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      Zika virus threshold determines transmission by European Aedes albopictus mosquitoes

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          ABSTRACT

          Since its emergence in Yap Island in 2007, Zika virus (ZIKV) has affected all continents except Europe. Despite the hundreds of cases imported to European countries from ZIKV-infested regions, no local cases have been reported in localities where the ZIKV-competent mosquito Aedes albopictus is well established. Here we analysed the vector competence of European Aedes ( aegypti and albopictus) mosquitoes to different genotypes of ZIKV. We demonstrate that Ae. albopictus from France was less susceptible to the Asian ZIKV than to the African ZIKV. Critically we show that effective crossing of anatomical barriers (midgut and salivary glands) after an infectious blood meal depends on a viral load threshold to trigger: (i) viral dissemination from the midgut to infect mosquito internal organs and (ii) viral transmission from the saliva to infect a vertebrate host. A viral load in body ≥4800 viral copies triggered dissemination and ≥12,000 viral copies set out transmission. Only 27.3% and 18.2% of Ae. albopictus Montpellier mosquitoes meet respectively these two criteria. Collectively, these compelling results stress the poor ability of Ae. albopictus to sustain a local transmission of ZIKV in Europe and provide a promising tool to evaluate the risk of ZIKV transmission in future outbreaks.

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          Most cited references 36

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          First report of autochthonous transmission of Zika virus in Brazil

          In the early 2015, several cases of patients presenting symptoms of mild fever, rash, conjunctivitis and arthralgia were reported in the northeastern Brazil. Although all patients lived in a dengue endemic area, molecular and serological diagnosis for dengue resulted negative. Chikungunya virus infection was also discarded. Subsequently, Zika virus (ZIKV) was detected by reverse transcription-polymerase chain reaction from the sera of eight patients and the result was confirmed by DNA sequencing. Phylogenetic analysis suggests that the ZIKV identified belongs to the Asian clade. This is the first report of ZIKV infection in Brazil.
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            Zika virus outbreak on Yap Island, Federated States of Micronesia.

            In 2007, physicians on Yap Island reported an outbreak of illness characterized by rash, conjunctivitis, and arthralgia. Although serum from some patients had IgM antibody against dengue virus, the illness seemed clinically distinct from previously detected dengue. Subsequent testing with the use of consensus primers detected Zika virus RNA in the serum of the patients but no dengue virus or other arboviral RNA. No previous outbreaks and only 14 cases of Zika virus disease have been previously documented. We obtained serum samples from patients and interviewed patients for information on clinical signs and symptoms. Zika virus disease was confirmed by a finding of Zika virus RNA or a specific neutralizing antibody response to Zika virus in the serum. Patients with IgM antibody against Zika virus who had a potentially cross-reactive neutralizing-antibody response were classified as having probable Zika virus disease. We conducted a household survey to estimate the proportion of Yap residents with IgM antibody against Zika virus and to identify possible mosquito vectors of Zika virus. We identified 49 confirmed and 59 probable cases of Zika virus disease. The patients resided in 9 of the 10 municipalities on Yap. Rash, fever, arthralgia, and conjunctivitis were common symptoms. No hospitalizations, hemorrhagic manifestations, or deaths due to Zika virus were reported. We estimated that 73% (95% confidence interval, 68 to 77) of Yap residents 3 years of age or older had been recently infected with Zika virus. Aedes hensilli was the predominant mosquito species identified. This outbreak of Zika virus illness in Micronesia represents transmission of Zika virus outside Africa and Asia. Although most patients had mild illness, clinicians and public health officials should be aware of the risk of further expansion of Zika virus transmission. 2009 Massachusetts Medical Society
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              Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors

              Background Several observations support the hypothesis that vector-driven selection plays an important role in shaping dengue virus (DENV) genetic diversity. Clustering of DENV genetic diversity at a particular location may reflect underlying genetic structure of vector populations, which combined with specific vector genotype × virus genotype (G × G) interactions may promote adaptation of viral lineages to local mosquito vector genotypes. Although spatial structure of vector polymorphism at neutral genetic loci is well-documented, existence of G × G interactions between mosquito and virus genotypes has not been formally demonstrated in natural populations. Here we measure G × G interactions in a system representative of a natural situation in Thailand by challenging three isofemale families from field-derived Aedes aegypti with three contemporaneous low-passage isolates of DENV-1. Results Among indices of vector competence examined, the proportion of mosquitoes with a midgut infection, viral RNA concentration in the body, and quantity of virus disseminated to the head/legs (but not the proportion of infected mosquitoes with a disseminated infection) strongly depended on the specific combinations of isofemale families and viral isolates, demonstrating significant G × G interactions. Conclusion Evidence for genetic specificity of interactions in our simple experimental design indicates that vector competence of Ae. aegypti for DENV is likely governed to a large extent by G × G interactions in genetically diverse, natural populations. This result challenges the general relevance of conclusions from laboratory systems that consist of a single combination of mosquito and DENV genotypes. Combined with earlier evidence for fine-scale genetic structure of natural Ae. aegypti populations, our finding indicates that the necessary conditions for local DENV adaptation to mosquito vectors are met.
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                Author and article information

                Journal
                Emerg Microbes Infect
                Emerg Microbes Infect
                TEMI
                temi20
                Emerging Microbes & Infections
                Taylor & Francis
                2222-1751
                2019
                18 November 2019
                : 8
                : 1
                : 1668-1678
                Affiliations
                [a ]Institut Pasteur, Department of Virology, Arboviruses and Insect Vectors , Paris, France
                [b ]Institut Pasteur, Department of Infection and Epidemiology, Emerging Diseases Epidemiology , France
                [c ]Office de l’Environnement de la Corse, Observatoire Conservatoire des Insectes de Corse, Corte , France
                [d ]Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa , Lisboa, Portugal
                [e ]UMR MIVEGEC (IRD 224-CNRS 5290-UM), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle, Institut de Recherche pour le Développement (IRD) , Montpellier, France
                [f ]VECCOTRA , Rivière salée, Martinique
                [g ]Unité des Virus Emergents (UVE), Aix Marseille Université, IHU Méditerranée Infection , Marseille, France
                Author notes
                [CONTACT ] Anna-Bella Failloux anna-bella.failloux@ 123456pasteur.fr

                Supplemental data for this article can be accessed https://doi.org/10.1080/22221751.2019.1689797

                Article
                1689797
                10.1080/22221751.2019.1689797
                6882490
                31735122
                © 2019 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 7, Tables: 3, Equations: 0, References: 37, Pages: 11
                Product
                Funding
                Funded by: European Union’s Horizon 2020
                Award ID: 734548
                Funded by: French Government’s Investissement d’Avenir
                Award ID: ANR-10-LABX-62-IBEID to A-BF
                This study was supported by the European Union’s Horizon 2020 research and innovation program ( 10.13039/501100007601/) under ZIKAlliance grant agreement no. 734548. It was partly funded by the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence “Integrative Biology of Emerging Infectious Diseases” (grant n°ANR-10-LABX-62-IBEID, 10.13039/501100001665 to A-BF), the European Union's Horizon 2020 research and innovation program under grant agreement no. 731060 (Infravec2, Research Infrastructures for the control of vector-borne diseases; http://infravec2.eu/), and the European Union’s Horizon 2020 research and innovation program under EVAg grant agreement no. 653316 ( https://www.european-virus-archive.com/).
                Categories
                Article

                europe, zika, epidemic potential, arbovirus, aedes albopictus

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