Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus

Abstract Background Japanese encephalitis virus (JEV) is the principal cause of mosquito-borne encephalitis in human populations within Asia. If introduced into new geographic areas, it could have further implications for public and animal health. However, potential mosquito vectors for virus transm...

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Main Authors: Luis M. Hernández-Triana, Arran J. Folly, Sanam Sewgobind, Fabian Z. X. Lean, Stuart Ackroyd, Alejandro Nuñez, Sarah Delacour, Andrea Drago, Patrizia Visentin, Karen L. Mansfield, Nicholas Johnson
Format: Article
Language:English
Published: BMC 2022-06-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-022-05329-0
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author Luis M. Hernández-Triana
Arran J. Folly
Sanam Sewgobind
Fabian Z. X. Lean
Stuart Ackroyd
Alejandro Nuñez
Sarah Delacour
Andrea Drago
Patrizia Visentin
Karen L. Mansfield
Nicholas Johnson
author_facet Luis M. Hernández-Triana
Arran J. Folly
Sanam Sewgobind
Fabian Z. X. Lean
Stuart Ackroyd
Alejandro Nuñez
Sarah Delacour
Andrea Drago
Patrizia Visentin
Karen L. Mansfield
Nicholas Johnson
author_sort Luis M. Hernández-Triana
collection DOAJ
description Abstract Background Japanese encephalitis virus (JEV) is the principal cause of mosquito-borne encephalitis in human populations within Asia. If introduced into new geographic areas, it could have further implications for public and animal health. However, potential mosquito vectors for virus transmission have not been fully investigated. The Asian tiger mosquito, Aedes albopictus, has emerged in Europe and is now expanding its geographical range into more northerly latitudes. Culex quinquefasciatus, although absent from Europe, has been detected in Turkey, a country with territory in Europe, and could act as a vector for JEV in other regions. To assess the risk of these invasive species acting as vectors for JEV and therefore potentially contributing to its geographical expansion, we have investigated the vector competence of Ae. albopictus and Cx. quinquefasciatus. Methods Two colonised lines of Ae. albopictus (Italy and Spain) and a line of Cx. quinquefasciatus (Tanzania) were compared for susceptibility to infection by oral feeding with JEV strain SA-14, genotype III at 106 PFU/ml and maintained at 25 °C. Specimens were processed at 7 and 14 days post-inoculation (dpi). Rates of infection, dissemination and transmission were assessed through detection of viral RNA by real-time polymerase chain reaction (RT-PCR) in mosquito body, legs and saliva, respectively, at each time point. Where possible, infection and dissemination were confirmed by immunohistochemical (IHC) detection of the JEV envelope protein. Results Aedes albopictus from Italy showed no susceptibility to infection with JEV strain SA-14. Conversely, Ae. albopictus colonised in Spain was susceptible and 100% of infected mosquitoes that were subjected to saliva screening expressed viral RNA at 14 dpi. Culex quinquefasciatus was highly susceptible to infection as early as 7 dpi and 50% of infected mosquitoes that were subjected to saliva screening expressed viral RNA at 14 dpi. Infection and dissemination were confirmed in Cx. quinquefasciatus by IHC detection of JEV envelope protein in both the mid-gut and salivary glands. Conclusions Aedes albopictus from two different locations in Europe range from being susceptible to JEV and capable of transmission through to being resistant. Culex quinquefasciatus also appears highly susceptible; therefore, both species could potentially act as vectors for JEV and facilitate the emergence of JEV into new regions. Graphical Abstract
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spelling doaj.art-44e3ea4328684b2292373b54a69f01632022-12-22T02:33:07ZengBMCParasites & Vectors1756-33052022-06-011511810.1186/s13071-022-05329-0Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virusLuis M. Hernández-Triana0Arran J. Folly1Sanam Sewgobind2Fabian Z. X. Lean3Stuart Ackroyd4Alejandro Nuñez5Sarah Delacour6Andrea Drago7Patrizia Visentin8Karen L. Mansfield9Nicholas Johnson10Vector Borne Diseases, Animal and Plant Health AgencyVector Borne Diseases, Animal and Plant Health AgencyVector Borne Diseases, Animal and Plant Health AgencyPathology and Animal Sciences Department, Animal and Plant Health AgencyPathology and Animal Sciences Department, Animal and Plant Health AgencyPathology and Animal Sciences Department, Animal and Plant Health AgencyVeterinary Faculty, University of ZaragozaEntostudio SrLEntostudio SrLVector Borne Diseases, Animal and Plant Health AgencyVector Borne Diseases, Animal and Plant Health AgencyAbstract Background Japanese encephalitis virus (JEV) is the principal cause of mosquito-borne encephalitis in human populations within Asia. If introduced into new geographic areas, it could have further implications for public and animal health. However, potential mosquito vectors for virus transmission have not been fully investigated. The Asian tiger mosquito, Aedes albopictus, has emerged in Europe and is now expanding its geographical range into more northerly latitudes. Culex quinquefasciatus, although absent from Europe, has been detected in Turkey, a country with territory in Europe, and could act as a vector for JEV in other regions. To assess the risk of these invasive species acting as vectors for JEV and therefore potentially contributing to its geographical expansion, we have investigated the vector competence of Ae. albopictus and Cx. quinquefasciatus. Methods Two colonised lines of Ae. albopictus (Italy and Spain) and a line of Cx. quinquefasciatus (Tanzania) were compared for susceptibility to infection by oral feeding with JEV strain SA-14, genotype III at 106 PFU/ml and maintained at 25 °C. Specimens were processed at 7 and 14 days post-inoculation (dpi). Rates of infection, dissemination and transmission were assessed through detection of viral RNA by real-time polymerase chain reaction (RT-PCR) in mosquito body, legs and saliva, respectively, at each time point. Where possible, infection and dissemination were confirmed by immunohistochemical (IHC) detection of the JEV envelope protein. Results Aedes albopictus from Italy showed no susceptibility to infection with JEV strain SA-14. Conversely, Ae. albopictus colonised in Spain was susceptible and 100% of infected mosquitoes that were subjected to saliva screening expressed viral RNA at 14 dpi. Culex quinquefasciatus was highly susceptible to infection as early as 7 dpi and 50% of infected mosquitoes that were subjected to saliva screening expressed viral RNA at 14 dpi. Infection and dissemination were confirmed in Cx. quinquefasciatus by IHC detection of JEV envelope protein in both the mid-gut and salivary glands. Conclusions Aedes albopictus from two different locations in Europe range from being susceptible to JEV and capable of transmission through to being resistant. Culex quinquefasciatus also appears highly susceptible; therefore, both species could potentially act as vectors for JEV and facilitate the emergence of JEV into new regions. Graphical Abstracthttps://doi.org/10.1186/s13071-022-05329-0MosquitoInvasive mosquitoesJapanese encephalitisZoonosisVector competencyEmerging infectious disease
spellingShingle Luis M. Hernández-Triana
Arran J. Folly
Sanam Sewgobind
Fabian Z. X. Lean
Stuart Ackroyd
Alejandro Nuñez
Sarah Delacour
Andrea Drago
Patrizia Visentin
Karen L. Mansfield
Nicholas Johnson
Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus
Parasites & Vectors
Mosquito
Invasive mosquitoes
Japanese encephalitis
Zoonosis
Vector competency
Emerging infectious disease
title Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus
title_full Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus
title_fullStr Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus
title_full_unstemmed Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus
title_short Susceptibility of Aedes albopictus and Culex quinquefasciatus to Japanese encephalitis virus
title_sort susceptibility of aedes albopictus and culex quinquefasciatus to japanese encephalitis virus
topic Mosquito
Invasive mosquitoes
Japanese encephalitis
Zoonosis
Vector competency
Emerging infectious disease
url https://doi.org/10.1186/s13071-022-05329-0
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