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      Risk Factors for the Presence of Chikungunya and Dengue Vectors ( Aedes aegypti and Aedes albopictus), Their Altitudinal Distribution and Climatic Determinants of Their Abundance in Central Nepal

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          Abstract

          Background

          The presence of the recently introduced primary dengue virus vector mosquito Aedes aegypti in Nepal, in association with the likely indigenous secondary vector Aedes albopictus, raises public health concerns. Chikungunya fever cases have also been reported in Nepal, and the virus causing this disease is also transmitted by these mosquito species. Here we report the results of a study on the risk factors for the presence of chikungunya and dengue virus vectors, their elevational ceiling of distribution, and climatic determinants of their abundance in central Nepal.

          Methodology/Principal Findings

          We collected immature stages of mosquitoes during six monthly cross-sectional surveys covering six administrative districts along an altitudinal transect in central Nepal that extended from Birgunj (80 m above sea level [asl]) to Dhunche (highest altitude sampled: 2,100 m asl). The dengue vectors Ae. aegypti and Ae. albopictus were commonly found up to 1,350 m asl in Kathmandu valley and were present but rarely found from 1,750 to 2,100 m asl in Dhunche. The lymphatic filariasis vector Culex quinquefasciatus was commonly found throughout the study transect. Physiographic region, month of collection, collection station and container type were significant predictors of the occurrence and co-occurrence of Ae. aegypti and Ae. albopictus. The climatic variables rainfall, temperature, and relative humidity were significant predictors of chikungunya and dengue virus vectors abundance.

          Conclusions/Significance

          We conclude that chikungunya and dengue virus vectors have already established their populations up to the High Mountain region of Nepal and that this may be attributed to the environmental and climate change that has been observed over the decades in Nepal. The rapid expansion of the distribution of these important disease vectors in the High Mountain region, previously considered to be non-endemic for dengue and chikungunya fever, calls for urgent actions to protect the health of local people and tourists travelling in the central Himalayas.

          Author Summary

          The local transmission of dengue fever was confirmed in five lowland urban areas in 2006, along with the first report of the primary vectors of dengue virus, Aedes aegypti mosquitoes. Subsequent studies revealed a wide distribution of Ae. aegypti in 2009, and the first locally acquired dengue fever case in Kathmandu, the capital city of Nepal, during an epidemic in 2010. These records of a rapid expansion of dengue viruses and their primary vector, Ae. aegypti, in the Middle Mountain region and the more pronounced warming of mountains prompted us to investigate the altitudinal distribution and determinants of the abundance of dengue virus vectors in central Nepal. The first local transmission of chikungunya virus was recently reported from central Nepal in 2013. In this study, we document the distribution of Ae. aegypti and the secondary vector of dengue viruses, Aedes albopictus, from the lowlands (80 m) up to 2,100 m altitude in Dhunche, Rasuwa district. The climatic variables rainfall, temperature and relative humidity were significant predictors of their abundances. The distribution extension of these important disease vectors in the High Mountain region calls for urgent actions to protect the health of local people and tourists travelling in the central Himalayas.

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          Most cited references57

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          Critical review of the vector status of Aedes albopictus.

          N G Gratz (2004)
          The mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), originally indigenous to South-east Asia, islands of the Western Pacific and Indian Ocean, has spread during recent decades to Africa, the mid-east, Europe and the Americas (north and south) after extending its range eastwards across Pacific islands during the early 20th century. The majority of introductions are apparently due to transportation of dormant eggs in tyres. Among public health authorities in the newly infested countries and those threatened with the introduction, there has been much concern that Ae. albopictus would lead to serious outbreaks of arbovirus diseases (Ae. albopictus is a competent vector for at least 22 arboviruses), notably dengue (all four serotypes) more commonly transmitted by Aedes (Stegomyia) aegypti (L.). Results of many laboratory studies have shown that many arboviruses are readily transmitted by Ae. albopictus to laboratory animals and birds, and have frequently been isolated from wild-caught mosquitoes of this species, particularly in the Americas. As Ae. albopictus continues to spread, displacing Ae. aegypti in some areas, and is anthropophilic throughout its range, it is important to review the literature and attempt to predict whether the medical risks are as great as have been expressed in scientific journals and the popular press. Examination of the extensive literature indicates that Ae. albopictus probably serves as a maintenance vector of dengue in rural areas of dengue-endemic countries of South-east Asia and Pacific islands. Also Ae. albopictus transmits dog heartworm Dirofilaria immitis (Leidy) (Spirurida: Onchocercidae) in South-east Asia, south-eastern U.S.A. and both D. immitis and Dirofilaria repens (Raillet & Henry) in Italy. Despite the frequent isolation of dengue viruses from wild-caught mosquitoes, there is no evidence that Ae. albopictus is an important urban vector of dengue, except in a limited number of countries where Ae. aegypti is absent, i.e. parts of China, the Seychelles, historically in Japan and most recently in Hawaii. Further research is needed on the dynamics of the interaction between Ae. albopictus and other Stegomyia species. Surveillance must also be maintained on the vectorial role of Ae. albopictus in countries endemic for dengue and other arboviruses (e.g. Chikungunya, EEE, Ross River, WNV, LaCrosse and other California group viruses), for which it would be competent and ecologically suited to serve as a bridge vector.
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            Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti.

            Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vector-pathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20 °C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10 °C) or constant temperature. A thermodynamic model predicted that at mean temperatures 18 °C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.
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              Global Spread and Persistence of Dengue

              Dengue is a spectrum of disease caused by four serotypes of the most prevalent arthropod-borne virus affecting humans today, and its incidence has increased dramatically in the past 50 years. Due in part to population growth and uncontrolled urbanization in tropical and subtropical countries, breeding sites for the mosquitoes that transmit dengue virus have proliferated, and successful vector control has proven problematic. Dengue viruses have evolved rapidly as they have spread worldwide, and genotypes associated with increased virulence have expanded from South and Southeast Asia into the Pacific and the Americas. This review explores the human, mosquito, and viral factors that contribute to the global spread and persistence of dengue, as well as the interaction between the three spheres, in the context of ecological and climate changes. What is known, as well as gaps in knowledge, is emphasized in light of future prospects for control and prevention of this pandemic disease.
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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, CA USA )
                1935-2727
                1935-2735
                16 March 2015
                March 2015
                : 9
                : 3
                : e0003545
                Affiliations
                [1 ]Nepal Health Research Council (NHRC), Ministry of Health and Population Complex, Kathmandu, Nepal
                [2 ]Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main, Germany
                [3 ]Institute for Atmospheric and Environmental Sciences (IAU), Goethe University, Frankfurt am Main, Germany
                [4 ]Institute of Occupational Medicine, Social Medicine and Environmental Medicine, Goethe University, Frankfurt am Main, Germany
                [5 ]Natural History Museum, Tribhuvan University, Swayambhu, Kathmandu, Nepal
                United States Army Medical Research Institute of Infectious Diseases, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: MD UK IG. Performed the experiments: MD IG. Analyzed the data: MD RBO BA. Contributed reagents/materials/analysis tools: MD UK. Wrote the paper: MD IG UK RBO BA. Coordinated field study and performed data management: HDJ.

                Article
                PNTD-D-14-01775
                10.1371/journal.pntd.0003545
                4361564
                25774518
                4e92c409-e395-4f23-8ce5-e2251a71b414
                Copyright @ 2015

                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
                : 9 October 2014
                : 16 January 2015
                Page count
                Figures: 3, Tables: 5, Pages: 20
                Funding
                This research was performed as a part of the collaborative research project “A longitudinal study on Aedes mosquitoes and climate change along an altitudinal transect in central Nepal” by the Nepal Health Research Council (NHRC) and the Biodiversity and Climate Research Centre (BiK-F). It was financially supported by the Government of Nepal, a DAAD PhD scholarship to MD and the research funding programme “LOEWE—Landes-Offensive zur Entwicklung wissenschaftlich-ökonomischer Exzellenz” of the Ministry of Higher Education, Research and the Arts of the State of Hesse, Germany. The funding bodies had no role in the study design, data collection, data analysis, interpretation of results, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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