Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes

ABSTRACT The incidence of locally acquired dengue infections increased during the last decade in the United States, compelling a sustained research effort concerning the dengue mosquito vector, Aedes aegypti, and its microbiome, which has been shown to influence virus transmission success. We examin...

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Autores principales: Sean M. Boyles, Carla N. Mavian, Esteban Finol, Maria Ukhanova, Caroline J. Stephenson, Gabriela Hamerlinck, Seokyoung Kang, Caleb Baumgartner, Mary Geesey, Israel Stinton, Katie Williams, Derrick K. Mathias, Mattia Prosperi, Volker Mai, Marco Salemi, Eva A. Buckner, John A. Lednicky, Adam R. Rivers, Rhoel R. Dinglasan
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:5a5bb94c68b14acd9ffb85935c32f94b2021-11-15T15:29:17ZUnder-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes10.1128/mSphere.00316-202379-5042https://doaj.org/article/5a5bb94c68b14acd9ffb85935c32f94b2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00316-20https://doaj.org/toc/2379-5042ABSTRACT The incidence of locally acquired dengue infections increased during the last decade in the United States, compelling a sustained research effort concerning the dengue mosquito vector, Aedes aegypti, and its microbiome, which has been shown to influence virus transmission success. We examined the “metavirome” of four populations of Aedes aegypti mosquitoes collected in 2016 to 2017 in Manatee County, FL. Unexpectedly, we discovered that dengue virus serotype 4 (DENV4) was circulating in these mosquito populations, representing the first documented case of such a phenomenon in the absence of a local DENV4 human case in this county over a 2-year period. We confirmed that all of the mosquito populations carried the same DENV4 strain, assembled its full genome, validated infection orthogonally by reverse transcriptase PCR, traced the virus origin, estimated the time period of its introduction to the Caribbean region, and explored the viral genetic signatures and mosquito-specific virome associations that potentially mediated DENV4 persistence in mosquitoes. We discuss the significance of prolonged maintenance of the DENV4 infections in A. aegypti that occurred in the absence of a DENV4 human index case in Manatee County with respect to the inability of current surveillance paradigms to detect mosquito vector infections prior to a potential local outbreak. IMPORTANCE Since 1999, dengue outbreaks in the continental United States involving local transmission have occurred only episodically and only in Florida and Texas. In Florida, these episodes appear to be coincident with increased introductions of dengue virus into the region through human travel and migration from countries where the disease is endemic. To date, the U.S. public health response to dengue outbreaks has been largely reactive, and implementation of comprehensive arbovirus surveillance in advance of predictable transmission seasons, which would enable proactive preventative efforts, remains unsupported. The significance of our finding is that it is the first documented report of DENV4 transmission to and maintenance within a local mosquito vector population in the continental United States in the absence of a human case during two consecutive years. Our data suggest that molecular surveillance of mosquito populations in high-risk, high-tourism areas of the United States may enable proactive, targeted vector control before potential arbovirus outbreaks.Sean M. BoylesCarla N. MavianEsteban FinolMaria UkhanovaCaroline J. StephensonGabriela HamerlinckSeokyoung KangCaleb BaumgartnerMary GeeseyIsrael StintonKatie WilliamsDerrick K. MathiasMattia ProsperiVolker MaiMarco SalemiEva A. BucknerJohn A. LednickyAdam R. RiversRhoel R. DinglasanAmerican Society for Microbiologyarticledengue virus serotype 4transmissionAedes aegyptiDENV4flavivirusmosquitoMicrobiologyQR1-502ENmSphere, Vol 5, Iss 2 (2020)
institution DOAJ
collection DOAJ
language EN
topic dengue virus serotype 4
transmission
Aedes aegypti
DENV4
flavivirus
mosquito
Microbiology
QR1-502
spellingShingle dengue virus serotype 4
transmission
Aedes aegypti
DENV4
flavivirus
mosquito
Microbiology
QR1-502
Sean M. Boyles
Carla N. Mavian
Esteban Finol
Maria Ukhanova
Caroline J. Stephenson
Gabriela Hamerlinck
Seokyoung Kang
Caleb Baumgartner
Mary Geesey
Israel Stinton
Katie Williams
Derrick K. Mathias
Mattia Prosperi
Volker Mai
Marco Salemi
Eva A. Buckner
John A. Lednicky
Adam R. Rivers
Rhoel R. Dinglasan
Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes
description ABSTRACT The incidence of locally acquired dengue infections increased during the last decade in the United States, compelling a sustained research effort concerning the dengue mosquito vector, Aedes aegypti, and its microbiome, which has been shown to influence virus transmission success. We examined the “metavirome” of four populations of Aedes aegypti mosquitoes collected in 2016 to 2017 in Manatee County, FL. Unexpectedly, we discovered that dengue virus serotype 4 (DENV4) was circulating in these mosquito populations, representing the first documented case of such a phenomenon in the absence of a local DENV4 human case in this county over a 2-year period. We confirmed that all of the mosquito populations carried the same DENV4 strain, assembled its full genome, validated infection orthogonally by reverse transcriptase PCR, traced the virus origin, estimated the time period of its introduction to the Caribbean region, and explored the viral genetic signatures and mosquito-specific virome associations that potentially mediated DENV4 persistence in mosquitoes. We discuss the significance of prolonged maintenance of the DENV4 infections in A. aegypti that occurred in the absence of a DENV4 human index case in Manatee County with respect to the inability of current surveillance paradigms to detect mosquito vector infections prior to a potential local outbreak. IMPORTANCE Since 1999, dengue outbreaks in the continental United States involving local transmission have occurred only episodically and only in Florida and Texas. In Florida, these episodes appear to be coincident with increased introductions of dengue virus into the region through human travel and migration from countries where the disease is endemic. To date, the U.S. public health response to dengue outbreaks has been largely reactive, and implementation of comprehensive arbovirus surveillance in advance of predictable transmission seasons, which would enable proactive preventative efforts, remains unsupported. The significance of our finding is that it is the first documented report of DENV4 transmission to and maintenance within a local mosquito vector population in the continental United States in the absence of a human case during two consecutive years. Our data suggest that molecular surveillance of mosquito populations in high-risk, high-tourism areas of the United States may enable proactive, targeted vector control before potential arbovirus outbreaks.
format article
author Sean M. Boyles
Carla N. Mavian
Esteban Finol
Maria Ukhanova
Caroline J. Stephenson
Gabriela Hamerlinck
Seokyoung Kang
Caleb Baumgartner
Mary Geesey
Israel Stinton
Katie Williams
Derrick K. Mathias
Mattia Prosperi
Volker Mai
Marco Salemi
Eva A. Buckner
John A. Lednicky
Adam R. Rivers
Rhoel R. Dinglasan
author_facet Sean M. Boyles
Carla N. Mavian
Esteban Finol
Maria Ukhanova
Caroline J. Stephenson
Gabriela Hamerlinck
Seokyoung Kang
Caleb Baumgartner
Mary Geesey
Israel Stinton
Katie Williams
Derrick K. Mathias
Mattia Prosperi
Volker Mai
Marco Salemi
Eva A. Buckner
John A. Lednicky
Adam R. Rivers
Rhoel R. Dinglasan
author_sort Sean M. Boyles
title Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes
title_short Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes
title_full Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes
title_fullStr Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes
title_full_unstemmed Under-the-Radar Dengue Virus Infections in Natural Populations of <named-content content-type="genus-species">Aedes aegypti</named-content> Mosquitoes
title_sort under-the-radar dengue virus infections in natural populations of <named-content content-type="genus-species">aedes aegypti</named-content> mosquitoes
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/5a5bb94c68b14acd9ffb85935c32f94b
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