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The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti

BACKGROUND: Wolbachia pipientis is a common endosymbiotic bacterium of arthropods that strongly inhibits dengue virus (DENV) infection and transmission in the primary vector, the mosquito Aedes aegypti. For that reason, Wolbachia-infected Ae. aegypti are currently being released into the field as pa...

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Autores principales: Pacidônio, Etiene Casagrande, Caragata, Eric Pearce, Alves, Debora Magalhães, Marques, João Trindade, Moreira, Luciano Andrade
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5474007/
https://www.ncbi.nlm.nih.gov/pubmed/28623959
http://dx.doi.org/10.1186/s13071-017-2236-z
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author Pacidônio, Etiene Casagrande
Caragata, Eric Pearce
Alves, Debora Magalhães
Marques, João Trindade
Moreira, Luciano Andrade
author_facet Pacidônio, Etiene Casagrande
Caragata, Eric Pearce
Alves, Debora Magalhães
Marques, João Trindade
Moreira, Luciano Andrade
author_sort Pacidônio, Etiene Casagrande
collection PubMed
description BACKGROUND: Wolbachia pipientis is a common endosymbiotic bacterium of arthropods that strongly inhibits dengue virus (DENV) infection and transmission in the primary vector, the mosquito Aedes aegypti. For that reason, Wolbachia-infected Ae. aegypti are currently being released into the field as part of a novel strategy to reduce DENV transmission. However, there is evidence that DENV can be transmitted vertically from mother to progeny, and this may help the virus persist in nature in the absence of regular human transmission. The effect of Wolbachia infection on this process had not previously been examined. RESULTS: We challenged Ae. aegypti with different Brazilian DENV isolates either by oral feeding or intrathoracic injection to ensure disseminated infection. We examined the effect of Wolbachia infection on the prevalence of DENV infection, and viral load in the ovaries. For orally infected mosquitoes, Wolbachia decreased the prevalence of infection by 71.29%, but there was no such effect when the virus was injected. Interestingly, regardless of the method of infection, Wolbachia infection strongly reduced DENV load in the ovaries. We then looked at the effect of Wolbachia on vertical transmission, where we observed only very low rates of vertical transmission. There was a trend towards lower rates in the presence of Wolbachia, with overall maximum likelihood estimate of infection rates of 5.04 per 1000 larvae for mosquitoes without Wolbachia, and 1.93 per 1000 larvae for Wolbachia-infected mosquitoes, after DENV injection. However, this effect was not statistically significant. CONCLUSIONS: Our data support the idea that vertical transmission of DENV is rare in nature, even in the absence of Wolbachia. Indeed, we observed that vertical transmission rates were low even when the midgut barrier was bypassed, which might help to explain why we only observed a trend towards lower vertical transmission rates in the presence of Wolbachia. Nevertheless, the low prevalence of disseminated DENV infection and lower DENV load in the ovaries supports the hypothesis that the presence of Wolbachia in Ae. aegypti would have an effect on the vertical transmission of DENV in the field. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-017-2236-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-54740072017-06-21 The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti Pacidônio, Etiene Casagrande Caragata, Eric Pearce Alves, Debora Magalhães Marques, João Trindade Moreira, Luciano Andrade Parasit Vectors Short Report BACKGROUND: Wolbachia pipientis is a common endosymbiotic bacterium of arthropods that strongly inhibits dengue virus (DENV) infection and transmission in the primary vector, the mosquito Aedes aegypti. For that reason, Wolbachia-infected Ae. aegypti are currently being released into the field as part of a novel strategy to reduce DENV transmission. However, there is evidence that DENV can be transmitted vertically from mother to progeny, and this may help the virus persist in nature in the absence of regular human transmission. The effect of Wolbachia infection on this process had not previously been examined. RESULTS: We challenged Ae. aegypti with different Brazilian DENV isolates either by oral feeding or intrathoracic injection to ensure disseminated infection. We examined the effect of Wolbachia infection on the prevalence of DENV infection, and viral load in the ovaries. For orally infected mosquitoes, Wolbachia decreased the prevalence of infection by 71.29%, but there was no such effect when the virus was injected. Interestingly, regardless of the method of infection, Wolbachia infection strongly reduced DENV load in the ovaries. We then looked at the effect of Wolbachia on vertical transmission, where we observed only very low rates of vertical transmission. There was a trend towards lower rates in the presence of Wolbachia, with overall maximum likelihood estimate of infection rates of 5.04 per 1000 larvae for mosquitoes without Wolbachia, and 1.93 per 1000 larvae for Wolbachia-infected mosquitoes, after DENV injection. However, this effect was not statistically significant. CONCLUSIONS: Our data support the idea that vertical transmission of DENV is rare in nature, even in the absence of Wolbachia. Indeed, we observed that vertical transmission rates were low even when the midgut barrier was bypassed, which might help to explain why we only observed a trend towards lower vertical transmission rates in the presence of Wolbachia. Nevertheless, the low prevalence of disseminated DENV infection and lower DENV load in the ovaries supports the hypothesis that the presence of Wolbachia in Ae. aegypti would have an effect on the vertical transmission of DENV in the field. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-017-2236-z) contains supplementary material, which is available to authorized users. BioMed Central 2017-06-17 /pmc/articles/PMC5474007/ /pubmed/28623959 http://dx.doi.org/10.1186/s13071-017-2236-z Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Short Report
Pacidônio, Etiene Casagrande
Caragata, Eric Pearce
Alves, Debora Magalhães
Marques, João Trindade
Moreira, Luciano Andrade
The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti
title The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti
title_full The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti
title_fullStr The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti
title_full_unstemmed The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti
title_short The impact of Wolbachia infection on the rate of vertical transmission of dengue virus in Brazilian Aedes aegypti
title_sort impact of wolbachia infection on the rate of vertical transmission of dengue virus in brazilian aedes aegypti
topic Short Report
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5474007/
https://www.ncbi.nlm.nih.gov/pubmed/28623959
http://dx.doi.org/10.1186/s13071-017-2236-z
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