Dog Ecology and Rabies Control in Africa
World Small Animal Veterinary Association World Congress Proceedings, 2014
Darryn Knobel, BVSc, PhD; Anne Conan, DVM, PhD
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, South Africa

Ecology is a broad field that deals with the relations of organisms to one another and to their physical surroundings. Population ecology is a subfield focusing on the dynamics of populations of particular species, and how these populations interact with their environment. In this paper, we discuss the importance of population ecology of domestic dogs Canis lupus familiaris in Africa for the effective implementation of rabies control and present an overview of recent studies on dog population ecology in southern Africa.

Rabies is a disease caused by infection with members of the genus Lyssavirus in the family Rhabdoviridae. In Africa, domestic dogs are a major reservoir host for rabies virus. Rabies transmitted by dogs remains a significant public health threat on the continent, particularly in underserved communities. In these settings, the virus is primarily maintained in populations of free-roaming dogs and is transmitted to people through bites or other contact with the saliva of infectious rabid dogs. Rabies in dog populations (and consequently in humans) can be controlled and in certain circumstances eliminated through the mass vaccination of dogs against the virus. The control of an infectious disease through vaccination relies on vaccinating a sufficient proportion of the host population to effect herd immunity. If a threshold proportion of individuals in a population are immune, the incidence of infection will decline. This critical vaccination threshold is a function of the basic reproductive number R0, which is the average number of secondary cases of infection produced by an infectious individual in an otherwise fully susceptible population. R0 for rabies in dogs has been estimated from a number of outbreaks around the world, and from this a critical vaccination threshold of 40% has been calculated.1 Thus, theory and empirical evidence predict that outbreaks of rabies in dogs can be controlled if at least 40% of the population is immune at any time. However, achieving this goal in free-roaming dog populations in underserved communities is hampered by the high birth and death rates in these populations, leading to high population turnover. In these areas, mass dog vaccination against rabies is usually implemented in short campaigns conducted annually or less frequently. Between campaigns, the proportion of immune individuals in the population declines as vaccinated dogs die and susceptible dogs enter the population through birth or migration. Understanding these dynamics through population ecology studies is therefore important for the effective implementation of rabies control through mass vaccination.

Despite the abundance of domestic dogs and the ubiquity of their association with us, we know surprisingly little about their population ecology. We understand more about the population demographics and ecology of some of their wild cousins, like the grey wolf Canis lupus, than we do about that of dogs themselves. The study of dogs is perhaps seen as the domain of veterinarians, who often lack the skills to implement population ecology studies, and who tend to focus on disease studies. Reluctance to undertake population ecology studies may also stem from the misperception that a large proportion of dogs in underserved communities in Africa are not owned, and therefore methodological approaches need to mimic those applied to wild carnivore populations. However, evidence from a number of recent studies in the region has shown that, despite appearances, the majority of dogs (over 90%) in these communities are owned.2-4 Thus, not only are levels of dog ownership and accessibility sufficient to enable control of rabies through mass dog vaccination, but they may also enable population ecology studies to be conducted using novel approaches adapted from human public health.

Health and demographic surveillance systems are used in public health to capture reliable population-based data on health in settings where there is limited registration of vital events, including births, deaths by age and sex, and medical causes of death.5 A health and demographic system (HDSS) monitors all individuals, households and residential units in a defined geographic area, known as a demographic surveillance area (DSA). Following an initial census of the defined population, longitudinal measurement of demographic and health variables is undertaken, through repeated visits at regular intervals to all residential units within the DSA. We propose that the HDSS approach be used as a model for population ecology studies of owned dogs in underserved communities in areas where canine rabies is endemic. These systems can also serve as platforms to investigate evidence-based approaches to rabies control and dog population management. To demonstrate the value of this approach, we describe a health and demographic surveillance system in dogs (HDSS-Dogs) in a population of owned, largely free-roaming dogs in an underserved community in South Africa.

The DSA of the HDSS-Dogs encompasses Hluvukani settlement (S 24°39' E 31°20'), an underserved community in Bushbuckridge Local Municipality, Mpumalanga Province. The DSA comprises around 2,000 households with a human population of around 10,000. The residential unit is a stand, on which one or occasionally more households reside. All stands are permanently and uniquely identified by the municipality. An initial census of the owned dog population in the DSA was conducted from July through November, 2011. To uniquely and permanently identify individual dogs, a microchip was subcutaneously implanted into dogs present at the start of the study, and into those dogs that entered the population during the study period. Following the census (round 1), five follow-up rounds (rounds 2–6) were conducted from December 2011 through May 2014. All owned dogs are recorded at each visit, as are demographic events including births, deaths, and migration into and out of the household. All 'residence episodes' of individual dogs in households are tracked and aggregated to provide the denominator of dog-time in the population. Residence episodes within households begin with birth or in-migration (e.g., purchase or receipt of a new dog) and terminate with death or out-migration (e.g., sale or gifting of dog to another household). Data from 1st January 2012 to 1st January 2014 are presented here. Data are presented in 3-month periods (i.e., quarterly). Point data are provided for the start of each quarter.

Table 1 shows the number of dogs, dog-owning households (DOHH), and the age and sex distribution of dogs, at the start of each quarter. Contrary to expectation, the total population of owned dogs declined by 10% during the 24-month period. However, there was a substantial fluctuation in this population, reaching a peak of 955 dogs in the last quarter of 2012 before declining sharply. Figure 1 shows the population sex ratio (males per female) for the same time points. Crude birth and death rates were very high (Figure 2). There is evidence of seasonality in birth rates, reaching an annual peak in mid-year (autumn/winter). Mortality rates in dogs under one year and older than two years were significantly higher than those of 1–2 year olds. Puppies under 4 months suffered particularly high mortality rates. There was no difference in mortality rate between years or between sexes. The mean estimate of vaccination coverage 12 months after simulating a starting vaccination coverage of 70% on 1st January 2012 was 46%. Repeating the simulation for 1st January 2013 resulted in a mean estimate of vaccination coverage of 54% on 1st January 2014.

Table 1. Demographic parameters from a population of owned dogs in Hluvukani, South Africa, 1st January 2012–1st January 2014

Quarter

Q1

Q2

Q3

Q4

Q5

Q6

Q7

Q8

Q9

Owned dogs

792

871

930

955

939

876

795

772

710

Dog-owning households

396

416

433

449

441

415

392

392

380

Sex

Male

450

495

533

549

557

522

483

470

442

Female

327

361

384

396

378

350

303

279

253

Unknown

15

15

13

10

4

4

9

23

15

Age

0–3 months

37

121

136

128

108

38

74

62

52

4–11 months

257

178

137

169

191

200

135

108

87

12–23 months

188

182

259

262

240

201

155

156

153

24–35 months

128

153

160

151

160

144

151

163

156

36 +

181

236

237

241

236

289

276

279

260

Unknown

1

1

1

4

4

4

4

4

2

Figure 1. Sex ratio (males per female dog) in a population of owned dogs in Hluvukani, South Africa, 1st January 2012–1st January 2014
Figure 1. Sex ratio (males per female dog) in a population of owned dogs in Hluvukani, South Africa, 1st January 2012–1st January 2014

 

Figure 2. Crude birth and death rates in a population of owned dogs in Hluvukani, South Africa, 1st January 2012–1st January 2014
Figure 2. Crude birth and death rates in a population of owned dogs in Hluvukani, South Africa, 1st January 2012–1st January 2014

 

This is a highly dynamic dog population, with rapid turnover and significant variability in demographic rates over time. Despite this, routinely achieving the WHO-recommended target vaccination coverage of 70% during mass dog vaccination campaigns conducted every 12 months will be sufficient to maintain coverage above the critical threshold of 40%, interrupting transmission of the disease and ultimately leading to its elimination from the population. The same conclusion was made in an independent study of two owned-dog populations in underserved urban communities in Gauteng Province, South Africa, where a similar methodology was applied.6 These studies demonstrate that health and demographic surveillance systems can be applied in populations of owned domestic dogs in Africa, to generate valuable data on the ecology of these populations, and to explore the implications for rabies control. Establishing a network of such sites, independently run but applying similar methodologies, would enable comparisons to be made and results to be generalised more broadly. Such a network will provide a reliable evidence base to help inform regional rabies control policies.

References

1.  Hampson K, Dushoff J, Cleaveland S, Haydon DT, Kaare M, Packer C, et al. Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biology. 2009;7(3):462–471.

2.  Butler JRA, Bingham J. Demography and dog-human relationships of the dog population in Zimbabwean communal lands. Veterinary Record. 2000;147(16):442–446.

3.  Kayali U, Mindekem R, Yemadji N, Vounatsou P, Kaninga Y, Ndoutamia AG, et al. Coverage of pilot parenteral vaccination campaign against canine rabies in N'Djamena, Chad. Bulletin of the World Health Organization. 2003;81(10):739–744.

4.  Gsell AS, Knobel DL, Kazwala RR, Vounatsou P, Zinsstag J. Domestic dog demographic structure and dynamics relevant to rabies control planning in urban areas in Africa: the case of Iringa, Tanzania. BMC Veterinary Research. 2012;8:1–10.

5.  Sankoh O, Byass P. The INDEPTH Network: filling vital gaps in global epidemiology. International Journal of Epidemiology. 2012;41(3):579–588.

6.  Morters MK, Restif O, Hampson K, Cleaveland S, Wood JLN, Conlan AJK. Evidence-based control of canine rabies: a critical review of population density reduction. Journal of Animal Ecology. 2013;82(1):6–14.

  

Speaker Information
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Darryn Knobel, BVSc, PhD
Department of Veterinary Tropical Diseases, Faculty of Veterinary Science
University of Pretoria
South Africa


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