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Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana

BACKGROUND: Aggravation of insecticide resistance in malaria vectors is threatening the efforts to control malaria by reducing the efficacy of insecticide-based interventions hence needs to be closely monitored. This study investigated the intensity of insecticide resistance of two major malaria vec...

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Autores principales: Mugenzi, Leon M. J., Akosah-Brempong, Gabriel, Tchouakui, Magellan, Menze, Benjamin D., Tekoh, Theofelix A., Tchoupo, Micareme, Nkemngo, Francis N., Wondji, Murielle J., Nwaefuna, Ekene K., 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/PMC9597992/
https://www.ncbi.nlm.nih.gov/pubmed/36284278
http://dx.doi.org/10.1186/s12879-022-07795-4
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author Mugenzi, Leon M. J.
Akosah-Brempong, Gabriel
Tchouakui, Magellan
Menze, Benjamin D.
Tekoh, Theofelix A.
Tchoupo, Micareme
Nkemngo, Francis N.
Wondji, Murielle J.
Nwaefuna, Ekene K.
Osae, Michael
Wondji, Charles S.
author_facet Mugenzi, Leon M. J.
Akosah-Brempong, Gabriel
Tchouakui, Magellan
Menze, Benjamin D.
Tekoh, Theofelix A.
Tchoupo, Micareme
Nkemngo, Francis N.
Wondji, Murielle J.
Nwaefuna, Ekene K.
Osae, Michael
Wondji, Charles S.
author_sort Mugenzi, Leon M. J.
collection PubMed
description BACKGROUND: Aggravation of insecticide resistance in malaria vectors is threatening the efforts to control malaria by reducing the efficacy of insecticide-based interventions hence needs to be closely monitored. This study investigated the intensity of insecticide resistance of two major malaria vectors An. funestus sensu stricto (s.s.) and An. gambiae sensu lato (s.l.) collected in southern Ghana and assessed the bio-efficacy of several long-lasting insecticidal nets (LLINs) against these mosquito populations. METHODS: The insecticide susceptibility profiles of Anopheles funestus s.s. and Anopheles gambiae s.l. populations from Obuasi region (Atatam), southern Ghana were characterized and the bio-efficacy of some LLINs was assessed to determine the impact of insecticide resistance on the effectiveness of these tools. Furthermore, molecular markers associated with insecticide resistance in both species were characterized in the F(0) and F(1) populations using PCR and qPCR methods. RESULTS: Anopheles funestus s.s. was the predominant species and was resistant to pyrethroids, organochlorine and carbamate insecticides, but fully susceptible to organophosphates. An. gambiae s.l. was resistant to all four insecticide classes. High intensity of resistance to 5 × and 10 × the discriminating concentration (DC) of pyrethroids was observed in both species inducing a considerable loss of efficacy of long-lasting insecticidal nets (LLINs). Temporal expression analysis revealed a massive 12-fold increase in expression of the CYP6P4a cytochrome P450 gene in An. funestus s.s., initially from a fold change of 41 (2014) to 500 (2021). For both species, the expression of candidate genes did not vary according to discriminating doses. An. gambiae s.l. exhibited high frequencies of target-site resistance including Vgsc-1014F (90%) and Ace-1 (50%) while these mutations were absent in An. funestus s.s. CONCLUSIONS: The multiple and high intensity of resistance observed in both malaria vectors highlights the need to implement resistance management strategies and the introduction of new insecticide chemistries. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12879-022-07795-4.
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spelling pubmed-95979922022-10-27 Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana Mugenzi, Leon M. J. Akosah-Brempong, Gabriel Tchouakui, Magellan Menze, Benjamin D. Tekoh, Theofelix A. Tchoupo, Micareme Nkemngo, Francis N. Wondji, Murielle J. Nwaefuna, Ekene K. Osae, Michael Wondji, Charles S. BMC Infect Dis Research BACKGROUND: Aggravation of insecticide resistance in malaria vectors is threatening the efforts to control malaria by reducing the efficacy of insecticide-based interventions hence needs to be closely monitored. This study investigated the intensity of insecticide resistance of two major malaria vectors An. funestus sensu stricto (s.s.) and An. gambiae sensu lato (s.l.) collected in southern Ghana and assessed the bio-efficacy of several long-lasting insecticidal nets (LLINs) against these mosquito populations. METHODS: The insecticide susceptibility profiles of Anopheles funestus s.s. and Anopheles gambiae s.l. populations from Obuasi region (Atatam), southern Ghana were characterized and the bio-efficacy of some LLINs was assessed to determine the impact of insecticide resistance on the effectiveness of these tools. Furthermore, molecular markers associated with insecticide resistance in both species were characterized in the F(0) and F(1) populations using PCR and qPCR methods. RESULTS: Anopheles funestus s.s. was the predominant species and was resistant to pyrethroids, organochlorine and carbamate insecticides, but fully susceptible to organophosphates. An. gambiae s.l. was resistant to all four insecticide classes. High intensity of resistance to 5 × and 10 × the discriminating concentration (DC) of pyrethroids was observed in both species inducing a considerable loss of efficacy of long-lasting insecticidal nets (LLINs). Temporal expression analysis revealed a massive 12-fold increase in expression of the CYP6P4a cytochrome P450 gene in An. funestus s.s., initially from a fold change of 41 (2014) to 500 (2021). For both species, the expression of candidate genes did not vary according to discriminating doses. An. gambiae s.l. exhibited high frequencies of target-site resistance including Vgsc-1014F (90%) and Ace-1 (50%) while these mutations were absent in An. funestus s.s. CONCLUSIONS: The multiple and high intensity of resistance observed in both malaria vectors highlights the need to implement resistance management strategies and the introduction of new insecticide chemistries. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12879-022-07795-4. BioMed Central 2022-10-25 /pmc/articles/PMC9597992/ /pubmed/36284278 http://dx.doi.org/10.1186/s12879-022-07795-4 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
Mugenzi, Leon M. J.
Akosah-Brempong, Gabriel
Tchouakui, Magellan
Menze, Benjamin D.
Tekoh, Theofelix A.
Tchoupo, Micareme
Nkemngo, Francis N.
Wondji, Murielle J.
Nwaefuna, Ekene K.
Osae, Michael
Wondji, Charles S.
Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana
title Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana
title_full Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana
title_fullStr Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana
title_full_unstemmed Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana
title_short Escalating pyrethroid resistance in two major malaria vectors Anopheles funestus and Anopheles gambiae (s.l.) in Atatam, Southern Ghana
title_sort escalating pyrethroid resistance in two major malaria vectors anopheles funestus and anopheles gambiae (s.l.) in atatam, southern ghana
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9597992/
https://www.ncbi.nlm.nih.gov/pubmed/36284278
http://dx.doi.org/10.1186/s12879-022-07795-4
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