Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México

Background: Aedes aegypti, the ‘yellow fever mosquito’, is the primary vector to humans of dengue and yellow fever flaviviruses (DENV, YFV), and is a known vector of the chikungunya alphavirus (CV). Because vaccines are not yet available for DENV or CV or are inadequately distributed in developing c...

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Autores principales: Kittayapong, Pattamaporn, Ponce García, Gustavo, Flores Suárez, Adriana Elizabeth, Fernández Salas, Ildefonso, Saavedra Rodríguez, Karla Lizet, Reyes Solis, Guadalupe del Carmen, Lozano Fuentes, Saúl, Guillermo Bond, J., Casas Martínez, Mauricio, Ramsey, Janine M., García Rejón, Julián Everardo, Domínguez Galera, Marco Antonio, Ranson, Hilary, Hemingway, Janet, Eisen, Lars, Black, William C.
Formato: Artículo
Lenguaje:inglés
Publicado: Public Library of Science 2009
Acceso en línea:http://eprints.uanl.mx/15096/1/784.PDF
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author Kittayapong, Pattamaporn
Ponce García, Gustavo
Flores Suárez, Adriana Elizabeth
Fernández Salas, Ildefonso
Saavedra Rodríguez, Karla Lizet
Reyes Solis, Guadalupe del Carmen
Lozano Fuentes, Saúl
Guillermo Bond, J.
Casas Martínez, Mauricio
Ramsey, Janine M.
García Rejón, Julián Everardo
Domínguez Galera, Marco Antonio
Ranson, Hilary
Hemingway, Janet
Eisen, Lars
Black, William C.
author_facet Kittayapong, Pattamaporn
Ponce García, Gustavo
Flores Suárez, Adriana Elizabeth
Fernández Salas, Ildefonso
Saavedra Rodríguez, Karla Lizet
Reyes Solis, Guadalupe del Carmen
Lozano Fuentes, Saúl
Guillermo Bond, J.
Casas Martínez, Mauricio
Ramsey, Janine M.
García Rejón, Julián Everardo
Domínguez Galera, Marco Antonio
Ranson, Hilary
Hemingway, Janet
Eisen, Lars
Black, William C.
author_sort Kittayapong, Pattamaporn
collection Repositorio Institucional
description Background: Aedes aegypti, the ‘yellow fever mosquito’, is the primary vector to humans of dengue and yellow fever flaviviruses (DENV, YFV), and is a known vector of the chikungunya alphavirus (CV). Because vaccines are not yet available for DENV or CV or are inadequately distributed in developing countries (YFV), management of Ae. aegypti remains the primary option to prevent and control outbreaks of the diseases caused by these arboviruses. Permethrin is one of the most widely used active ingredients in insecticides for suppression of adult Ae. aegypti. In 2007, we documented a replacement mutation in codon 1,016 of the voltage-gated sodium channel gene (para) of Ae. aegypti that encodes an isoleucine rather than a valine and confers resistance to permethrin. Ile1,016 segregates as a recessive allele conferring knockdown resistance to homozygous mosquitoes at 5–10 mg of permethrin in bottle bioassays. Methods and Findings: A total of 81 field collections containing 3,951 Ae. aegypti were made throughout Me´xico from 1996 to 2009. These mosquitoes were analyzed for the frequency of the Ile1,016 mutation using a melting-curve PCR assay. Dramatic increases in frequencies of Ile1,016 were recorded from the late 1990’s to 2006–2009 in several states including Nuevo Leo´n in the north, Veracruz on the central Atlantic coast, and Yucata´n, Quintana Roo and Chiapas in the south. From 1996 to 2000, the overall frequency of Ile1,016 was 0.04% (95% confidence interval (CI95) = 0.12%; n = 1,359 mosquitoes examined). The earliest detection of Ile1,016 was in Nuevo Laredo on the U.S. border in 1997. By 2003–2004 the overall frequency of Ile1,016 had increased ,100-fold to 2.7% (60.80% CI95; n = 808). When checked again in 2006, the frequency had increased slightly to 3.9% (61.15% CI95; n = 473). This was followed in 2007–2009 by a sudden jump in Ile1,016 frequency to 33.2% (61.99% CI95; n = 1,074 mosquitoes). There was spatial heterogeneity in Ile1,016 frequencies among 2007–2008 collections, which ranged from 45.7% (62.00% CI95) in the state of Veracruz to 51.2% (64.36% CI95) in the Yucata´n peninsula and 14.5% (62.23% CI95) in and around Tapachula in the state of Chiapas. Spatial heterogeneity was also evident at smaller geographic scales. For example within the city of Chetumal, Quintana Roo, Ile1,016 frequencies varied from 38.3%–88.3%. A linear regression analysis based on seven collections from 2007 revealed that the frequency of Ile1,016 homozygotes accurately predicted knockdown rate for mosquitoes exposed to permethrin in a bioassay (R2 = 0.98). Conclusions: We have recorded a dramatic increase in the frequency of the Ile1,016 mutation in the voltage-gated sodium channel gene of Ae. aegypti in Me´xico from 1996 to 2009. This may be related to heavy use of permethrin-based insecticides in mosquito control programs. Spatial heterogeneity in Ile1,016 frequencies in 2007 and 2008 collections may reflect differences in selection pressure or in the initial frequency of Ile1,016. The rapid recent increase in Ile1,016 is predicted by a simple model of positive directional selection on a recessive allele. Unfortunately this model also predicts rapid fixation of Ile1,016 unless there is negative fitness associated with Ile1,016 in the absence of permethrin. If so, then spatial refugia of susceptible Ae. aegypti or rotational schedules of different classes of adulticides could be established to slow or prevent fixation of Ile1,016.
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spelling eprints-150962021-08-20T19:55:56Z http://eprints.uanl.mx/15096/ Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México Kittayapong, Pattamaporn Ponce García, Gustavo Flores Suárez, Adriana Elizabeth Fernández Salas, Ildefonso Saavedra Rodríguez, Karla Lizet Reyes Solis, Guadalupe del Carmen Lozano Fuentes, Saúl Guillermo Bond, J. Casas Martínez, Mauricio Ramsey, Janine M. García Rejón, Julián Everardo Domínguez Galera, Marco Antonio Ranson, Hilary Hemingway, Janet Eisen, Lars Black, William C. Background: Aedes aegypti, the ‘yellow fever mosquito’, is the primary vector to humans of dengue and yellow fever flaviviruses (DENV, YFV), and is a known vector of the chikungunya alphavirus (CV). Because vaccines are not yet available for DENV or CV or are inadequately distributed in developing countries (YFV), management of Ae. aegypti remains the primary option to prevent and control outbreaks of the diseases caused by these arboviruses. Permethrin is one of the most widely used active ingredients in insecticides for suppression of adult Ae. aegypti. In 2007, we documented a replacement mutation in codon 1,016 of the voltage-gated sodium channel gene (para) of Ae. aegypti that encodes an isoleucine rather than a valine and confers resistance to permethrin. Ile1,016 segregates as a recessive allele conferring knockdown resistance to homozygous mosquitoes at 5–10 mg of permethrin in bottle bioassays. Methods and Findings: A total of 81 field collections containing 3,951 Ae. aegypti were made throughout Me´xico from 1996 to 2009. These mosquitoes were analyzed for the frequency of the Ile1,016 mutation using a melting-curve PCR assay. Dramatic increases in frequencies of Ile1,016 were recorded from the late 1990’s to 2006–2009 in several states including Nuevo Leo´n in the north, Veracruz on the central Atlantic coast, and Yucata´n, Quintana Roo and Chiapas in the south. From 1996 to 2000, the overall frequency of Ile1,016 was 0.04% (95% confidence interval (CI95) = 0.12%; n = 1,359 mosquitoes examined). The earliest detection of Ile1,016 was in Nuevo Laredo on the U.S. border in 1997. By 2003–2004 the overall frequency of Ile1,016 had increased ,100-fold to 2.7% (60.80% CI95; n = 808). When checked again in 2006, the frequency had increased slightly to 3.9% (61.15% CI95; n = 473). This was followed in 2007–2009 by a sudden jump in Ile1,016 frequency to 33.2% (61.99% CI95; n = 1,074 mosquitoes). There was spatial heterogeneity in Ile1,016 frequencies among 2007–2008 collections, which ranged from 45.7% (62.00% CI95) in the state of Veracruz to 51.2% (64.36% CI95) in the Yucata´n peninsula and 14.5% (62.23% CI95) in and around Tapachula in the state of Chiapas. Spatial heterogeneity was also evident at smaller geographic scales. For example within the city of Chetumal, Quintana Roo, Ile1,016 frequencies varied from 38.3%–88.3%. A linear regression analysis based on seven collections from 2007 revealed that the frequency of Ile1,016 homozygotes accurately predicted knockdown rate for mosquitoes exposed to permethrin in a bioassay (R2 = 0.98). Conclusions: We have recorded a dramatic increase in the frequency of the Ile1,016 mutation in the voltage-gated sodium channel gene of Ae. aegypti in Me´xico from 1996 to 2009. This may be related to heavy use of permethrin-based insecticides in mosquito control programs. Spatial heterogeneity in Ile1,016 frequencies in 2007 and 2008 collections may reflect differences in selection pressure or in the initial frequency of Ile1,016. The rapid recent increase in Ile1,016 is predicted by a simple model of positive directional selection on a recessive allele. Unfortunately this model also predicts rapid fixation of Ile1,016 unless there is negative fitness associated with Ile1,016 in the absence of permethrin. If so, then spatial refugia of susceptible Ae. aegypti or rotational schedules of different classes of adulticides could be established to slow or prevent fixation of Ile1,016. Public Library of Science 2009 Article PeerReviewed text en cc_by_nc_nd http://eprints.uanl.mx/15096/1/784.PDF http://eprints.uanl.mx/15096/1.haspreviewThumbnailVersion/784.PDF Kittayapong, Pattamaporn y Ponce García, Gustavo y Flores Suárez, Adriana Elizabeth y Fernández Salas, Ildefonso y Saavedra Rodríguez, Karla Lizet y Reyes Solis, Guadalupe del Carmen y Lozano Fuentes, Saúl y Guillermo Bond, J. y Casas Martínez, Mauricio y Ramsey, Janine M. y García Rejón, Julián Everardo y Domínguez Galera, Marco Antonio y Ranson, Hilary y Hemingway, Janet y Eisen, Lars y Black, William C. (2009) Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México. PloS Neglected tropical diseases, 3 (10). e531. ISSN 1935-2727 http://doi.org/10.1371/journal.pntd.0000531 doi:10.1371/journal.pntd.0000531
spellingShingle Kittayapong, Pattamaporn
Ponce García, Gustavo
Flores Suárez, Adriana Elizabeth
Fernández Salas, Ildefonso
Saavedra Rodríguez, Karla Lizet
Reyes Solis, Guadalupe del Carmen
Lozano Fuentes, Saúl
Guillermo Bond, J.
Casas Martínez, Mauricio
Ramsey, Janine M.
García Rejón, Julián Everardo
Domínguez Galera, Marco Antonio
Ranson, Hilary
Hemingway, Janet
Eisen, Lars
Black, William C.
Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México
thumbnail https://rediab.uanl.mx/themes/sandal5/images/online.png
title Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México
title_full Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México
title_fullStr Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México
title_full_unstemmed Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México
title_short Recent rapid rise of a permethrin knock down resistance allele in Aedes aegypti in México
title_sort recent rapid rise of a permethrin knock down resistance allele in aedes aegypti in mexico
url http://eprints.uanl.mx/15096/1/784.PDF
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