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      Culling Dogs in Scenarios of Imperfect Control: Realistic Impact on the Prevalence of Canine Visceral Leishmaniasis

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          Abstract

          Background

          Visceral leishmaniasis belongs to the list of neglected tropical diseases and is considered a public health problem worldwide. Spatial correlation between the occurrence of the disease in humans and high rates of canine infection suggests that in the presence of the vector, canine visceral leishmaniasis is the key factor for triggering transmission to humans. Despite the control strategies implemented, such as the sacrifice of infected dogs being put down, the incidence of American visceral leishmaniasis remains high in many Latin American countries.

          Methodology/Principal Findings

          Mathematical models were developed to describe the transmission dynamics of canine leishmaniasis and its control by culling. Using these models, imperfect control scenarios were implemented to verify the possible factors which alter the effectiveness of controlling this disease in practice.

          Conclusions/Significance

          A long-term continuous program targeting both asymptomatic and symptomatic dogs should be effective in controlling canine leishmaniasis in areas of low to moderate transmission (R 0 up to 1.4). However, the indiscriminate sacrifice of asymptomatic dogs with positive diagnosis may jeopardize the effectiveness of the control program, if tests with low specificity are used, increasing the chance of generating outrage in the population, and leading to lower adherence to the program. Therefore, culling must be planned accurately and implemented responsibly and never as a mechanical measure in large scale. In areas with higher transmission, culling alone is not an effective control strategy.

          Author Summary

          Visceral leishmaniasis is listed as a neglected tropical disease and is considered a public health problem worldwide. The disease has been documented since 1885, the first case being reported in India. After over 120 years, the incidence of the disease remains high despite control strategies implemented. In areas where the disease is zoonotic, such as in Brazil, identification as well as removal of infected dogs is recommended in highly endemic areas for they are considered to be the reservoir of the Leishmania chagasi parasite. The theoretical basis that supports the culling of infected dogs is the assumption that the incidence of human infection is directly related to the number of infectious dogs. However, there is no consensus among researchers on the effectiveness of this strategy for controlling either human or canine visceral leishmaniasis. In this context, mathematical models can provide a basis for determining the strategies with the greatest potential for success. This paper aims to contribute to this discussion by introducing further complexities into the problem, in particular, the imperfect diagnosis of this infection and the time gap between laboratory diagnosis and culling and the presence of asymptomatic infections.

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          Most cited references12

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          The logic of visceral leishmaniasis control.

          C. Dye (1996)
          Mathematical models are used to compare the effectiveness of various untested, unused, and undeveloped methods for controlling canine and human zoonotic visceral leishmaniasis (ZVL), including insecticides, vaccines, killing serologically positive and sick dogs, and drugs. For given percentage changes in control parameters, insecticides are the most effective control method. Where transmission occurs peridomestically and vectors are accessible to treatment, as in parts of tropical America, insecticides are expected to reduce the incidence of human ZVL even more effectively than they reduce the prevalence of canine leishmaniasis, a result that should encourage properly designed vector control trials. The second best strategy is to reduce susceptibility to leishmaniasis by vaccinating people or dogs, or by eliminating childhood malnutrition where it is common. Both killing vectors and reducing susceptibility (by whatever means) are more effective than killing dogs or treating them with drugs. In Europe, where vector control is less likely to be successful and canine leishmaniasis is a major veterinary problem, a dog vaccine is highly desirable. Better drugs for dogs will help case management but, with regard to bringing down the incidence in the dog population, immunization is the ultimate goal.
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            Impact of canine control on the epidemiology of canine and human visceral leishmaniasis in Brazil.

            Brazil is the only country endemic for zoonotic visceral leishmaniasis (ZVL) that regularly conducts epidemiologic and prophylactic control programs that involve the treatment of human cases, insect vector control, and the removal of seropositive infected dogs. This report reviews 60 studies reporting data on the efficacy of these recommended control tools and concludes that in Brazil 1) eradication of the disease in Minas Gerais was achieved by the concomitant use of the three control methods, 2) although seropositivity by an immunofluorescent assay is not completely related to infectiousness, the removal of seropositive dogs leads to a significant reduction of canine and human incidence, 3) improvement of the sensitivity of the diagnostic tool used for canine control should optimize the efficacy of control, and 4) although difficult and expensive, the public health dog control campaigns performed in Brazil reduced the incidence of ZVL and should be maintained since treatment of dogs is an unrealistic intervention, both because of its prohibitive cost and relatively poor effectiveness.
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              Effect of eliminating seropositive canines on the transmission of visceral leishmaniasis in Brazil.

              In Brazil, where Leishmania chagasi causes endemic American visceral leishmaniasis (AVL), the spread and maintenance of human disease are attributed to canine reservoirs. However, despite measures directed toward the elimination of infected canines, the incidence of human disease continues to increase. To evaluate the role of infected canines in the acquisition of AVL by humans, we undertook a controlled intervention study in three similar, but isolated, valleys of Pancas, Espírito Santo, Brazil. In the two experimental (intervention) valleys, infected dogs were eliminated whereas in the control valley, seropositive canines remained untouched. During the 12-month study period, human seropositivity rates, as measured by dot enzyme-linked immunosorbent assay, increased from 15% to 54% in the intervention valleys and from 14% to 54% in the control valley. The elimination of infected canines in the intervention valleys did not result in a statistically significant difference between the incidences of human serological conversion in the intervention and control valleys at either 6 (20% and 22%, respectively; P = .5961) or 12 months (26% and 27%, respectively; P = .9442). The role of humans as a significant reservoir for AVL is proposed as an explanation for the study results.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                August 2013
                8 August 2013
                : 7
                : 8
                : e2355
                Affiliations
                [1 ]Program for Scientific Computing, Oswaldo Cruz Foundation (Fiocruz), Rio de Janeiro, Brazil
                [2 ]School of Applied Mathematics (EMAP) of the Getulio Vargas Foundation (FGV), Rio de Janeiro, Brazil
                [3 ]Department of Epidemiology, Social Medicine Institute, State University of Rio de Janeiro (UERJ), Rio de Janeiro, Brazil
                University of Pittsburgh, United States of America
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DNCCC CTC MAS. Performed the experiments: DNCCC CTC MAS. Analyzed the data: DNCCC CTC GLW. Contributed reagents/materials/analysis tools: DNCCC CTC MAS. Wrote the paper: DNCCC CTC.

                Article
                PNTD-D-12-01302
                10.1371/journal.pntd.0002355
                3738479
                23951375
                863d0682-4f8a-4a53-b953-8ef6990e0616
                Copyright @ 2013

                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
                : 3 October 2012
                : 21 June 2013
                Page count
                Pages: 8
                Funding
                This work was partially supported by the National School of Public Health (ENSP)/Oswaldo Cruz Foundation (FIOCRUZ), FAPERJ and CNPq (GLW: Process – 306267/2010-1). CTC holds a scholarship from CNPq. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Population Modeling
                Infectious Disease Modeling
                Population Biology
                Epidemiology
                Infectious Disease Epidemiology
                Population Dynamics
                Disease Dynamics
                Population Modeling

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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