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      Culex quinquefasciatus from Rio de Janeiro Is Not Competent to Transmit the Local Zika Virus

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          Abstract

          Background

          The Americas have suffered a dramatic epidemic of Zika since May in 2015, when Zika virus (ZIKV) was first detected in Brazil. Mosquitoes belonging to subgenus Stegomyia of Aedes, particularly Aedes aegypti, are considered the primary vectors of ZIKV. However, the rapid spread of the virus across the continent raised several concerns about the transmission dynamics, especially about potential mosquito vectors. The purpose of this work was to assess the vector competence of the house mosquito Culex quinquefasciatus from an epidemic Zika area, Rio de Janeiro, Brazil, for local circulating ZIKV isolates.

          Methodology/Principal Findings

          Culex quinquefasciatus and Ae. aegypti (positive control of ZIKV infection) from Rio de Janeiro were orally exposed to two ZIKV strains isolated from human cases from Rio de Janeiro (Rio-U1 and Rio-S1). Fully engorged mosquitoes were held in incubators at 26 ± 1°C, 12 h:12 h light:dark cycle and 70 ± 10% humidity. For each combination mosquito population—ZIKV strain, 30 specimens were examined for infection, dissemination and transmission rates, at 7, 14 and 21 days after virus exposure by analyzing body (thorax plus abdomen), head and saliva respectively. Infection rates were minimal to completely absent in all Cx. quinquefasciatus-virus combinations and were significantly high for Ae. aegypti. Moreover, dissemination and transmission were not detected in any Cx. quinquefasciatus mosquitoes whatever the incubation period and the ZIKV isolate. In contrast, Ae. aegypti ensured high viral dissemination and moderate to very high transmission.

          Conclusions/Significance

          The southern house mosquito Cx. quinquefasciatus from Rio de Janeiro was not competent to transmit local strains of ZIKV. Thus, there is no experimental evidence that Cx. quinquefasciatus likely plays a role in the ZIKV transmission. Consequently, at least in Rio, mosquito control to reduce ZIKV transmission should remain focused on Ae. aegypti.

          Author Summary

          The pandemic Zika epidemic has affected nearly all American countries. The etiological agent is a mosquito-borne-virus originated from Africa that spread to Asia and more recently, to the Pacific region and the Americas. We experimentally demonstrated that the common house nightly biting mosquito Culex quinquefasciatus from Rio de Janeiro was not susceptible to locally circulating Zika virus (ZIKV) strains. Dissemination was not observed in Cx. quinquefasciatus regardless of the ZIKV isolate used and the incubation period after the ingestion of an infected blood meal. No infectious ZIKV particle was detected in the saliva of the four Cx. quinquefasciatus populations examined until 3 weeks after virus exposure. In contrast, we confirmed that local Aedes aegypti mosquitoes can be infected, disseminate ZIKV at significantly high rates, and assured moderate to very high viral transmission after day 14 of virus exposure. We concluded that Cx. quinquefasciatus is not competent to transmit local ZIKV. Our results support that mosquito control should focus on Ae. aegypti to reduce Zika transmission.

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          Most cited references55

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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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              Differential Susceptibilities of Aedes aegypti and Aedes albopictus from the Americas to Zika Virus

              Background Since the major outbreak in 2007 in the Yap Island, Zika virus (ZIKV) causing dengue-like syndromes has affected multiple islands of the South Pacific region. In May 2015, the virus was detected in Brazil and then spread through South and Central America. In December 2015, ZIKV was detected in French Guiana and Martinique. The aim of the study was to evaluate the vector competence of the mosquito spp. Aedes aegypti and Aedes albopictus from the Caribbean (Martinique, Guadeloupe), North America (southern United States), South America (Brazil, French Guiana) for the currently circulating Asian genotype of ZIKV isolated from a patient in April 2014 in New Caledonia. Methodology/Principal Findings Mosquitoes were orally exposed to an Asian genotype of ZIKV (NC-2014-5132). Upon exposure, engorged mosquitoes were maintained at 28°±1°C, a 16h:8h light:dark cycle and 80% humidity. 25–30 mosquitoes were processed at 4, 7 and 14 days post-infection (dpi). Mosquito bodies (thorax and abdomen), heads and saliva were analyzed to measure infection, dissemination and transmission, respectively. High infection but lower disseminated infection and transmission rates were observed for both Ae. aegypti and Ae. albopictus. Ae. aegypti populations from Guadeloupe and French Guiana exhibited a higher dissemination of ZIKV than the other Ae. aegypti populations examined. Transmission of ZIKV was observed in both mosquito species at 14 dpi but at a low level. Conclusions/Significance This study suggests that although susceptible to infection, Ae. aegypti and Ae. albopictus were unexpectedly low competent vectors for ZIKV. This may suggest that other factors such as the large naïve population for ZIKV and the high densities of human-biting mosquitoes contribute to the rapid spread of ZIKV during the current outbreak.
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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
                6 September 2016
                September 2016
                : 10
                : 9
                : e0004993
                Affiliations
                [1 ]Laboratório de Mosquitos Transmissores de Hematozoários, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil
                [2 ]Laboratório de Biologia Molecular de Flavivírus, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil
                [3 ]Laboratório de Pesquisa Clínica em Doenças Febris Agudas, Instituto Nacional de Infectologia, Rio de Janeiro, Brazil
                [4 ]Institut Pasteur, Arboviruses and Insect Vectors, Paris, France
                The Connecticut Agricultural Experiment Station, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                • Conceived and designed the experiments: RLdO PB ABF.

                • Performed the experiments: RLdO RSF SSC AFdB KABdS RMdM MGdC LMSR.

                • Analyzed the data: RLdO RSF MCB.

                • Contributed reagents/materials/analysis tools: RLdO MCB.

                • Wrote the paper: RLdO ABF PB MCB.

                Article
                PNTD-D-16-01193
                10.1371/journal.pntd.0004993
                5012671
                27598421
                0a2b8726-0862-432a-b6c2-a315527d2b9b
                © 2016 Fernandes et al

                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
                : 28 June 2016
                : 19 August 2016
                Page count
                Figures: 3, Tables: 0, Pages: 13
                Funding
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES-COFECUB)
                Award ID: 799-14
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003762, Institut Pasteur;
                Award ID: ANR-10-LABX-62-IBEID
                Award Recipient :
                Funded by: FAPERJ- Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro
                Award ID: E-26/102.351/2013
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 1UO1 AI115595-01
                Award Recipient :
                This work was funded by CAPES-COFECUB COORDENAÇÃO DE APERFEIÇOAMENTO DE PESSOAL DE NÍVEL SUPERIOR (grant n. 799/14), the Institut Pasteur, the French Government's Investissement d'Avenir program, aboratoire d'Excellence "Integrative Biology of Emerging Infectious Diseases"(grant n. ANR-10-LABX-62-IBEID), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (grant n. E-26/102.351/2013), Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant n. 309577/2013-6). National Institut of Health (grant n. 1UO1 AI115595-01). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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