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      Peridomestic Aedes malayensis and Aedes albopictus are capable vectors of arboviruses in cities

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          Abstract

          Background

          Dengue and chikungunya are global re-emerging mosquito-borne diseases. In Singapore, sustained vector control coupled with household improvements reduced domestic mosquito populations for the past 45 years, particularly the primary vector Aedes aegypti. However, while disease incidence was low for the first 30 years following vector control implementation, outbreaks have re-emerged in the past 15 years. Epidemiological observations point to the importance of peridomestic infection in areas not targeted by control programs. We investigated the role of vectors in peri-domestic areas.

          Methods

          We carried out entomological surveys to identify the Aedes species present in vegetated sites in highly populated areas and determine whether mosquitoes were present in open-air areas frequented by people. We compared vector competence of Aedes albopictus and Aedes malayensis with Ae. aegypti after oral infection with sympatric dengue serotype 2 and chikungunya viruses. Mosquito saliva was tested for the presence of infectious virus particles as a surrogate for transmission following oral infection.

          Results

          We identified Aedes albopictus and Aedes malayensis throughout Singapore and quantified their presence in forested and opened grassy areas. Both Ae. albopictus and Ae. malayensis can occupy sylvatic niches and were highly susceptible to both arboviruses. A majority of saliva of infected Ae. malayensis contained infectious particles for both viruses.

          Conclusions

          Our study reveals the prevalence of competent vectors in peri-domestic areas, including Ae. malayensis for which we established the vector status. Epidemics can be driven by infection foci, which are epidemiologically enhanced in the context of low herd immunity, selective pressure on arbovirus transmission and the presence of infectious asymptomatic persons, all these conditions being present in Singapore. Learning from Singapore’s vector control success that reduced domestic vector populations, but has not sustainably reduced arboviral incidence, we suggest including peri-domestic vectors in the scope of vector management.

          Author summary

          Dengue and chikungunya are mosquito-borne diseases and re-emerging as a global burden of the 21 st century. Because of the absence of cure and limitations of the current vaccine, vector control remains the sole efficient intervention to mitigate epidemics. The highly-populated city of Singapore represents an example of successful vector control, where the primary vector Aedes aegypti has practically disappeared from households. However, there as well, dengue and chikungunya are re-emerging. In this study, we surveyed peridomestic sites for mosquito vectors and identified Aedes albopictus and Aedes malayensis throughout Singapore and in open-air areas frequented by people. We further showed that both mosquito species are highly susceptible to dengue and chikungunya viruses and detected infectious virus particles in mosquito saliva, indicating their transmission capacity. Our study provides evidence that Ae. albopictus and Ae. malayensis possess all the traits necessary to contribute to virus transmission in cities and suggest that peridomestic areas be included in vector management programme.

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          Most cited references68

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          The global emergence/resurgence of arboviral diseases as public health problems.

          During the past 20 years there has been a dramatic resurgence or emergence of epidemic arboviral diseases affecting both humans and domestic animals. These epidemics have been caused primarily by viruses thought to be under control such as dengue, Japanese encephalitis, yellow fever, and Venezuelan equine encephalitis, or viruses that have expanded their geographic distribution such as West Nile and Rift Valley fever. Several of these viruses are presented as case studies to illustrate the changing epidemiology. The factors responsible for the dramatic resurgence of arboviral diseases in the waning years of the 20th century are discussed, as is the need for rebuilding the public health infrastructure to deal with epidemic vector-borne diseases in the 21st century.
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            Phylogeny of the genus Flavivirus.

            We undertook a comprehensive phylogenetic study to establish the genetic relationship among the viruses of the genus Flavivirus and to compare the classification based on molecular phylogeny with the existing serologic method. By using a combination of quantitative definitions (bootstrap support level and the pairwise nucleotide sequence identity), the viruses could be classified into clusters, clades, and species. Our phylogenetic study revealed for the first time that from the putative ancestor two branches, non-vector and vector-borne virus clusters, evolved and from the latter cluster emerged tick-borne and mosquito-borne virus clusters. Provided that the theory of arthropod association being an acquired trait was correct, pairwise nucleotide sequence identity among these three clusters provided supporting data for a possibility that the non-vector cluster evolved first, followed by the separation of tick-borne and mosquito-borne virus clusters in that order. Clades established in our study correlated significantly with existing antigenic complexes. We also resolved many of the past taxonomic problems by establishing phylogenetic relationships of the antigenically unclassified viruses with the well-established viruses and by identifying synonymous viruses.
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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: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Investigation
                Role: Data curationRole: Formal analysisRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Investigation
                Role: Investigation
                Role: Methodology
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                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
                26 June 2017
                June 2017
                : 11
                : 6
                : e0005667
                Affiliations
                [1 ]Program in Emerging Infectious Disease, Duke-NUS Medical School, Singapore
                [2 ]Department of Clinical Virology, Christian Medical College, Vellore, Tamilnadu, India
                [3 ]Department of Biological Sciences, National University of Singapore, Singapore
                [4 ]MIVEGEC, UMR IRD 224-CNRS5290-Université de Montpellier, Montpellier, France
                North Carolina State University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-4250-6459
                http://orcid.org/0000-0001-6040-040X
                http://orcid.org/0000-0002-3056-9973
                Article
                PNTD-D-17-00285
                10.1371/journal.pntd.0005667
                5501678
                28650959
                b06961c5-e0a6-42dd-9efc-53e845bcfd2c

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 26 February 2017
                : 26 May 2017
                Page count
                Figures: 3, Tables: 1, Pages: 17
                Funding
                Funded by: Ministry of Health Singapore
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001381, National Research Foundation Singapore;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007680, Naval Medical Research Center;
                Award ID: N40345-11-A-0017-00033
                Award Recipient :
                Support for this research came from a grant from the Singapore Infectious Disease Initiative (SIDI/2013/011) funded by the MOH awarded to IHM, the Naval Medical Research Unit-2 BPA (N40345-11-A-0017-00033) awarded to IHM, from the National Research Foundation Singapore under its NIG scheme (NMRC/BNIG/2032/2015) awarded to JP, and from the Duke-NUS Signature Research Programme funded by the Agency for Science, Technology and Research (A*STAR), Singapore, and the Ministry of Health, Singapore. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Organisms
                Viruses
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Aedes Aegypti
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Aedes Aegypti
                People and Places
                Geographical Locations
                Asia
                Singapore
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Arboviral Infections
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Control
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Oviposition
                Custom metadata
                vor-update-to-uncorrected-proof
                2017-07-07
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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