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      Model-Based Investigations of Different Vector-Related Intervention Strategies to Eliminate Visceral Leishmaniasis on the Indian Subcontinent

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          Abstract

          The elimination of infectious diseases requires reducing transmission below a certain threshold. The Visceral Leishmaniasis (VL) Elimination Initiative in Southeast Asia aims to reduce the annual VL incidence rate below 1 case per 10,000 inhabitants in endemic areas by 2015 via a combination of case management and vector control. Using a previously developed VL transmission model, we investigated transmission thresholds dependent on measures reducing the sand fly density either by killing sand flies (e.g., indoor residual spraying and long-lasting insecticidal nets) or by destroying breeding sites (e.g., environmental management).

          Model simulations suggest that elimination of VL is possible if the sand fly density can be reduced by 67% through killing sand flies, or if the number of breeding sites can be reduced by more than 79% through measures of environmental management.

          These results were compared to data from two recent cluster randomised controlled trials conducted in India, Nepal and Bangladesh showing a 72% reduction in sand fly density after indoor residual spraying, a 44% and 25% reduction through the use of long-lasting insecticidal nets and a 42% reduction after environmental management.

          Based on model predictions, we identified the parameters within the transmission cycle of VL that predominantly determine the prospects of intervention success. We suggest further research to refine model-based predictions into the elimination of VL.

          Author Summary

          Visceral leishmaniasis is suspected to be the second largest parasitic killer in the world after malaria. On the Indian subcontinent, the vector-borne disease is caused by the protozoan flagellate Leishmania donovani and transmitted by the sand fly Phlebotomus argentipes. The regional elimination programme has suggested as a target line to reduce the annual incidence below 1 case in 10,000 by 2015. Using a previously developed mathematical model, we investigated to what extent the sand fly population must be controlled to achieve elimination. These calculated thresholds were compared to data from two recent trials conducted in India, Nepal and Bangladesh to evaluate the efficacy of different vector control measures. Our results indicate that elimination should be feasible because the evaluated effect of indoor residual spraying exceeds the threshold. However, emerging insecticide resistance may compromise the effectiveness of this measure. The observed effects of long lasting insecticidal nets and environmental management do not seem to be sufficient to reach either threshold. Integrated vector management based on indoor residual spraying combined with long lasting insecticidal nets and more effective environmental management may allow overcoming the limitations of the current vector control methods and should also prevent re-emergence of the infection after local extinction.

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          Most cited references48

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          Visceral leishmaniasis: what are the needs for diagnosis, treatment and control?

          Visceral leishmaniasis (VL) is a systemic protozoan disease that is transmitted by phlebotomine sandflies. Poor and neglected populations in East Africa and the Indian sub-continent are particularly affected. Early and accurate diagnosis and treatment remain key components of VL control. In addition to improved diagnostic tests, accurate and simple tests are needed to identify treatment failures. Miltefosine, paromomycin and liposomal amphotericin B are gradually replacing pentavalent antimonials and conventional amphotericin B as the preferred treatments in some regions, but in other areas these drugs are still being evaluated in both mono- and combination therapies. New diagnostic tools and new treatment strategies will only have an impact if they are made widely available to patients.
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            Post-kala-azar dermal leishmaniasis.

            Post-kala-azar dermal leishmaniasis (PKDL) is a complication of visceral leishmaniasis (VL); it is characterised by a macular, maculopapular, and nodular rash in a patient who has recovered from VL and who is otherwise well. The rash usually starts around the mouth from where it spreads to other parts of the body depending on severity. It is mainly seen in Sudan and India where it follows treated VL in 50% and 5-10% of cases, respectively. Thus, it is largely restricted to areas where Leishmania donovani is the causative parasite. The interval at which PKDL follows VL is 0-6 months in Sudan and 2-3 years in India. PKDL probably has an important role in interepidemic periods of VL, acting as a reservoir for parasites. There is increasing evidence that the pathogenesis is largely immunologically mediated; high concentrations of interleukin 10 in the peripheral blood of VL patients predict the development of PKDL. During VL, interferon gamma is not produced by peripheral blood mononuclear cells (PBMC). After treatment of VL, PBMC start producing interferon gamma, which coincides with the appearance of PKDL lesions due to interferon-gamma-producing cells causing skin inflammation as a reaction to persisting parasites in the skin. Diagnosis is mainly clinical, but parasites can be seen by microscopy in smears with limited sensitivity. PCR and monoclonal antibodies may detect parasites in more than 80% of cases. Serological tests and the leishmanin skin test are of limited value. Treatment is always needed in Indian PKDL; in Sudan most cases will self cure but severe and chronic cases are treated. Sodium stibogluconate is given at 20 mg/kg for 2 months in Sudan and for 4 months in India. Liposomal amphotericine B seems effective; newer compounds such as miltefosine that can be administered orally or topically are of major potential interest. Although research has brought many new insights in pathogenesis and management of PKDL, several issues in particular in relation to control remain unsolved and deserve urgent attention.
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              Mosquito behavior and vector control.

              Effective indoor residual spraying against malaria vectors depends on whether mosquitoes rest indoors (i.e., endophilic behavior). This varies among species and is affected by insecticidal irritancy. Exophilic behavior has evolved in certain populations exposed to prolonged spraying programs. Optimum effectiveness of insecticide-treated nets presumably depends on vectors biting at hours when most people are in bed. Time of biting varies among different malaria vector species, but so far there is inconclusive evidence for these evolving so as to avoid bednets. Use of an untreated net diverts extra biting to someone in the same room who is without a net. Understanding choice of oviposition sites and dispersal behavior is important for the design of successful larval control programs including those using predatory mosquito larvae. Prospects for genetic control by sterile males or genes rendering mosquitoes harmless to humans will depend on competitive mating behavior. These methods are hampered by the immigration of monogamous, already-mated females.
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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
                April 2014
                24 April 2014
                : 8
                : 4
                : e2810
                Affiliations
                [1 ]Department of Clinical Epidemiology and Applied Biometry, University of Tübingen, Tübingen, Germany
                [2 ]Numerus Limited, Tübingen, Germany
                [3 ]Barcelona Centre for International Health Research (CRESIB, Hospital Clínic-Universitat de Barcelona), Barcelona, Spain
                [4 ]Department of Public Health, Institute of Tropical Medicine, Antwerp, Belgium
                [5 ]Department of Medicine, Institute of Medical Sciences, Banaras Hindu University, Varanasi, India
                [6 ]Department of Medicine, BP Koirala Institute of Health Sciences, Dharan, Nepal
                [7 ]Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
                [8 ]Laboratory of Microbiology, Parasitology and Hygiene, University of Antwerp, Antwerp, Belgium
                Oswaldo Cruz Foundation, Brazil
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AS HPD ME. Performed the experiments: AS. Analyzed the data: AS HPD. Contributed reagents/materials/analysis tools: AP BO SS SR MB JCD. Wrote the paper: AS HPD ME.

                Article
                PNTD-D-13-01436
                10.1371/journal.pntd.0002810
                3998939
                24762676
                339b1a4c-f995-44db-9866-7747411b3c9d
                Copyright @ 2014

                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
                : 20 September 2013
                : 10 March 2014
                Page count
                Pages: 9
                Funding
                This investigation was funded by the EU project KalaDrug-R (EC-FP7-222895). The data used to validate the model were generated within the KALANET project funded by the European Union under its 6th Framework Program (INCODEV/Project 015374). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Population Biology
                Medicine and Health Sciences
                Epidemiology
                Infectious Disease Epidemiology
                Physical Sciences
                Mathematics
                Applied Mathematics

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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