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      Specific human antibody responses to Aedes aegypti and Aedes polynesiensis saliva: A new epidemiological tool to assess human exposure to disease vectors in the Pacific

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          Abstract

          Background

          Aedes mosquitoes severely affect the health and wellbeing of human populations by transmitting infectious diseases. In French Polynesia, Aedes aegypti is the main vector of dengue, chikungunya and Zika, and Aedes polynesiensis the primary vector of Bancroftian filariasis and a secondary vector of arboviruses. Tools for assessing the risk of disease transmission or for measuring the efficacy of vector control programmes are scarce. A promising approach to quantify the human-vector contact relies on the detection and the quantification of antibodies directed against mosquito salivary proteins.

          Methodology/Principal findings

          An ELISA test was developed to detect and quantify the presence of immunoglobulin G (IgG) directed against proteins from salivary gland extracts (SGE) of Ae. aegypti and Ae. polynesiensis in human populations exposed to either species, through a cross-sectional study. In Tahiti and Moorea islands where Ae. aegypti and Ae. polynesiensis are present, the test revealed that 98% and 68% of individuals have developed IgG directed against Ae. aegypti and Ae. polynesiensis SGE, respectively. By comparison, ELISA tests conducted on a cohort of people from metropolitan France, not exposed to these Aedes mosquitoes, indicated that 97% of individuals had no IgG directed against SGE of either mosquito species. The analysis of additional cohorts representing different entomological Aedes contexts showed no ELISA IgG cross-reactivity between Ae. aegypti and Ae. polynesiensis SGE.

          Conclusions/Significance

          The IgG response to salivary gland extracts seems to be a valid and specific biomarker of human exposure to the bites of Ae. aegypti and Ae. polynesiensis. This new immuno-epidemiological tool will enhance our understanding of people exposure to mosquito bites, facilitate the identification of areas where disease transmission risk is high and permit to evaluate the efficacy of novel vector control strategies in Pacific islands and other tropical settings.

          Author summary

          In Pacific islands like in most tropical regions, Aedes mosquitoes affect the health of human populations by transmitting diseases like dengue, chikungunya, Zika and filariasis. The biting nuisance of Aedes mosquitoes also impacts local tourism, affecting the sustainability of island economies. Mosquito saliva is injected during the biting process, and the response triggered by the human immune system to proteins contained in mosquito saliva was shown to be a relevant biomarker of exposure to mosquito bites. Using this approach, we have developed an immuno-epidemiological tool to investigate the exposure of people to the bites of Aedes aegypti and Aedes polynesiensis, two significant mosquito vectors of infectious diseases in French Polynesia and other island countries and territories in the Pacific. This novel tool proved specific and reliable. It will improve the assessment of disease transmission risk and be useful for measuring the efficacy of both conventional and innovative vector control strategies.

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          Most cited references48

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          ZIKA VIRUS INFECTION IN MAN.

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            Zika Virus Seroprevalence, French Polynesia, 2014–2015

            During 2013–2014, French Polynesia experienced an outbreak of Zika virus infection. Serosurveys conducted at the end of the outbreak and 18 months later showed lower than expected disease prevalence rates (49%) and asymptomatic:symptomatic case ratios (1:1) in the general population but significantly different prevalence rates (66%) and asymptomatic:symptomatic ratios (1:2) in schoolchildren.
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              Identification of human-derived volatile chemicals that interfere with attraction of Aedes aegypti mosquitoes.

              It is known that human individuals show different levels of attractiveness to mosquitoes. In this study, we investigated the chemical basis for low attractiveness. We recorded behaviors of Aedes aegypti toward the hands of human volunteers and toward the volatile chemicals produced by their bodies. Some individuals, and their corresponding volatiles, elicited low upwind flight, relative attraction, and probing activity. Analyzing the components by gas chromatography coupled to electrophysiological recordings from the antennae of Aedes aegypti, enabled the location of 33 physiologically relevant compounds. The results indicated that higher levels of specific compounds may be responsible for decreased "attractiveness." In behavioral experiments, five of the compounds caused a significant reduction in upwind flight of Aedes aegypti to attractive human hands. Thus, unattractiveness of individuals may result from a repellent, or attractant "masking," mechanism.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: ResourcesRole: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Validation
                Role: Formal analysisRole: VisualizationRole: Writing – original draft
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: 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
                24 July 2018
                July 2018
                : 12
                : 7
                : e0006660
                Affiliations
                [1 ] UMR MIVEGEC, IRD, CNRS, UM, Institut de Recherche pour le Développement, Nouméa, Nouvelle-Calédonie
                [2 ] UMR MIVEGEC IRD, CNRS, UM, Institut de Recherche pour le Développement, Montpellier, France
                [3 ] Pôle de recherche et de veille sur les maladies infectieuses émergentes, Institut Louis Malardé, Papeete, Tahiti, Polynésie française
                [4 ] Laboratoire d’entomologie médicale, Institut Louis Malardé, Paea, Tahiti, Polynésie française
                North Carolina State University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2994-3697
                http://orcid.org/0000-0002-4227-2851
                http://orcid.org/0000-0002-8757-0350
                Article
                PNTD-D-17-02076
                10.1371/journal.pntd.0006660
                6075770
                30040826
                27b3de85-296a-47da-a968-403f40b240fa
                © 2018 Mathieu-Daudé 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
                : 22 January 2018
                : 3 July 2018
                Page count
                Figures: 3, Tables: 1, Pages: 16
                Funding
                Funded by: French Polynesian government
                Award ID: #34312/MEE/REC
                Award Recipient :
                Funded by: Grand Observatoire du Pacifique Sud
                Award ID: #2011-2
                Award Recipient :
                This study was supported in part by the French Polynesian government grant #34312/MEE/REC (recipient HCB), and the Grand Observatoire du Pacifique Sud grant #2011-2 (recipient FMD) ( http://www.observatoire-gops.org/en/accueil). FAM was a recipient of a Infectiopôle Sud Foundation fellowship. 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
                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
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Aedes Aegypti
                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
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Islands
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Disease Control
                People and places
                Geographical locations
                Oceania
                French Polynesia
                Research and Analysis Methods
                Immunologic Techniques
                Immunoassays
                Enzyme-Linked Immunoassays
                Social Sciences
                Political Science
                Governments
                Armed Forces
                Military Personnel
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Saliva
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Saliva
                Biology and Life Sciences
                Physiology
                Body Fluids
                Saliva
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Saliva
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-08-03
                All relevant data are within the paper and its Supporting Information files. Cohort data were anonymized to ensure participant confidentiality.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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