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      Potential for sylvatic and urban Aedes mosquitoes from Senegal to transmit the new emerging dengue serotypes 1, 3 and 4 in West Africa

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          Abstract

          Dengue fever (DEN) is the most common arboviral disease in the world and dengue virus (DENV) causes 390 million annual infections around the world, of which 240 million are inapparent and 96 million are symptomatic. During the past decade a changing epidemiological pattern has been observed in Africa, with DEN outbreaks reported in all regions. In Senegal, all DENV serotypes have been reported. These important changes in the epidemiological profile of DEN are occurring in a context where there is no qualified vaccine against DEN. Further there is significant gap of knowledge on the vector bionomics and transmission dynamics in the African region to effectively prevent and control epidemics. Except for DENV-2, few studies have been performed with serotypes 1, 3, and 4, so this study was undertaken to fill out this gap. We assessed the vector competence of Aedes (Diceromyia) furcifer, Ae. (Diceromyia) taylori, Ae. (Stegomyia) luteocephalus, sylvatic and urban Ae. (Stegomyia) aegypti populations from Senegal for DENV-1, DENV-3 and DENV-4 using experimental oral infection. Whole bodies and wings/legs were tested for DENV presence by cell culture assays and saliva samples were tested by real time RT-PCR to estimate infection, disseminated infection and transmission rates. Our results revealed a low capacity of sylvatic and urban Aedes mosquitoes from Senegal to transmit DENV-1, DENV-3 and DENV-4 and an impact of infection on their mortality. The highest potential transmission rate was 20% despite the high susceptibility and disseminated infection rates up to 93.7% for the 3 Ae. aegypti populations tested, and 84.6% for the sylvatic vectors Ae. furcifer, Ae. taylori and Ae. luteocephalus.

          Author summary

          Dengue fever remains a major public health problem in all tropical regions of the world and causes 390 million infections each year. In Africa, while dengue outbreaks were rare during the last century, recurrent urban epidemic have been reported in all regions the last decade. Serotype 3, never reported in West Africa, caused major outbreaks in 2009 in several capital cities while serotype 2, usually confined to the forest cycle, spilled over into urban areas in Senegal and Mauritania in 2014–2015. These changes are occurring in a context where vector control remains the only effective approach to prevent and control epidemics. However, the design and the implementation of efficient vector control require an accurate knowledge of the vector bionomics and competence while such data are lacking in the African region. To fill out this gap we experimentally infected domestic and wild mosquitoes from Senegal to assess their vector competence for dengue serotypes 1, 3 and 4. Finally both domestic and wild Senegalese mosquitoes showed a low ability to transmit dengue viruses.

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          Most cited references43

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          Arthropod-borne viral infections of man in Nigeria, 1964-1970.

          During the years 1964 to 1970, 171 arboviruses of 15 different types were isolated from humans in Nigeria. Isolation rates were highest in 1969, and lowest in 1965 and 1967. Monthly arbovirus activity was highest in the rainy season months of June, July and August and lowest in the dry months of January and February. Viruses were isolated from all age groups, with the majority from children one to four years old. The viruses isolated in largest numbers were chikungunya and yellow fever, which caused epidemics in 1969, and dengue types 1 and 2 and Tataguine, which are endemic in Ibadan. Bwamba virus was isolated in 1964 and 1969, and Bunyamwera group viruses were encountered for the first time in 1969. Other viruses recovered less frequently were Zika, Igbo-Ora (an agent related to o'nyong-nyong), two viruses related to the Uganda mosquito virus Ug MP 359, Dugbe, Thogoto, Lebombo and Shuni. Several of these are new agents and have not previously been isolated from man. Clinical details are presented where available.
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            Evolutionary relationships of endemic/epidemic and sylvatic dengue viruses.

            Endemic/epidemic dengue viruses (DEN) that are transmitted among humans by the mosquito vectors Aedes aegypti and Aedes albopictus are hypothesized to have evolved from sylvatic DEN strains that are transmitted among nonhuman primates in West Africa and Malaysia by other Aedes mosquitoes. We tested this hypothesis with phylogenetic studies using envelope protein gene sequences of both endemic/epidemic and sylvatic strains. The basal position of sylvatic lineages of DEN-1, -2, and -4 suggested that the endemic/epidemic lineages of these three DEN serotypes evolved independently from sylvatic progenitors. Time estimates for evolution of the endemic/epidemic forms ranged from 100 to 1,500 years ago, and the evolution of endemic/epidemic forms represents relatively recent events in the history of DEN evolution. Analysis of envelope protein amino acid changes predicted to have accompanied endemic/epidemic emergence suggested a role for domain III in adaptation to new mosquito and/or human hosts.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Supervision
                Role: MethodologyRole: Writing – review & editing
                Role: Methodology
                Role: InvestigationRole: Writing – review & editing
                Role: Formal analysisRole: SoftwareRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Formal analysisRole: SoftwareRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                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
                13 February 2019
                February 2019
                : 13
                : 2
                : e0007043
                Affiliations
                [1 ] Unité d’Entomologie Médicale, Institut Pasteur de Dakar, Dakar, Senegal
                [2 ] Institute for Human Infections and Immunity, Center for Tropical Diseases and Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas
                [3 ] Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, Texas, United States of America
                [4 ] Epidemiological Infectious Disease Unit, Institut Pasteur de Dakar, Dakar, Senegal
                University of Florida, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-3683-8521
                Article
                PNTD-D-18-00852
                10.1371/journal.pntd.0007043
                6373929
                30759080
                023095ea-96ee-4bae-a3c6-cb9d0c39f371

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 29 May 2018
                : 2 December 2018
                Page count
                Figures: 4, Tables: 5, Pages: 16
                Funding
                This work was funded by National Institute of Health grants R24AI120942 and R01AI121452 and the Institut Pasteur de Dakar. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Medicine and Health Sciences
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                Disease Vectors
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                Infectious disease & Microbiology
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