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      Vector competence of Anopheles quadrimaculatus and Aedes albopictus for genetically distinct Jamestown Canyon virus strains circulating in the Northeast United States

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          Abstract

          Background

          Jamestown Canyon virus (JCV; Peribunyaviridae, Orthobunyavirus) is a mosquito-borne pathogen belonging to the California serogroup. The virus is endemic in North America and increasingly recognized as a public health concern. In this study, we determined the vector competence of Anopheles (An.) quadrimaculatus and Aedes (Ae.) albopictus for five JCV strains belonging to the two lineages circulating in the Northeast.

          Methods

          An. quadrimaculatus and Ae. albopictus were fed blood meals containing two lineage A strains and three lineage B strains. Vector competence of both mosquito species was evaluated at 7- and 14-days post-feeding (dpf) by testing for virus presence in bodies, legs, and saliva.

          Results

          Our results demonstrated that Ae. albopictus mosquitoes are a competent vector for both lineages, with similar transmission levels for all strains tested. Variable levels of infection (46–83%) and dissemination (17–38%) were measured in An. quadrimaculatus, yet no transmission was detected for the five JCV strains evaluated.

          Conclusions

          Our results demonstrate that establishment of Ae. albopictus in the Northeast could increase the risk of JCV but suggest An. quadrimaculatus are not a competent vector for JCV.

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          Most cited references43

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          Critical review of the vector status of Aedes albopictus.

          N G Gratz (2004)
          The mosquito Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), originally indigenous to South-east Asia, islands of the Western Pacific and Indian Ocean, has spread during recent decades to Africa, the mid-east, Europe and the Americas (north and south) after extending its range eastwards across Pacific islands during the early 20th century. The majority of introductions are apparently due to transportation of dormant eggs in tyres. Among public health authorities in the newly infested countries and those threatened with the introduction, there has been much concern that Ae. albopictus would lead to serious outbreaks of arbovirus diseases (Ae. albopictus is a competent vector for at least 22 arboviruses), notably dengue (all four serotypes) more commonly transmitted by Aedes (Stegomyia) aegypti (L.). Results of many laboratory studies have shown that many arboviruses are readily transmitted by Ae. albopictus to laboratory animals and birds, and have frequently been isolated from wild-caught mosquitoes of this species, particularly in the Americas. As Ae. albopictus continues to spread, displacing Ae. aegypti in some areas, and is anthropophilic throughout its range, it is important to review the literature and attempt to predict whether the medical risks are as great as have been expressed in scientific journals and the popular press. Examination of the extensive literature indicates that Ae. albopictus probably serves as a maintenance vector of dengue in rural areas of dengue-endemic countries of South-east Asia and Pacific islands. Also Ae. albopictus transmits dog heartworm Dirofilaria immitis (Leidy) (Spirurida: Onchocercidae) in South-east Asia, south-eastern U.S.A. and both D. immitis and Dirofilaria repens (Raillet & Henry) in Italy. Despite the frequent isolation of dengue viruses from wild-caught mosquitoes, there is no evidence that Ae. albopictus is an important urban vector of dengue, except in a limited number of countries where Ae. aegypti is absent, i.e. parts of China, the Seychelles, historically in Japan and most recently in Hawaii. Further research is needed on the dynamics of the interaction between Ae. albopictus and other Stegomyia species. Surveillance must also be maintained on the vectorial role of Ae. albopictus in countries endemic for dengue and other arboviruses (e.g. Chikungunya, EEE, Ross River, WNV, LaCrosse and other California group viruses), for which it would be competent and ecologically suited to serve as a bridge vector.
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            Genetic and phenotypic variation of West Nile virus in New York, 2000-2003.

            West Nile virus (WNV) strains circulating during the first five years of WNV transmission in New York were collected, partial nucleotide sequences were determined, and in vitro and in vivo phenotypic analyses of selected strains were undertaken to determine whether observed increases in the intensity of enzootic and epidemic transmission in New York State during 2002 and 2003 were associated with viral genetic changes. Functionally diverse regions of the WNV genome were also compared to determine whether some regions may be more or less variable than others. The complete envelope coding regions of 67 strains and fragments of the nonstructural protein 5 (NS5) and 3' noncoding regions of 39 strains collected during 2002 and 2003 were examined. West Nile virus in New York remains relatively genetically homogeneous. Viral genetic diversity was greater in 2002 and 2003 at both the nucleotide and amino acid levels than in previous years due to the emergence of a new WNV genotype in 2002. This genotype persisted and became dominant in 2003. Envelope and NS5 coding regions were approximately two-fold more likely than the 3' untranslated region to contain nucleotide substitutions, and the envelope region was approximately three-fold more likely to contain amino acid substitutions than the NS5 region. Variation was noted in in vivo mosquito transmission assays, but not in in vitro growth studies. Strains belonging to the epizootiologically dominant clade were transmitted after approximately two fewer days of extrinsic incubation, providing a possible mechanism for the dominance of this clade. The observed increase in the intensity of WNV transmission beginning in 2002 was associated with an increase in viral genetic diversity that was the result of the emergence of an additional phylogenetic clade. This genotype seems to possess an advantage over previously recognized WNV strains in mosquito transmission phenotype.
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              Effects of Zika Virus Strain and Aedes Mosquito Species on Vector Competence

              In the Western Hemisphere, Zika virus is thought to be transmitted primarily by Aedes aegypti mosquitoes. To determine the extent to which Ae. albopictus mosquitoes from the United States are capable of transmitting Zika virus and the influence of virus dose, virus strain, and mosquito species on vector competence, we evaluated multiple doses of representative Zika virus strains in Ae. aegypti and Ae. albopictus mosquitoes. Virus preparation (fresh vs. frozen) significantly affected virus infectivity in mosquitoes. We calculated 50% infectious doses to be 6.1–7.5 log10 PFU/mL; minimum infective dose was 4.2 log10 PFU/mL. Ae. albopictus mosquitoes were more susceptible to infection than Ae. aegypti mosquitoes, but transmission efficiency was higher for Ae. aegypti mosquitoes, indicating a transmission barrier in Ae. albopictus mosquitoes. Results suggest that, although Zika virus transmission is relatively inefficient overall and dependent on virus strain and mosquito species, Ae. albopictus mosquitoes could become major vectors in the Americas.
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                Author and article information

                Contributors
                Constentin.DIEME@pasteur-guinee.org
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                23 June 2022
                23 June 2022
                2022
                : 15
                : 226
                Affiliations
                [1 ]Institut Pasteur de Guinée, Conakry, Guinea
                [2 ]GRID grid.238491.5, ISNI 0000 0004 0367 6866, Wadsworth Center, , New York State Department of Health, ; Slingerlands, NY USA
                [3 ]GRID grid.265850.c, ISNI 0000 0001 2151 7947, Department of Biomedical Sciences, School of Public Health, , State University of New York at Albany, ; Albany, NY USA
                Article
                5342
                10.1186/s13071-022-05342-3
                9229909
                35739573
                65abb6fb-7643-4526-8414-c9fc6964517d
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

                History
                : 30 March 2022
                : 20 May 2022
                Categories
                Research
                Custom metadata
                © The Author(s) 2022

                Parasitology
                jamestown canyon virus,aedes albopictus,anopheles quadrimaculatus,vector competence

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