The demography of free-roaming dog populations and applications to disease and population control

Understanding the demography of domestic dog populations is essential for effective disease control, particularly of canine-mediated rabies. Demographic data are also needed to plan effective population management. However, no study has comprehensively evaluated the contribution of demographic processes (i.e. births, deaths and movement) to variations in dog population size or density, or determined the factors that regulate these processes, including human factors. We report the results of a 3-year cohort study of domestic dogs, which is the first to generate detailed data on the temporal variation of these demographic characteristics. The study was undertaken in two communities in each of Bali, Indonesia and Johannesburg, South Africa, in rabies-endemic areas and where the majority of dogs were free-roaming. None of the four communities had been engaged in any dog population management interventions by local authorities or animal welfare organizations. All identified dogs in the four communities were monitored individually throughout the study. We observed either no population growth or a progressive decline in population size during the study period. There was no clear evidence that population size was regulated through environmental resource constraints. Rather, almost all of the identified dogs were owned and fed regularly by their owners, consistent with population size regulated by human demand. Finally, a substantial fraction of the dogs originated from outside the population, entirely through the translocation of dogs by people, rather than from local births. These findings demonstrate that previously reported growth of dog populations is not a general phenomenon and challenge the widely held view that free-roaming dogs are unowned and form closed populations. Synthesis and applications. These observations have broad implications for disease and population control. The accessibility of dogs for vaccination and evaluation through owners and the movement of dogs (some of them infected) by people will determine the viable options for disease control strategies. The impact of human factors on population dynamics will also influence the feasibility of annual vaccination campaigns to control rabies and population control through culling or sterilization. The complex relationship between dogs and people is critically important in the transmission and control of canine-mediated rabies. For effective management, human factors must be considered in the development of disease and population control programmes

Achieving population-level immunity to rabies in free-roaming dogs in Africa and Asia.

Canine rabies can be effectively controlled by vaccination with readily available, high-quality vaccines. These vaccines should provide protection from challenge in healthy dogs, for the claimed period, for duration of immunity, which is often two or three years. It has been suggested that, in free-roaming dog populations where rabies is endemic, vaccine-induced protection may be compromised by immuno-suppression through malnutrition, infection and other stressors. This may reduce the proportion of dogs that seroconvert to the vaccine during vaccination campaigns and the duration of immunity of those dogs that seroconvert. Vaccination coverage may also be limited through insufficient vaccine delivery during vaccination campaigns and the loss of vaccinated individuals from populations through demographic processes. This is the first longitudinal study to evaluate temporal variations in rabies vaccine-induced serological responses, and factors associated with these variations, at the individual level in previously unvaccinated free-roaming dog populations. Individual-level serological and health-based data were collected from three cohorts of dogs in regions where rabies is endemic, one in South Africa and two in Indonesia. We found that the vast majority of dogs seroconverted to the vaccine; however, there was considerable variation in titres, partly attributable to illness and lactation at the time of vaccination. Furthermore, >70% of the dogs were vaccinated through community engagement and door-to-door vaccine delivery, even in Indonesia where the majority of the dogs needed to be caught by net on successive occasions for repeat blood sampling and vaccination. This demonstrates the feasibility of achieving population-level immunity in free-roaming dog populations in rabies-endemic regions. However, attrition of immune individuals through demographic processes and waning immunity necessitates repeat vaccination of populations within at least two years to ensure communities are protected from rabies. These findings support annual mass vaccination campaigns as the most effective means to control canine rabies.This study was funded by the International Fund for Animal Welfare (IFAW) http://www.ifaw.org/united-kingdom and the World Society for the Protection of Animals (WSPA) http://www.wspa.org.uk/, with support from the Charles Slater Fund and Jowett Fund. OR is supported by the Royal Society, and JLNW the Alborada Trust. JLNW, OR and ARF receive support from the Research and Policy for Infectious Disease Dynamics Program of the Science and Technology Directorate, Department of Homeland Security, Fogarty International Centre, National Institute of Health. DLH and ARF are supported by the U.K. Department for the Environment, Food and Rural Affairs project number SEV3500. TJM is supported by Biotechnology and Biological Sciences Research Council grant number BB/I012192/1.This is the final version. It was first published by PLOS in PLOS Neglected Tropical Diseases at http://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0003160

Achieving population-level immunity to rabies in free-roaming dogs in Africa and Asia

Published onlineJournal ArticleResearch Support, Non-U.S. Gov'tCanine rabies can be effectively controlled by vaccination with readily available, high-quality vaccines. These vaccines should provide protection from challenge in healthy dogs, for the claimed period, for duration of immunity, which is often two or three years. It has been suggested that, in free-roaming dog populations where rabies is endemic, vaccine-induced protection may be compromised by immuno-suppression through malnutrition, infection and other stressors. This may reduce the proportion of dogs that seroconvert to the vaccine during vaccination campaigns and the duration of immunity of those dogs that seroconvert. Vaccination coverage may also be limited through insufficient vaccine delivery during vaccination campaigns and the loss of vaccinated individuals from populations through demographic processes. This is the first longitudinal study to evaluate temporal variations in rabies vaccine-induced serological responses, and factors associated with these variations, at the individual level in previously unvaccinated free-roaming dog populations. Individual-level serological and health-based data were collected from three cohorts of dogs in regions where rabies is endemic, one in South Africa and two in Indonesia. We found that the vast majority of dogs seroconverted to the vaccine; however, there was considerable variation in titres, partly attributable to illness and lactation at the time of vaccination. Furthermore, >70% of the dogs were vaccinated through community engagement and door-to-door vaccine delivery, even in Indonesia where the majority of the dogs needed to be caught by net on successive occasions for repeat blood sampling and vaccination. This demonstrates the feasibility of achieving population-level immunity in free-roaming dog populations in rabies-endemic regions. However, attrition of immune individuals through demographic processes and waning immunity necessitates repeat vaccination of populations within at least two years to ensure communities are protected from rabies. These findings support annual mass vaccination campaigns as the most effective means to control canine rabies.This study was funded by the International Fund for Animal Welfare (IFAW) http://www.ifaw.org/united-kingdom and the World Society for the Protection of Animals (WSPA) http://www.wspa.org.uk/, with support from the Charles Slater Fund and Jowett Fund. OR is supported by the Royal Society, and JLNW the Alborada Trust. JLNW, OR and ARF receive support from the Research and Policy for Infectious Disease Dynamics Program of the Science and Technology Directorate, Department of Homeland Security, Fogarty International Centre, National Institute of Health. DLH and ARF are supported by the U.K. Department for the Environment, Food and Rural Affairs project number SEV3500. TJM is supported by Biotechnology and Biological Sciences Research Council grant number BB/I012192/1. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Declines in titre in the Zenzele research cohort.

<p>Titres of all the dogs (n = 82) in the Zenzele research cohort that were blood sampled all at four time points (30, 90, 180 and 360 days after vaccination). Upper outliers (i.e. the dogs with day 30 titres ≥128 IU/ml) are excluded. Titres in IU/ml are shown on the log scale. The geometric mean titre is shown in red.</p

Variations in titre in the Antiga research cohort.

<p>Titres of all the dogs in the Antiga research cohort. Upper outliers (i.e. the fifteen dogs with day 180 titres of 11.3 IU/ml) are excluded. The median titre (thick, horizontal line), 25th and 75th percentiles (thin horizontal lines), and either minimum and maximum titres or 1.5× the interquartile range (dashed vertical lines) are shown for each time point after vaccination (at day 180 and 360).</p

The number of dogs in the research cohorts and the number of unvaccinated controls in Bali that were blood sampled at each time point (this table is reproduced with additional information in the Supporting Information Table S3).

<p>*day 0 immediately prior to vaccination for the research cohort.</p><p>The number of dogs in the research cohorts and the number of unvaccinated controls in Bali that were blood sampled at each time point (this table is reproduced with additional information in the Supporting Information <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003160#pntd.0003160.s004" target="_blank">Table S3</a>).</p

Variations in titre in the Zenzele research cohort.

<p>Titres of all the dogs in the Zenzele research cohort. Upper outliers (i.e. the seven dogs with day 30 titres ≥128 IU/ml) are excluded. The median titre (thick, horizontal line), 25th and 75th percentiles (thin horizontal lines), and either minimum and maximum titres or 1.5× the interquartile range (dashed vertical lines) are shown for each time point after vaccination (at day 30, 90, 180 and 360). Day 0 shows the distribution of titres immediately prior to vaccination.</p

Variations in titre in the Kelusa research cohort.

<p>Titres of all the dogs in the Kelusa research cohort. Upper outliers (i.e. the four dogs with day 180 titres of 11.3 IU/ml) are excluded. The median titre (thick, horizontal line), 25th and 75th percentiles (thin horizontal lines), and either minimum and maximum titres or 1.5× the interquartile range (dashed vertical lines) are shown for each time point after vaccination (at day 180 and 360).</p