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      Chikungunya Virus Transmission Potential by Local Aedes Mosquitoes in the Americas and Europe

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          Abstract

          Background

          Chikungunya virus (CHIKV), mainly transmitted in urban areas by the mosquitoes Aedes aegypti and Aedes albopictus, constitutes a major public health problem. In late 2013, CHIKV emerged on Saint-Martin Island in the Caribbean and spread throughout the region reaching more than 40 countries. Thus far, Ae. aegypti mosquitoes have been implicated as the sole vector in the outbreaks, leading to the hypothesis that CHIKV spread could be limited only to regions where this mosquito species is dominant.

          Methodology/Principal Findings

          We determined the ability of local populations of Ae. aegypti and Ae. albopictus from the Americas and Europe to transmit the CHIKV strain of the Asian genotype isolated from Saint-Martin Island (CHIKV_SM) during the recent epidemic, and an East-Central-South African (ECSA) genotype CHIKV strain isolated from La Réunion Island (CHIKV_LR) as a well-characterized control virus. We also evaluated the effect of temperature on transmission of CHIKV_SM by European Ae. albopictus. We found that (i) Aedes aegypti from Saint-Martin Island transmit CHIKV_SM and CHIKV_LR with similar efficiency, (ii) Ae. aegypti from the Americas display similar transmission efficiency for CHIKV_SM, (iii) American and European populations of the alternative vector species Ae. albopictus were as competent as Ae. aegypti populations with respect to transmission of CHIKV_SM and (iv) exposure of European Ae. albopictus to low temperatures (20°C) significantly reduced the transmission potential for CHIKV_SM.

          Conclusions/Significance

          CHIKV strains belonging to the ECSA genotype could also have initiated local transmission in the new world. Additionally, the ongoing CHIKV outbreak in the Americas could potentially spread throughout Ae. aegypti- and Ae. albopictus-infested regions of the Americas with possible imported cases of CHIKV to Ae. albopictus-infested regions in Europe. Colder temperatures may decrease the local transmission of CHIKV_SM by European Ae. albopictus, potentially explaining the lack of autochthonous transmission of CHIKV_SM in Europe despite the hundreds of imported CHIKV cases returning from the Caribbean.

          Author Summary

          More than one million chikungunya cases have been reported in the Americas since October 2013, when the Asian genotype of chikungunya virus (CHIKV) was imported by a traveller returning from Asia. CHIKV is mainly transmitted in urban areas by the domestic mosquitoes Aedes aegypti and Aedes albopictus. In this study, we evaluate the potential for the CHIKV circulating in the Caribbean to initiate outbreaks in Aedes-infested regions of continental America and Europe by assessing the ability of local mosquitoes to experimentally transmit the virus. Mosquitoes were exposed to a blood-meal containing the virus which must overcome several barriers to infect various tissues in the vector before being secreted in the mosquito saliva when biting a host. We found that Ae. aegypti and Ae. albopictus transmitted similarly the virus. When exposing Ae. albopictus from Europe at a temperature of 20°C after infection, we detect a significant drop of CHIKV transmission potential. Our results suggest that the CHIKV outbreak in the Americas could potentially spread throughout Ae. aegypti- and Ae. albopictus-infested regions of the Americas however with a limited risk of spillovers in Ae. albopictus-infested regions in Europe. These data will be useful for adapting vector control strategies and epidemiological surveillance.

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          Most cited references23

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          An integrated semiconductor device enabling non-optical genome sequencing.

          The seminal importance of DNA sequencing to the life sciences, biotechnology and medicine has driven the search for more scalable and lower-cost solutions. Here we describe a DNA sequencing technology in which scalable, low-cost semiconductor manufacturing techniques are used to make an integrated circuit able to directly perform non-optical DNA sequencing of genomes. Sequence data are obtained by directly sensing the ions produced by template-directed DNA polymerase synthesis using all-natural nucleotides on this massively parallel semiconductor-sensing device or ion chip. The ion chip contains ion-sensitive, field-effect transistor-based sensors in perfect register with 1.2 million wells, which provide confinement and allow parallel, simultaneous detection of independent sequencing reactions. Use of the most widely used technology for constructing integrated circuits, the complementary metal-oxide semiconductor (CMOS) process, allows for low-cost, large-scale production and scaling of the device to higher densities and larger array sizes. We show the performance of the system by sequencing three bacterial genomes, its robustness and scalability by producing ion chips with up to 10 times as many sensors and sequencing a human genome.
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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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              Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus.

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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
                20 May 2015
                May 2015
                : 9
                : 5
                : e0003780
                Affiliations
                [1 ]Institut Pasteur, Department of Virology, Arboviruses and Insect Vectors, Paris, France
                [2 ]Sorbonne Universités, Université Pierre et Marie Curie-Paris 6, Institut de Formation Doctorale (IFD), Paris, France
                [3 ]Laboratório de Transmissores de Hematozoários, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil
                [4 ]Centre de Démoustication/Conseil Général de La Martinique, Fort-de-France, Martinique, France
                [5 ]Agence Régionale de Danté (ARS) Guadeloupe, Saint-Martin et Saint-Barthélemy, Pole de Santé Publique, Gourbeyre, Guadeloupe, France
                [6 ]Institut Pasteur de la Guyane, Unité d’Entomologie médicale, Cayenne, French Guiana
                [7 ]Centre National de Référence (CNR) des Arbovirus, Institut de Recherche Biomédicale des Armées Hôpital d’Instruction des Armées Laveran, Marseille, France
                [8 ]Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, Kansas, United States of America
                [9 ]Biosecurity Research Institute, Kansas State University, Manhattan, Kansas, United States of America
                [10 ]Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida, United States of America
                [11 ]Aix Marseille Université, IRD French Institute of Research for Development, EHESP French School of Public Health, EPV UMR_D 190 ‘Emergence des Pathologies Virales’, Marseille, France
                [12 ]IHU Méditerranée Infection, APHM Public Hospitals of Marseille, Marseille, France
                University of Texas Medical Branch, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AVR RLdO XdL ABF. Performed the experiments: AVR RLdO LM MV SF SMA AN. Analyzed the data: AVR AN XdL ABF. Contributed reagents/materials/analysis tools: AY JG RG ID ILG DLV YJSH LPL. Wrote the paper: AVR ABF.

                Article
                PNTD-D-15-00291
                10.1371/journal.pntd.0003780
                4439146
                25993633
                4bff8f5d-8c56-42b1-94bf-d806ea8e51b0
                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
                : 23 February 2015
                : 22 April 2015
                Page count
                Figures: 4, Tables: 2, Pages: 18
                Funding
                This study was funded by the Institut Pasteur, the French Government's Investissement d'Avenir program, Laboratoire d'Excellence "Integrative Biology of Emerging Infectious Diseases" (grant n°ANR-10-LABX-62-IBEID), and the CAPES-COFECUB. AVR was supported by the French Ministry of Superior Education and Research. The funders had no role in study design, data collection and analysis, 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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