Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential

Arbovirus emergence and epidemic potential, as approximated by the vectorial capacity formula, depends on host and vector parameters, including the vector’s intrinsic ability to replicate then transmit the pathogen known as vector competence. Vector competence is a complex, time-dependent, quantitat...

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Main Authors: Viginier, Barbara, Cappuccio, Lucie, Garnier, Céline, Martin, Edwige, Maisse, Carine, Valiente Moro, Claire, Minard, Guillaume, Fontaine, Albin, Lequime, Sébastian, Ratinier, Maxime, Arnaud, Frédérick, Raquin, Vincent
Format: Article
Language:English
Published: Peer Community In 2023-10-01
Series:Peer Community Journal
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Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.326/
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author Viginier, Barbara
Cappuccio, Lucie
Garnier, Céline
Martin, Edwige
Maisse, Carine
Valiente Moro, Claire
Minard, Guillaume
Fontaine, Albin
Lequime, Sébastian
Ratinier, Maxime
Arnaud, Frédérick
Raquin, Vincent
author_facet Viginier, Barbara
Cappuccio, Lucie
Garnier, Céline
Martin, Edwige
Maisse, Carine
Valiente Moro, Claire
Minard, Guillaume
Fontaine, Albin
Lequime, Sébastian
Ratinier, Maxime
Arnaud, Frédérick
Raquin, Vincent
author_sort Viginier, Barbara
collection DOAJ
description Arbovirus emergence and epidemic potential, as approximated by the vectorial capacity formula, depends on host and vector parameters, including the vector’s intrinsic ability to replicate then transmit the pathogen known as vector competence. Vector competence is a complex, time-dependent, quantitative phenotype influenced by biotic and abiotic factors. A combination of experimental and modelling approaches is required to assess arbovirus intra-vector dynamics and estimate epidemic potential. In this study, we measured infection, dissemination, and transmission dynamics of chikungunya virus (CHIKV) in a field-derived Aedes albopictus population (Lyon, France) after oral exposure to a range of virus doses spanning human viraemia. Statistical modelling indicates rapid and efficient CHIKV progression in the vector mainly due to an absence of a dissemination barrier, with 100% of the infected mosquitoes ultimately exhibiting a disseminated infection, regardless of the virus dose. Transmission rate data revealed a time-dependent, but overall weak, transmission barrier, with individuals transmitting as soon as 2 days post-exposure (dpe) and >50% infectious mosquitoes at 6 dpe for the highest dose. Based on these experimental intra-vector dynamics data, epidemiological simulations conducted with an agent-based model showed that even at low mosquito biting rates, CHIKV could trigger outbreaks locally. Together, this reveals the epidemic potential of CHIKV upon transmission by Aedes albopictus in mainland France.
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spelling doaj-art-7805669c2d924815bf2733d6579c47892025-02-07T10:16:48ZengPeer Community InPeer Community Journal2804-38712023-10-01310.24072/pcjournal.32610.24072/pcjournal.326Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential Viginier, Barbara0https://orcid.org/0000-0002-0733-8974Cappuccio, Lucie1https://orcid.org/0009-0000-7118-4060Garnier, Céline2Martin, Edwige3Maisse, Carine4https://orcid.org/0000-0003-2848-1638 Valiente Moro, Claire5https://orcid.org/0000-0002-7193-405XMinard, Guillaume6https://orcid.org/0000-0002-2079-8844Fontaine, Albin7https://orcid.org/0000-0001-6869-6516Lequime, Sébastian8https://orcid.org/0000-0002-3140-0651Ratinier, Maxime9https://orcid.org/0000-0003-2271-3549Arnaud, Frédérick10https://orcid.org/0000-0001-6893-9848Raquin, Vincent11https://orcid.org/0000-0001-6814-4199IVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceIVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceIVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceUniversite Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR Ecologie Microbienne, F-69622 Villeurbanne, FranceIVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceUniversite Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR Ecologie Microbienne, F-69622 Villeurbanne, FranceUniversite Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR Ecologie Microbienne, F-69622 Villeurbanne, FranceUnité Parasitologie et Entomologie, Département Microbiologie et maladies infectieuses, Institut de Recherche Biomédicale des Armées (IRBA), Marseille, France; Aix Marseille Univ, IRD, SSA, AP-HM, UMR Vecteurs–Infections Tropicales et Méditerranéennes (VITROME), Marseille, France; IHU Méditerranée Infection, Marseille, FranceCluster of Microbial Ecology, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The NetherlandsIVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceIVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceIVPC UMR754, INRAE, Universite Claude Bernard Lyon 1, EPHE, PSL Research University, F-69007 Lyon, FranceArbovirus emergence and epidemic potential, as approximated by the vectorial capacity formula, depends on host and vector parameters, including the vector’s intrinsic ability to replicate then transmit the pathogen known as vector competence. Vector competence is a complex, time-dependent, quantitative phenotype influenced by biotic and abiotic factors. A combination of experimental and modelling approaches is required to assess arbovirus intra-vector dynamics and estimate epidemic potential. In this study, we measured infection, dissemination, and transmission dynamics of chikungunya virus (CHIKV) in a field-derived Aedes albopictus population (Lyon, France) after oral exposure to a range of virus doses spanning human viraemia. Statistical modelling indicates rapid and efficient CHIKV progression in the vector mainly due to an absence of a dissemination barrier, with 100% of the infected mosquitoes ultimately exhibiting a disseminated infection, regardless of the virus dose. Transmission rate data revealed a time-dependent, but overall weak, transmission barrier, with individuals transmitting as soon as 2 days post-exposure (dpe) and >50% infectious mosquitoes at 6 dpe for the highest dose. Based on these experimental intra-vector dynamics data, epidemiological simulations conducted with an agent-based model showed that even at low mosquito biting rates, CHIKV could trigger outbreaks locally. Together, this reveals the epidemic potential of CHIKV upon transmission by Aedes albopictus in mainland France. https://peercommunityjournal.org/articles/10.24072/pcjournal.326/Arbovirus; vector; mosquito; Aedes albopictus; chikungunya virus; epidemiology; vector competence; modelisation
spellingShingle Viginier, Barbara
Cappuccio, Lucie
Garnier, Céline
Martin, Edwige
Maisse, Carine
Valiente Moro, Claire
Minard, Guillaume
Fontaine, Albin
Lequime, Sébastian
Ratinier, Maxime
Arnaud, Frédérick
Raquin, Vincent
Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential
Peer Community Journal
Arbovirus; vector; mosquito; Aedes albopictus; chikungunya virus; epidemiology; vector competence; modelisation
title Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential
title_full Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential
title_fullStr Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential
title_full_unstemmed Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential
title_short Chikungunya intra-vector dynamics in Aedes albopictus from Lyon (France) upon exposure to a human viremia-like dose range reveals vector barrier’s permissiveness and supports local epidemic potential
title_sort chikungunya intra vector dynamics in aedes albopictus from lyon france upon exposure to a human viremia like dose range reveals vector barrier s permissiveness and supports local epidemic potential
topic Arbovirus; vector; mosquito; Aedes albopictus; chikungunya virus; epidemiology; vector competence; modelisation
url https://peercommunityjournal.org/articles/10.24072/pcjournal.326/
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