Under-the-Radar Dengue Virus Infections in Natural Populations of Aedes aegypti Mosquitoes
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...
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doaj-f95c8e3bf5db4493a5a3deff538773712020-11-25T01:22:18ZengAmerican Society for MicrobiologymSphere2379-50422020-04-0152e00316-2010.1128/mSphere.00316-20Under-the-Radar Dengue Virus Infections in Natural Populations of Aedes aegypti MosquitoesSean 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. DinglasanSince 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.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.https://doi.org/10.1128/mSphere.00316-20dengue virus serotype 4transmissionaedes aegyptidenv4flavivirusmosquitoarbovirussurveillanceinsect-specific viruses |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
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 |
spellingShingle |
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 Aedes aegypti Mosquitoes mSphere dengue virus serotype 4 transmission aedes aegypti denv4 flavivirus mosquito arbovirus surveillance insect-specific viruses |
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 Aedes aegypti Mosquitoes |
title_short |
Under-the-Radar Dengue Virus Infections in Natural Populations of Aedes aegypti Mosquitoes |
title_full |
Under-the-Radar Dengue Virus Infections in Natural Populations of Aedes aegypti Mosquitoes |
title_fullStr |
Under-the-Radar Dengue Virus Infections in Natural Populations of Aedes aegypti Mosquitoes |
title_full_unstemmed |
Under-the-Radar Dengue Virus Infections in Natural Populations of Aedes aegypti Mosquitoes |
title_sort |
under-the-radar dengue virus infections in natural populations of aedes aegypti mosquitoes |
publisher |
American Society for Microbiology |
series |
mSphere |
issn |
2379-5042 |
publishDate |
2020-04-01 |
description |
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.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. |
topic |
dengue virus serotype 4 transmission aedes aegypti denv4 flavivirus mosquito arbovirus surveillance insect-specific viruses |
url |
https://doi.org/10.1128/mSphere.00316-20 |
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