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Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa

BACKGROUND: New insecticides with a novel mode of action such as neonicotinoids have recently been recommended for public health by WHO. Resistance monitoring of such novel insecticides requires a robust protocol to monitor the development of resistance in natural populations. In this study, we comp...

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Autores principales: Tchouakui, Magellan, Assatse, Tatiane, Mugenzi, Leon M. J., Menze, Benjamin D., Nguiffo-Nguete, Daniel, Tchapga, Williams, Kayondo, Jonathan, Watsenga, Francis, Manzambi, Emile Zola, Osae, Michael, Wondji, Charles S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9036736/
https://www.ncbi.nlm.nih.gov/pubmed/35462556
http://dx.doi.org/10.1186/s40249-022-00962-4
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author Tchouakui, Magellan
Assatse, Tatiane
Mugenzi, Leon M. J.
Menze, Benjamin D.
Nguiffo-Nguete, Daniel
Tchapga, Williams
Kayondo, Jonathan
Watsenga, Francis
Manzambi, Emile Zola
Osae, Michael
Wondji, Charles S.
author_facet Tchouakui, Magellan
Assatse, Tatiane
Mugenzi, Leon M. J.
Menze, Benjamin D.
Nguiffo-Nguete, Daniel
Tchapga, Williams
Kayondo, Jonathan
Watsenga, Francis
Manzambi, Emile Zola
Osae, Michael
Wondji, Charles S.
author_sort Tchouakui, Magellan
collection PubMed
description BACKGROUND: New insecticides with a novel mode of action such as neonicotinoids have recently been recommended for public health by WHO. Resistance monitoring of such novel insecticides requires a robust protocol to monitor the development of resistance in natural populations. In this study, we comparatively used three different solvents to assess the susceptibility of malaria vectors to neonicotinoids across Africa. METHODS: Mosquitoes were collected from May to July 2021 from three agricultural settings in Cameroon (Njombe-Penja, Nkolondom, and Mangoum), the Democratic Republic of Congo (Ndjili-Brasserie), Ghana (Obuasi), and Uganda (Mayuge). Using the CDC bottle test, we compared the effect of three different solvents (ethanol, acetone, MERO) on the efficacy of neonicotinoids against Anopheles gambiae s.l. In addition, TaqMan assays were used to genotype key pyrethroid-resistant markers in An. gambiae and odds ratio based on Fisher exact test were used to evaluate potential cross-resistance between pyrethroids and clothianidin. RESULTS: Lower mortality was observed when using absolute ethanol or acetone alone as solvent for clothianidin (11.4‒51.9% mortality in Nkolondom, 31.7‒48.2% in Mangoum, 34.6‒56.1% in Mayuge, 39.4‒45.6% in Obuasi, 83.7‒89.3% in Congo and 71.1‒95.9% in Njombe pendja) compared to acetone + MERO for which 100% mortality were observed for all the populations. Similar observations were done for imidacloprid and acetamiprid. Synergist assays (PBO, DEM and DEF) with clothianidin revealed a significant increase of mortality suggesting that metabolic resistance mechanisms are contributing to the reduced susceptibility. A negative association was observed between the L1014F-kdr mutation and clothianidin resistance with a greater frequency of homozygote resistant mosquitoes among the dead than among survivors (OR = 0.5; P = 0.02). However, the I114T-GSTe2 was in contrast significantly associated with a greater ability to survive clothianidin with a higher frequency of homozygote resistant among survivors than other genotypes (OR = 2.10; P = 0.013). CONCLUSIONS: This study revealed a contrasted susceptibility pattern depending on the solvents with ethanol/acetone resulting to lower mortality, thus possibly overestimating resistance, whereas the MERO consistently showed a greater efficacy of neonicotinoids but it could prevent to detect early resistance development. Therefore, we recommend monitoring the susceptibility using both acetone alone and acetone + MERO (4 µg/ml for clothianidin) to capture the accurate resistance profile of the mosquito populations. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-022-00962-4.
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spelling pubmed-90367362022-04-26 Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa Tchouakui, Magellan Assatse, Tatiane Mugenzi, Leon M. J. Menze, Benjamin D. Nguiffo-Nguete, Daniel Tchapga, Williams Kayondo, Jonathan Watsenga, Francis Manzambi, Emile Zola Osae, Michael Wondji, Charles S. Infect Dis Poverty Research Article BACKGROUND: New insecticides with a novel mode of action such as neonicotinoids have recently been recommended for public health by WHO. Resistance monitoring of such novel insecticides requires a robust protocol to monitor the development of resistance in natural populations. In this study, we comparatively used three different solvents to assess the susceptibility of malaria vectors to neonicotinoids across Africa. METHODS: Mosquitoes were collected from May to July 2021 from three agricultural settings in Cameroon (Njombe-Penja, Nkolondom, and Mangoum), the Democratic Republic of Congo (Ndjili-Brasserie), Ghana (Obuasi), and Uganda (Mayuge). Using the CDC bottle test, we compared the effect of three different solvents (ethanol, acetone, MERO) on the efficacy of neonicotinoids against Anopheles gambiae s.l. In addition, TaqMan assays were used to genotype key pyrethroid-resistant markers in An. gambiae and odds ratio based on Fisher exact test were used to evaluate potential cross-resistance between pyrethroids and clothianidin. RESULTS: Lower mortality was observed when using absolute ethanol or acetone alone as solvent for clothianidin (11.4‒51.9% mortality in Nkolondom, 31.7‒48.2% in Mangoum, 34.6‒56.1% in Mayuge, 39.4‒45.6% in Obuasi, 83.7‒89.3% in Congo and 71.1‒95.9% in Njombe pendja) compared to acetone + MERO for which 100% mortality were observed for all the populations. Similar observations were done for imidacloprid and acetamiprid. Synergist assays (PBO, DEM and DEF) with clothianidin revealed a significant increase of mortality suggesting that metabolic resistance mechanisms are contributing to the reduced susceptibility. A negative association was observed between the L1014F-kdr mutation and clothianidin resistance with a greater frequency of homozygote resistant mosquitoes among the dead than among survivors (OR = 0.5; P = 0.02). However, the I114T-GSTe2 was in contrast significantly associated with a greater ability to survive clothianidin with a higher frequency of homozygote resistant among survivors than other genotypes (OR = 2.10; P = 0.013). CONCLUSIONS: This study revealed a contrasted susceptibility pattern depending on the solvents with ethanol/acetone resulting to lower mortality, thus possibly overestimating resistance, whereas the MERO consistently showed a greater efficacy of neonicotinoids but it could prevent to detect early resistance development. Therefore, we recommend monitoring the susceptibility using both acetone alone and acetone + MERO (4 µg/ml for clothianidin) to capture the accurate resistance profile of the mosquito populations. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40249-022-00962-4. BioMed Central 2022-04-25 /pmc/articles/PMC9036736/ /pubmed/35462556 http://dx.doi.org/10.1186/s40249-022-00962-4 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Tchouakui, Magellan
Assatse, Tatiane
Mugenzi, Leon M. J.
Menze, Benjamin D.
Nguiffo-Nguete, Daniel
Tchapga, Williams
Kayondo, Jonathan
Watsenga, Francis
Manzambi, Emile Zola
Osae, Michael
Wondji, Charles S.
Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa
title Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa
title_full Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa
title_fullStr Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa
title_full_unstemmed Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa
title_short Comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across Africa
title_sort comparative study of the effect of solvents on the efficacy of neonicotinoid insecticides against malaria vector populations across africa
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9036736/
https://www.ncbi.nlm.nih.gov/pubmed/35462556
http://dx.doi.org/10.1186/s40249-022-00962-4
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