male
Female
60-71 months
Male
Athol
17,4% (42)
64,3% (27)
35,7% (15)
15,8% (38)
68,4% (26)
31,6% (12)
18,7% (45)
60,0% (27)
40,0% (18)
22,4% (54)
66,7% (36)
33,3% (18)
5,8% (14)
57,1% (8)
42,9% (6)
4,6% (11)
72,7% (8)
Utah
19,6% (21)
52,4% (11)
47,6% (10)
11,2% (12)
41,7% (5)
58,3% (7)
15,0% (16)
62,5% (10)
37,5% (6)
15,0% (16)
43,8% (7)
56,2% (9)
12,1% (13)
46,2% (6)
53,8% (7)
4,7% (5)
80,0% (4)
Dixie
15,8% (6)
50,0% (3)
50,0% (3)
10,5% (4)
75,0% (3)
25,0% (1)
13,2% (5)
80,0% (4)
20,0% (1)
10,5% (4)
75,0% (3)
25,0% (1)
5,3% (2)
0% (0)
100,0% (2)
5,3% (2)
100,0% (2)
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 12
Female
72+ months
Male
Female
Age unknown
Male
Female
27,3% (3)
7,5% (18)
44,4% (8)
55,6% (10)
7,9% (19)
31,6% (6)
68,4% (13)
20,0% (1)
10,3% (11)
72,7% (8)
27,3% (3)
12,1% (13)
92,3% (12)
7,7% (1)
0% (0)
7,9% (3)
33,3% (1)
67,7% (2)
31,6% (12)
75,0% (9)
25,0% (3)
Table 5 Age distribution by sex in % and number of animals (n)
Age distribution
35.0%
Percentage of dogs
30.0%
25.0%
20.0%
Athol
15.0%
Utah
10.0%
Dixie
5.0%
0.0%
4-11 m
12-23 m 24-35 m 36-47 m 48-59 m 60-71 m
72+ m Unknown
Age class
Figure 1 Age distribution as percentages of the total number of dogs per community
Female reproduction
Table 6 summarizes the female reproduction information obtained during the questionnaire surveys.
Reasons for puppies dying are shown in Figure 2. What happened to the puppies in the period after
birth, according to their owners, is shown in Figure 3.
Variable
No. of adult females (12+ months)
Total no. of litters in lifetime
Average no. of litters past 12 months
(standard deviation)
No. pups born in the past 12 months
Average litter size
Median litter size
Mode litter size
IQR litter size
Pups dead %
Average no. of pups dead
Athol
67
120
1,2
(0,5)
246
5,0
5
3
2-7
45,9%
4,0
Utah
33
48
1,0
(0,4)
110
5,0
5
Dixie
10
22
1,3
(0,4)
42
5,2
4
3,3-6
43,6%
3,2
2,8-7,5
0%
0
Table 6 Summary female reproduction information collected from questionnaire survey
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 13
Percentage of total responses
Reasons for puppies dying
35.0%
30.0%
25.0%
20.0%
15.0%
10.0%
5.0%
0.0%
Athol
Utah
Reasons given
Figure 2 Reasons given by owners for puppies dying
Fate of puppies
Percentage of total responses
60.0%
50.0%
40.0%
Athol
30.0%
Utah
20.0%
Dixie
10.0%
0.0%
Kept
Given away
Sold
Died
Unknown
Figure 3 Fate of puppies according to the owners
4.3
Contraception demand
The owners of female dogs were asked whether or not they would be interested in contraception for
their dog(s). Table 7 shows the percentages of particular responses from owners of female dogs.
Owners in Athol were willing to pay an average of $7 (median $5, mode $10, range $2-$10) for the 2year contraception injection. In Utah owners were willing to pay an average of $8 (median $10, mode
$10, range $2-$10) for the 2-year contraception injection. Dog owners in Dixie were willing to pay an
average of $9 (median $10, mode $10, range $5-$10) for the 2-year contraception injection.
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 14
Variable
Demand for injection
Interested
Not interested
Unknown
Reasons for interest
To prevent litters
To inhibit estrus behavior
Both reasons
Preference
Permanent
Temporary
Willing to pay
20 Rand ($2)
100 Rand ($9)
200 Rand ($18)
Athol
Utah
Dixie
78,5% (51)
15,4% (10)
6,2% (4)
81,5% (22)
18,5% (5)
0% (0)
75% (6)
25% (2)
0% (0)
35,3% (18)
2,0% (1)
62,8% (32)
4,6% (1)
0% (0)
95,5% (21)
0% (0)
0% (0)
100% (6)
88,2% (45)
11,8% (6)
95,5% (21)
4,6% (2)
100% (6)
0% (0)
95,5%(21)
83,3% (20)
0% (0)
100% (7)
50% (7)
0% (0)
100% (1)
83,3% (5)
0% (0)
Table 7 Summary contraception information collected from questionnaire surveys
4.4
Vaccination coverage
General information regarding vaccination coverage
Table 8 shows the different types of vaccinations (e.g. rabies, 5-in-1, other type, and unknown type)
and the number of times these vaccinations were mentioned by the owners of the vaccinated dogs.
Variable
Rabies
5-in-1
Other
Unknown
Athol
128
1
1
2
Utah
79
0
0
1
Dixie
24
0
0
0
Table 8 Summary of vaccination types
Dog owners were asked where or by whom their dogs were vaccinated. Table 9 summarizes the
responses given by the owners.
Variable
Campaign
Hluvukani Clinic
Private vet
Unknown
Athol
87,5% (112)
11,7% (15)
0% (0)
0,8% (1)
Utah
89,9% (71)
10,1% (8)
0% (0)
0% (0)
Dixie
95,8% (23)
4,2% (1)
0% (0)
0% (0)
Table 9 Overview in % (n) of the different locations and people involved in vaccinating dogs
Overall vaccination coverage sampled population
Athol
The sample population in Athol of which we were able to collect the vaccination status consists of 241
animals. In eight cases it occurred that the owner did not know the vaccination status of their dog
which gives us a total of 233 dogs of which the vaccination status is known. Unfortunately another two
owners, despite stating their animal as ‘vaccinated’, could not remember the type of vaccine that was
given. These 2 dogs have thus been stated to have an ‘unknown’ vaccination status with regard to the
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 15
following analyses. The sampled population size of which the vaccination status is known come to a
total of 231 dogs plus 22 dogs with an unknown vaccination status.
Utah
The sample population in Utah of which we were able to collect the vaccination status consists of 107
animals. In one case it occurred that the owner did not know the vaccination status of his/her dog
which gives us a total of 106 dogs of which the vaccination status is known. Unfortunately one owner,
despite stating his/her animal as ‘vaccinated’, could not remember the type of vaccine that was given.
This dog has thus been stated ‘unvaccinated’ with regard to the following analyses. The sampled
population size of which the vaccination status is known come to a total of 105 dogs plus 10 dogs
with an unknown vaccination status.
Dixie
The sample population in Dixie of which we were able to collect the vaccination status consists of 37
animals. In three cases it occurred that the owner did not know the vaccination status. The sampled
population size of which the vaccination status is known comes to a total of 34 dogs plus 11 dogs of
with an unknown vaccination status.
The results in Table 10 are based on calculations using the sample size of 253 dogs for Athol, 115
dogs for Utah, and 45 dogs for Dixie. Vaccination coverage is based on dogs vaccinated within the last
three years. Dogs vaccinated more than three years ago are considered unvaccinated.
Variable
Sampled no. of dogs
+/- certificate
+ certificate
Unvaccinated
Unknown
Vaccination coverage range
Athol
253
48,6% (123)
22,1% (56)
42,7% (108)
8,7% (22)
48.6% - 57.3%
Utah
115
68,7% (79)
33% (38)
22,6% (26)
8,7% (10)
68.7% - 77.4%
Dixie
45
53,3% (24)
6,7% (3)
22,2% (10)
24,4% (11)
53.3% - 77.8%
Table 10 Vaccination coverage in % (n) of sampled dog population (with or without certificate & with certificate
only), and percentage (n) of unvaccinated dogs and dogs with an’ unknown’ vaccination status. Including and
excluding the group of dogs with an unknown vaccination status in the vaccination coverage range shows us
upper and lower limits of vaccination coverage in the three communities.
The vaccination coverage can be further specified by subdividing the coverage in to different groups.
Table 11 demonstrates the vaccination coverage set out in categories of ‘time since last vaccination’.
Thereafter Table 12 subdivides the vaccination coverage even further in to age groups and sex.
Variable
< 12 months ago
12-23 months ago
24-35 months ago
> 36 months ago
Athol
51,1% (118)
2,2% (5)
0% (0)
1,3% (3)
Utah
65,7% (69)
6,7% (7)
2,9% (3)
0% (0)
Dixie
52,9% (18)
11,8% (4)
5,9% (2)
0% (0)
Table 11 Vaccinated coverage (+/- certificate) in % (n) categorized by ‘time since last vaccination’
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 16
Variable
Juveniles*
Male
Female
Adults
Male
Female
Athol
31,0% (13)
25,9% (7)
40,0% (6)
60,0% (108)
59,2% (67)
61,2% (41)
Utah
38,1% (8)
36,4% (4)
40,0% (4)
84,9% (62)
85,0% (34)
84,8% (28)
Dixie
83,3% (5)
100% (3)
66,7% (2)
75,0% (15)
84,6% (11)
57,1% (4)
Table 12 Vaccination coverage (+/- certificate) in % (n) categorized by age group and sex (*less than 12 months
of age)
Percentage of animals vaccinated
Vaccination coverage juveniles
120.0%
100.0%
80.0%
Athol
60.0%
Utah
40.0%
Dixie
20.0%
0.0%
Male
Male + certificate
Female
Female + certificate
Figure 4 Vaccination coverage juveniles (with or without certificate & with certificate only)
Percentage of animals vaccinated
Vaccination coverage adults
90.0%
80.0%
70.0%
60.0%
50.0%
Athol
40.0%
Utah
30.0%
Dixie
20.0%
10.0%
0.0%
Male
Male + certificate
Female
Female + certificate
Figure 5 Vaccination coverage juveniles (with or without certificate & with certificate only)
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 17
Variable
4-11 months
Male
Female
12-23 months
Male
Female
24-35 months
Male
Female
36-47 months
Male
Female
48-59 months
Male
Female
60-71 months
Male
Female
72+ months
Male
Female
Unknown age
Male
Female
Athol
31,0% (13)
25,9% (7)
40,0% (6)
52,6% (20)
53,8% (14)
50,0% (6)
57,8% (26)
55,6% (15)
61,1% (11)
72,2% (39)
69,4% (25)
77,8% (14)
71,4% (10)
87,5% (7)
50,0% (3)
54,5% (6)
37,5% (3)
100% (3)
66,7% (12)
75,0% (6)
60,0% (6)
10,5% (2)
0% (0)
15,4% (2)
Utah
38,1% (8)
36,4% (4)
40,0% (4)
75,0% (9)
60,0% (3)
85,7% (6)
75,0% (12)
80,0% (8)
66,7% (4)
93,8% (15)
100% (7)
88,9% (8)
92,3% (12)
100% (6)
85,7% (6)
80,0% (4)
75,0% (3)
100% (1)
90,9% (10)
87,5% (7)
100% (3)
69,2% (9)
66,7% (8)
100% (1)
Dixie
83,3% (5)
100% (3)
66,7% (2)
75,0% (3)
100% (3)
0% (0)
100% (5)
100% (4)
100% (1)
50,0% (2)
66,7% (2)
0% (0)
50,0% (2)
0% (0)
50,0% (1)
100% (2)
100% (2)
0% (0)
100% (3)
100% (1)
100% (2)
33,3% (4)
44,4% (4)
0% (0)
Table 13 Total rabies vaccination coverage, in % and number of animals (n), within the last three years by age/sex
(with or without certificate)
Significance of sex and confinement on vaccination status
The vaccination status of dogs in the 3 villages was not found to be significantly associated (p>0.05)
with sex or degree of confinement (Table 15, 16 and 17).
Variable
Sex
Male
Female
Confinement
Always
In part
Roams free
Vaccinated
Non-vaccinated
74
49
64
44
P
0.97477288
0.29056535
17
17
89
13
9
86
Table 15 Significance (P<0,05) of sex and degree of confinement on vaccination status in Athol
Variable
Sex
Male
Female
Confinement
Always
In part
Roams free
Vaccinated
Non-vaccinated
46
33
15
11
14
17
48
3
6
17
P
0.92441941
0.83953792
Table 16 Significance (P<0,05) of sex and degree of confinement on vaccination status in Utah
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 18
Variable
Sex
Male
Female
Confinement
Always
In part
Roams free
Vaccinated
Non-vaccinated
18
6
5
5
3
4
17
1
0
9
P
0.14771141
0.21642648
Table 17 Significance (P<0,05) of sex and degree of confinement on vaccination status in Dixie
Dog population characteristics and rabies vaccination coverage
at the wildlife interface in the Mpumalanga Province of South Africa
Page | 19
5 Discussion
Rabies poses a threat not only for dog welfare and wildlife conservation, but also to human health,
especially in developing countries with the greatest burden in poor rural communities. With the
domestic dogs being the main reservoir of the virus, control of the disease lies in recognizing the
implications of demographic characteristics of dog populations [29]. Assessing the rabies vaccination
coverage in dog populations is necessary to monitor the effectiveness of vaccination campaigns. This
report provides the results of the first attempt to gain a better understanding of dog ecology, dog
demography, and the success rate of recent vaccination campaigns in three communities bordering a
large private nature reserve in the Mpumalanga Province of South Africa.
The study area was chosen for its proximity to an Animal Health Centre and its personnel, the
presence of rural settlements adjacent to conservation areas, and for the fact that rabies vaccination
campaigns have been carried out in the study villages in the past couple of years. Ecological studies of
dog populations in rural settlements bordering the fences of conservation areas, which are home to
an abundance of wildlife, are generally rare and have not been conducted in this particular study area.
The four communities in which the interviews took place are less than three kilometers from the
nearest wildlife fencing. Cases of dogs roaming free in the conservation area are reported on a regular
basis and spillover of rabies to wildlife species is a realistic scenario.
Although the results are based on a census survey to collect information of each individual dog
in each community, details from a number of dogs could not be obtained due to the short time frame
of this study or the absence of the owners of the dogs during the period in the field. Exact numbers
on missing data are mentioned in the results section above. The rabies vaccination coverage is
nevertheless accurately determined within the three communities by describing two scenarios in our
statistical analysis. However, the bias with collection of information through questionnaires is the
validation of responses given by the interviewees and conclusions may be biased by response rates
and motivation of responding individuals. Therefore the age structure of dogs and the vaccination
coverage based on oral declaration without proof of a certificate must be interpreted with care.
Dog densities of 169 dogs/km2 in Athol, 128 dogs/km2 in Utah, and 133 dogs/km2 in Dixie are lower
than study results from urban wards in central Tanzania (334 dogs/km2) [9] and India [26] but higher
than dog densities found in rural areas of the Serengeti District and the Ngorongoro District in
Tanzania where dog densities have been found to be respectively 10,3 dogs/km2 and 2,5 dogs/km2
[22]. The estimated average densities in our study have by far exceeded the suggested threshold of >5
dogs/km2 for persistence of rabies in domestic dog populations in Africa [23] and the density of <25
dogs/km2 typical for rural Africa [15]. However, our study did not include rangeland when calculating
the study area and therefore a re-evaluation of dog densities should be made based on an accurate
measurement of the study area including the untilled land which surrounds the cultivated land. The
number of dogs in the latter calculation would stay the same but the area would increase, resulting in
much lower dog densities.
We found that the dog:human ratio is 1:11 and 1:15 in the three studied communities. The
dog:human ratio in Africa has been reported to lie between 1:3 and 1:12, whereas 1:6 is used as an
indicator for the global ratio [49]. Although rural areas commonly tend to have higher owned
dogs:human residents ratios compared to cities [28, 49], this study shows us low dog:human ratios in
rural areas compared to results that have been reported in Chile where the ratio in rural areas is 1:7
[29] and rural villages of Northern Tanzania where the ratio is 1:6 [15]. Even so, without local
references of human and dog densities and dog:human ratios it is relatively difficult to get full insight
Dog population characteristics and rabies vaccination coverage
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into dog demographics. More longitudinal studies will need to be conducted before conclusions can
be drawn on dog population dynamics in this region of South Africa.
The overall proportion of dog owning households identified in the three communities (25%,
15.3%, and 19.3%) correspond to estimates from non-African countries such as Taiwan (22,9%), Japan
(24,2%), and Sweden (15,5%) but also with the mean percentage of 20,1% and 11,5-33,8% of DOHH
reported in rural communities in Tanzania [28, 50]. Rural populations in Zimbabwe (54%), Zambia
(42%) and Kenya (53-81%) reported higher proportions of DOHH [28]. Whether lower rates of dog
ownership in our study allows for a more successful control of rabies remains to be seen.
More than 60% of the dogs were found to be free roaming in all three communities. These results are
similar to confinement status statistics found in comparable settings in Madagascar [46], Kenya [51],
and Chile where it appears that although urban areas have higher proportions of confined animals,
the number of reported ownerless dogs roaming free in urban settlements is much higher than in
rural areas [29]. It seems the group of free roaming dogs in rural areas do not consist of ‘strays’ but
rather of owned dogs roaming free as the result of the unwillingness of the owners to confine their
animals [11].
A significant association between confinement and vaccination status has been demonstrated
by dog rabies study in the Philippines [52]. Our study on the other hand does not match these
findings. We did not detect any significance between confinement characteristics and the vaccination
status of dogs in the three communities, which is consistent with the results found in communities in
the Serengeti [53]. Nevertheless, it seems a legitimate theory that with a majority of dogs roaming free
in all three communities, accessibility to vaccination is much less likely even though the owners are
usually traceable. Besides, owners are often unable to handle their dog which also contributes to
fewer dogs accessible for vaccination.
The dog populations were comprised principally of adult (>1 year of age) animals which made up 52 69% of the dog populations in the three communities. Rural villages in India show a comparable
distribution of age [26]. In Athol 23% of the age distribution was skewed toward dogs between the
ages of 2-3 years, while in Utah most dogs were between the ages of 4-12 months old. With the
overall mean age of the dog population in the three communities being > 3 years and therefore more
than the duration of immunity offered by the rabies vaccine (3 years), we assume that one dose of
vaccine would (generally) be insufficient to protect each dog for the duration of life.
Our study has not included puppies under the age of three months because it is a common
perception that these youngsters cannot be vaccinated. Including them in our study would have
negatively influenced our vaccination coverage results. Nevertheless, if we had included the number of
puppies under the age of three months in our age group <12 months of age, a much larger
proportion of the dog population would have been less than one year old which is consistent with
reports from Kenya and the Philippines [28]. If this would be the case then more frequent vaccination
of dogs (including newborn puppies) and more knowledge of the turnover rate in these particular dog
populations would be necessary to fully understand the dog population dynamics and to design an
appropriate vaccination model.
The sex ratio of the dog population in all three communities is skewed towards males, with 61% males
in Athol, 59% males in Utah, and 65% males in Dixie. These findings are consistent with reports from
other parts of the world where male dogs also predominate [26, 29, 54]. Male dogs are preferred due
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to the belief that they are better at guarding property, protecting livestock, and hunting [46]. A second
likely explanation is the killing or abandoning of female puppies by the owner in the first weeks after
birth and therefore a higher mortality rate of females due to active selection of male dogs [49]. A
research on associations of cryptorchidism with sex ratio on 11.000 litters in 12 purebred dog breeds
in The Netherlands prove highly significant global effects of carriership for cryptorchidism on
reproductive performance at weaning level [55]. Further insight into possible reasons for the unequal
distribution of sexes in our study area could potentially be of great value for animal population
management measures. Despite the unequal distribution, sex did not appear to be positively
associated with vaccination coverage, which is in contrast with results from the Philippines where sex
and vaccination status are significantly associated [52].
The dog population turnover rate was not calculated in our study but data on fecundity of
females was collected from household interviews. From information on litters in the past 12 months
the average number of litters in all three communities ranged from 1,0-1,3 litter(s), the mean size of
the litter was 5,0-5,2 pups and the mortality in the first week after birth 0-45,9%. These findings are
consistent with results from Kenya where mean litter size was found to be 4,7 and 5,2 and mortality
22% [51]. According to the dog owners, disease was the most common reason for the loss of puppies
although the majority of dog owners replied not to know the reason for their animals dying. Previous
studies have also found disease to be the most common cause of loss ranging from 36-52% [28].
Whether or not the low survivorship of new born puppies is compensated by a high fecundity rate and
thus a frequent population turnover and continued population growth will need to be further
investigated.
Neutered dogs are not a common finding in any of the three communities. In Athol none of the
dogs was neutered, in Utah 11% of males and 0% of females were found to be neutered, and in Dixie
the percentage of neutered males and females was respectively 5% and 3%. These results are not
surprising for the proportion of neutered dogs in the developing world is typically less than <10%
[28]. A single mobile clinic which is currently offering free neutering in the Bushbuckridge Municipality
may very likely have insufficient capacity to visit communities as frequent as necessary for fertility
control of these dog populations. An alternative for surgical intervention could potentially be the use
of immunocontraceptive vaccines in tandem with rabies vaccination programs [43]. Our study results
demonstrate the positive interest in and the willingness of the dog owners to pay for such a vaccine.
More detailed research will need to be performed on the differences in reproduction, survival, and
accessibility of dogs, as well as personal preferences and beliefs of dog owners in order to decide on
appropriate fertility inhibitors.
The effectiveness of previous vaccination campaigns in the study area was monitored by assessing the
rabies vaccination coverage around 4-6 months after the annual vaccination campaigns. Vaccination
coverage results of 48,6% in Athol, 68,7% in Utah and 53,3% in Dixie at that time of the year when this
study took place are sufficient in context of the critical threshold of ~40% in the period between
campaigns. Coverage will naturally decline after a campaign because of the natural turnover of a
population but whether it remains high enough in between campaigns to prevent outbreaks of rabies
is, among other factors, dependent on whether or not the target coverage of ~70% is achieved during
the annual campaign. The vaccination coverage achieved in our study is slightly lower compared to
the coverage reported from rural areas in Tanzania (80,3%), Philippines( 76%), Mexico (78,4%) and Sri
Lanka (66%) [28].
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Our overall vaccination coverage calculations (with or without certificate & with certificate only)
are based on the assumption that the dogs of which the vaccination coverage is unknown are not
vaccinated against rabies. For Athol, Utah, and Dixie these results are respectively 48,6%, 68,7%, and
53,3%. These rates also represent the lower limits of the vaccination range in each of the communities
individually. In order to get an idea of the upper limit of the vaccination coverage range calculations
were repeated, this time assuming that the dogs with an unknown vaccination status are indeed
vaccinated against rabies. The rates representing the upper limits of the vaccination range are 57,3%
in Athol, 77,4% in Utah, and 77,8% in Dixie. In case of the latter scenario both Utah and Dixie reach the
70% vaccination target. Nevertheless, it is unlikely that all dogs with an unknown vaccination status
are vaccinated against rabies and therefore these higher coverage rates are most probably
overestimates of the true coverage. If we only consider dogs to be vaccinated when they have their
certificate our study reaches significantly lower coverage results of 22,1% in Athol, 33,0% in Utah and
6,7% in Dixie. It is, however, plausible that dogs declared as vaccinated by their owner but without a
certificate of proof were misidentified as vaccinated and the overall vaccination coverage may thence
be overestimated. Local populations need to be made aware of their responsibility in saving their
vaccination certificates for example by instructing dog owners of the legal importance of the
certificates as an indicator of vaccination against rabies.
Despite the overall vaccination coverage being less than 70% in all three communities at the
time of this research, there are only a few reported rabies cases in the area. This suggests that the
lower levels of vaccination coverage may also be effective because they remain above the critical
threshold to prevent rabies outbreaks, which has been demonstrated in similar studies implemented
in Tanzania [8], and therefore the sporadic cases of rabies do not turn into epidemics. The differences
in required vaccination coverage are possibly due to the fact that each region has specific
transmission dynamics and therefor requires a different model based on a regional variety of
parameters. More scrutiny on demographic rates such as the birth- and death rates are very important
in determining both the target coverage to be achieved in the annual campaigns and the minimum
required coverage in between campaigns in this part of Africa. The target of 70% considered
necessary to prevent rabies outbreaks can only be achieved by implementing control measures that
reflect the characteristics of the dog population in the control area, including the ecology of the dog
population, an accurate estimation of the size of the dog population, and the frequency of campaigns
required to maintain coverage in a population with high a turnover rate. To improve the accessibility
of dogs to vaccination it is important to assess owner-specific reasons and dog-specific reasons for
failure of vaccination and to undertake long-term public education programs in the region. These
programs could promote owners to keep their dogs confined to the household and also take away
misconceptions regarding vaccination. Whenever vaccination targets are not reached, a second round
of vaccination should be applied.
Our results show that over 85% of dogs in all three communities were vaccinated during a
vaccination campaign where house-to-house visits were carried out. Although the central-point
vaccination strategy has proven to be simple and successful for vaccination of rural dogs in a previous
study in Tanzania [10], each country and region may require different approaches. Cultural attitudes
towards the handling of dogs and the intention of dog owners to care for their animals’ health could
ask for a different delivery of vaccinations (e.g. house-to-house, oral vaccination, central-point).
Perhaps the distance of the household from the central-point vaccination site could also be critical to
the success of a program. The rationale of dog owners’ participation in vaccination programs may be
Dog population characteristics and rabies vaccination coverage
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influenced by social, cultural and economic factors which will have to be further elaborated in this
particular area in South Africa in order to decide on the most effective strategy for vaccination.
There is a definite potential for rabies spill-over to wildlife species and the cross over is fairly easy due
to the generalist nature of the rabies virus strains. The three communities in this study lie adjacent to a
large private game reserve which presents the possibility of spill-over of rabies from domestic dogs to
wildlife populations. In order to gain more insight into the transmission dynamics in this particular
area, genetic characterization of rabies viruses remains an important tool for identifying sources of
infection and tracing routes of spread of rabies [56, 57]. Newly emerging virus-host associations can
be identified and knowledge of disease dynamics increased.
Previous studies on reservoir dynamics suggest that wildlife are not able to maintain rabies
cycles but can act as a reservoir for disease transmission to target populations. Certain maintenance
hosts may also become infected but are usually a dead-end host due to low transmission ratios.
Therefore the elimination of canine rabies in the maintenance host through mass dog vaccination
campaigns is also in this part of Africa likely to be sufficient for control of rabies in all other species
[22]. When rabies control measures in domestic dog populations appear to be insufficient it may be
necessary to analyze management interventions that directly target the wildlife host.
Not only veterinarians should increase their efforts to collect accurate data with optimal rabies
surveillance systems, also local communities, central authorities, and most importantly clinics and
hospitals need to join forces to collaborate and integrate. By working together we can tackle the
reasons for the low priority of rabies, the lack of resources, the gaps in knowledge of disease aspects,
and the lack of expertise in control strategies. Veterinarians, medical practitioners, and health
authorities have the responsibility to apply intersectoral collaboration under the motto of ‘One Health’
[58]. These parties should establish a strategy to increase awareness in local populations, share and
adjust protocols, exchange research data and conclusions, promote preventative measures, and
inform each other about disease aspects in humans and animals.
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6 Conclusion
In Bushbuckridge Local Municipality, Mpumalanga Province of South Africa where the study took
place, a combination of demographic studies and longitudinal studies of local free-ranging dog
populations will provide the required knowledge and insight about the dynamic and persistence of
rabies in the area. Analyses of continuously collected data will ensure maximum effectiveness and
coverage of vaccination campaigns. Analyzing details of the dog populations such as size, density,
movement, and turnover rates, and understanding the attitudes and actions of dog owners will assist
in bringing together the required resources needed for rabies control in this area.
The vaccination coverage in Athol, Utah and Dixie in the Bushbuckridge Municipality highlight the
importance of commitment towards rabies control programs in this area. Communication, awareness
creation, surveillance and consistency are the key words in the chances of success of such a program.
We need to strive for a high level of risk perception among dog owners and an increased belief in the
benefits of vaccination through public education activities. Proactive and sustainable vaccination
programs in the Western World have proven their efficacy in the eradication of domestic dog rabies;
this should provide a motivation and a model for South Africa in the fight against rabies.
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