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      Competence of mosquitoes native to the United Kingdom to support replication and transmission of Rift Valley fever virus

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          Abstract

          Background

          Rift Valley fever phlebovirus (RVFV) is a mosquito-borne arbovirus causing severe disease in humans and livestock. It is endemic in Africa and spread to the Arabian Peninsula in 2000 raising concerns it could emerge in Europe. The ability of temperate mosquitoes from the United Kingdom (UK) to support replication and transmission of RVFV is unknown.

          Methods

          In this study, two colonised lines of Culex pipiens, wild-caught Aedes detritus and Ae. rusticus from the UK were infected with pathogenic strains of RVFV to assess their vector competence. Mosquitoes were offered artificial blood-meals containing 10 6 or 10 7 plaque forming units (PFU)/ml RVFV, simulating natural peak viraemia in young ruminants, and maintained at 20 °C or 25 °C for up to 21 days. Bodies, legs and saliva were collected and tested for the presence of viral RNA and infectious virus to determine the infection, dissemination and transmission potential.

          Results

          Across temperatures, doses and strains the average infection, dissemination and transmission rates were: 35, 13 and 5% ( n = 91) for Cx. pipiens (Caldbeck); 23, 14 and 5% ( n = 138) for Cx. pipiens (Brookwood); 36, 28 and 7% ( n = 118) for Ae. detritus. However, despite 35% ( n = 20) being susceptible to infection, Ae. rusticus did not transmit RVFV. Survival of Aedes species was negatively affected by maintenance at 25 °C compared to the more representative peak average British summer temperature of 20 °C. Increased mortality was also observed with some species infected with 10 7 PFU/ml compared to 10 6 PFU/ml.

          Conclusions

          It can be concluded that temperate mosquito species present in the UK demonstrate a transmission potential for RVFV in the laboratory but, even at high temperatures, this occurred at low efficiency.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-018-2884-7) contains supplementary material, which is available to authorized users.

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          Most cited references42

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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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            Enzootic hepatitis or rift valley fever. An undescribed virus disease of sheep cattle and man from east africa

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              "Bird biting" mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology.

              The transmission of vector-borne pathogens is greatly influenced by the ecology of their vector, which is in turn shaped by genetic ancestry, the environment, and the hosts that are fed on. One group of vectors, the mosquitoes in the Culex pipiens complex, play key roles in the transmission of a range of pathogens including several viruses such as West Nile and St. Louis encephalitis viruses, avian malaria (Plasmodium spp.), and filarial worms. The Cx. pipiens complex includes Culex pipiens pipiens with two forms, pipiens and molestus, Culex pipiens pallens, Culex quinquefasciatus, Culex australicus, and Culex globocoxitus. While several members of the complex have limited geographic distributions, Cx. pipienspipiens and Cx. quinquefasciatus are found in all known urban and sub-urban temperate and tropical regions, respectively, across the world, where they are often principal disease vectors. In addition, hybrids are common in areas of overlap. Although gaps in our knowledge still remain, the advent of genetic tools has greatly enhanced our understanding of the history of speciation, domestication, dispersal, and hybridization. We review the taxonomy, genetics, evolution, behavior, and ecology of members of the Cx. pipiens complex and their role in the transmission of medically important pathogens. The adaptation of Cx. pipiens complex mosquitoes to human-altered environments led to their global distribution through dispersal via humans and, combined with their mixed feeding patterns on birds and mammals (including humans), increased the transmission of several avian pathogens to humans. We highlight several unanswered questions that will increase our ability to control diseases transmitted by these mosquitoes. Copyright © 2011 Elsevier B.V. All rights reserved.
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                Author and article information

                Contributors
                sarah.lumley@phe.gov.uk
                Luis.Hernandez-Triana@apha.gsi.gov.uk
                D.Horton@surrey.ac.uk
                Mar.Fernandez@apha.gsi.gov.uk
                Jolyon.Medlock@phe.gov.uk
                Roger.Hewson@phe.gov.uk
                Tony.Fooks@apha.gsi.gov.uk
                Nick.Johnson@apha.gsi.gov.uk
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                18 May 2018
                18 May 2018
                2018
                : 11
                : 308
                Affiliations
                [1 ]Microbiology Services Division, Public Health England, Wiltshire, UK
                [2 ]ISNI 0000 0004 0407 4824, GRID grid.5475.3, School of Veterinary Medicine, , University of Surrey, ; Guildford, UK
                [3 ]ISNI 0000 0004 1765 422X, GRID grid.422685.f, Wildlife Zoonoses and Vector-borne Diseases Research Group, Animal and Plant Health Agency, ; Addlestone, Surrey, UK
                [4 ]ISNI 0000 0004 1936 8470, GRID grid.10025.36, NIHR Health Protection Research Unit in Emerging and Zoonotic Infections, , University of Liverpool, ; Liverpool, UK
                [5 ]ISNI 0000 0004 1936 8470, GRID grid.10025.36, Department of Clinical Infection, Microbiology and Immunology, , University of Liverpool, ; Liverpool, UK
                Author information
                http://orcid.org/0000-0002-8605-3650
                Article
                2884
                10.1186/s13071-018-2884-7
                5960175
                29776384
                40454b1f-36ca-4c50-9a9d-853f513ba371
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 12 February 2018
                : 2 May 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002142, Animal Health and Veterinary Laboratories Agency;
                Award ID: SV3045 and SE4113
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Parasitology
                rift valley fever virus,mosquito,vector competence,uk,arbovirus
                Parasitology
                rift valley fever virus, mosquito, vector competence, uk, arbovirus

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