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      Transmission Dynamics and Prospects for the Elimination of Canine Rabies

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          Abstract

          Rabies has been eliminated from domestic dog populations in Western Europe and North America, but continues to kill many thousands of people throughout Africa and Asia every year. A quantitative understanding of transmission dynamics in domestic dog populations provides critical information to assess whether global elimination of canine rabies is possible. We report extensive observations of individual rabid animals in Tanzania and generate a uniquely detailed analysis of transmission biology, which explains important epidemiological features, including the level of variation in epidemic trajectories. We found that the basic reproductive number for rabies, R 0, is very low in our study area in rural Africa (∼1.2) and throughout its historic global range (<2). This finding provides strong support for the feasibility of controlling endemic canine rabies by vaccination, even near wildlife areas with large wild carnivore populations. However, we show that rapid turnover of domestic dog populations has been a major obstacle to successful control in developing countries, thus regular pulse vaccinations will be required to maintain population-level immunity between campaigns. Nonetheless our analyses suggest that with sustained, international commitment, global elimination of rabies from domestic dog populations, the most dangerous vector to humans, is a realistic goal.

          Author Summary

          Canine rabies has been successfully eliminated from Western Europe and North America, but in the developing world, someone dies every ten minutes from this horrific disease, which is primarily spread by domestic dogs. A quantitative understanding of rabies transmission dynamics in domestic dog populations is crucial to determining whether global elimination can be achieved. The unique pathology of rabies allowed us to trace case-to-case transmission directly, during a rabies outbreak in northern Tanzania. From these unusual data, we generated a detailed analysis of rabies transmission biology and found evidence for surprisingly low levels of transmission. We also analysed outbreak data from around the world and found that the transmission of canine rabies has been inherently low throughout its global historic range, explaining the success of control efforts in developed countries. However, we show that when birth and death rates in domestic dog populations are high, such as in our study populations in Tanzania, it is more difficult to maintain population-level immunity in between vaccination campaigns. Nonetheless, we conclude that, although the level of vaccination coverage required is higher than would be predicted from naïve transmission models, global elimination of canine rabies can be achieved through appropriately designed, sustained domestic dog vaccination campaigns.

          Abstract

          Low transmission rates in rural Africa and elsewhere suggest that sustained, appropriately designed domestic dog vaccination campaigns could lead to global elimination of canine rabies, which would save over 50,000 human lives per year.

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          Most cited references72

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          Re-evaluating the burden of rabies in Africa and Asia.

          To quantify the public health and economic burden of endemic canine rabies in Africa and Asia. Data from these regions were applied to a set of linked epidemiological and economic models. The human population at risk from endemic canine rabies was predicted using data on dog density, and human rabies deaths were estimated using a series of probability steps to determine the likelihood of clinical rabies developing in a person after being bitten by a dog suspected of having rabies. Model outputs on mortality and morbidity associated with rabies were used to calculate an improved disability-adjusted life year (DALY) score for the disease. The total societal cost incurred by the disease is presented. Human mortality from endemic canine rabies was estimated to be 55 000 deaths per year (90% confidence interval (CI) = 24 000-93 000). Deaths due to rabies are responsible for 1.74 million DALYs lost each year (90% CI = 0.75-2.93). An additional 0.04 million DALYs are lost through morbidity and mortality following side-effects of nerve-tissue vaccines. The estimated annual cost of rabies is USD 583.5 million (90% CI = USD 540.1-626.3 million). Patient-borne costs for post-exposure treatment form the bulk of expenditure, accounting for nearly half the total costs of rabies. Rabies remains an important yet neglected disease in Africa and Asia. Disparities in the affordability and accessibility of post-exposure treatment and risks of exposure to rabid dogs result in a skewed distribution of the disease burden across society, with the major impact falling on those living in poor rural communities, in particular children.
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            Heterogeneities in the transmission of infectious agents: implications for the design of control programs.

            From an analysis of the distributions of measures of transmission rates among hosts, we identify an empirical relationship suggesting that, typically, 20% of the host population contributes at least 80% of the net transmission potential, as measured by the basic reproduction number, R0. This is an example of a statistical pattern known as the 20/80 rule. The rule applies to a variety of disease systems, including vector-borne parasites and sexually transmitted pathogens. The rule implies that control programs targeted at the "core" 20% group are potentially highly effective and, conversely, that programs that fail to reach all of this group will be much less effective than expected in reducing levels of infection in the population as a whole.
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              Heterogeneities in the transmission of infectious agents: Implications for the design of control programs

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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                plbi
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                March 2009
                10 March 2009
                : 7
                : 3
                : e1000053
                Affiliations
                [1 ] Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America
                [2 ] Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, United Kingdom
                [3 ] Department of Biology, McMaster University, Hamilton, Ontario, Canada
                [4 ] The Roslin Institute/ Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Roslin, Midlothian, United Kingdom
                [5 ] Boyd Orr Centre for Population and Ecosystem Health, University of Glasgow, Glasgow, United Kingdom
                [6 ] Centre for Infectious Diseases, School of Biological Sciences, University of Edinburgh, Edinburgh, Midlothian, United Kingdom
                [7 ] Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, Minnesota, United States of America
                Centers for Disease Control and Prevention, United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: K.Hampson@ 123456Shef.ac.uk
                Article
                08-PLBI-RA-2505R2 plbi-07-03-10
                10.1371/journal.pbio.1000053
                2653555
                19278295
                26aa931a-fadb-4876-9942-5064074ad2a8
                Copyright: © 2009 Hampson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 23 June 2008
                : 21 January 2009
                Page count
                Pages: 10
                Categories
                Research Article
                Ecology
                Infectious Diseases
                Public Health and Epidemiology
                Custom metadata
                Hampson K, Dushoff J, Cleaveland S, Haydon DT, Kaare M, et al. (2009) Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biol 7(3): e1000053. doi: 10.1371/journal.pbio.1000053

                Life sciences
                Life sciences

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