Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania

Abstract Background Long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in...

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Main Authors: Polius G. Pinda, Claudia Eichenberger, Halfan S. Ngowo, Dickson S. Msaky, Said Abbasi, Japhet Kihonda, Hamis Bwanaly, Fredros O. Okumu
Format: Article
Language:English
Published: BMC 2020-11-01
Series:Malaria Journal
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12936-020-03483-3
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author Polius G. Pinda
Claudia Eichenberger
Halfan S. Ngowo
Dickson S. Msaky
Said Abbasi
Japhet Kihonda
Hamis Bwanaly
Fredros O. Okumu
author_facet Polius G. Pinda
Claudia Eichenberger
Halfan S. Ngowo
Dickson S. Msaky
Said Abbasi
Japhet Kihonda
Hamis Bwanaly
Fredros O. Okumu
author_sort Polius G. Pinda
collection DOAJ
description Abstract Background Long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in > 80% of malaria infections, even in villages where the species occurs at lower densities than the other vector, Anopheles arabiensis. This study compared the insecticide resistance phenotypes between the two malaria vectors in an area where pyrethroid-LLINs are widely used. Methods The study used the World Health Organization (WHO) assays with 1×, 5× and 10× insecticide doses to assess levels of resistance, followed by synergist bioassays to understand possible mechanisms of the observed resistance phenotypes. The tests involved adult mosquitoes collected from three villages across two districts in south-eastern Tanzania and included four insecticide classes. Findings At baseline doses (1×), both species were resistant to the two candidate pyrethroids (permethrin and deltamethrin), but susceptible to the organophosphate (pirimiphos-methyl). Anopheles funestus, but not An. arabiensis was also resistant to the carbamate (bendiocarb). Both species were resistant to DDT in all villages except in one village where An. arabiensis was susceptible. Anopheles funestus showed strong resistance to pyrethroids, surviving the 5× and 10× doses, while An. arabiensis reverted to susceptibility at the 5× dose. Pre-exposure to the synergist, piperonyl butoxide (PBO), enhanced the potency of the pyrethroids against both species and resulted in full susceptibility of An. arabiensis (> 98% mortality). However, for An. funestus from two villages, permethrin-associated mortalities after pre-exposure to PBO only exceeded 90% but not 98%. Conclusions In south-eastern Tanzania, where An. funestus dominates malaria transmission, the species also has much stronger resistance to pyrethroids than its counterpart, An. arabiensis, and can survive more classes of insecticides. The pyrethroid resistance in both species appears to be mostly metabolic and may be partially addressed using synergists, e.g. PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and inform new intervention choices for such settings. In short and medium-term, these may include PBO-based LLINs or improved IRS with compounds to which the vectors are still susceptible.
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spelling doaj.art-788f6e5722044d968aee9cc9c348e3172022-12-21T23:57:41ZengBMCMalaria Journal1475-28752020-11-0119111110.1186/s12936-020-03483-3Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern TanzaniaPolius G. Pinda0Claudia Eichenberger1Halfan S. Ngowo2Dickson S. Msaky3Said Abbasi4Japhet Kihonda5Hamis Bwanaly6Fredros O. Okumu7Environmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteEnvironmental Health and Ecological Sciences Department, Ifakara Health InstituteAbstract Background Long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in > 80% of malaria infections, even in villages where the species occurs at lower densities than the other vector, Anopheles arabiensis. This study compared the insecticide resistance phenotypes between the two malaria vectors in an area where pyrethroid-LLINs are widely used. Methods The study used the World Health Organization (WHO) assays with 1×, 5× and 10× insecticide doses to assess levels of resistance, followed by synergist bioassays to understand possible mechanisms of the observed resistance phenotypes. The tests involved adult mosquitoes collected from three villages across two districts in south-eastern Tanzania and included four insecticide classes. Findings At baseline doses (1×), both species were resistant to the two candidate pyrethroids (permethrin and deltamethrin), but susceptible to the organophosphate (pirimiphos-methyl). Anopheles funestus, but not An. arabiensis was also resistant to the carbamate (bendiocarb). Both species were resistant to DDT in all villages except in one village where An. arabiensis was susceptible. Anopheles funestus showed strong resistance to pyrethroids, surviving the 5× and 10× doses, while An. arabiensis reverted to susceptibility at the 5× dose. Pre-exposure to the synergist, piperonyl butoxide (PBO), enhanced the potency of the pyrethroids against both species and resulted in full susceptibility of An. arabiensis (> 98% mortality). However, for An. funestus from two villages, permethrin-associated mortalities after pre-exposure to PBO only exceeded 90% but not 98%. Conclusions In south-eastern Tanzania, where An. funestus dominates malaria transmission, the species also has much stronger resistance to pyrethroids than its counterpart, An. arabiensis, and can survive more classes of insecticides. The pyrethroid resistance in both species appears to be mostly metabolic and may be partially addressed using synergists, e.g. PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and inform new intervention choices for such settings. In short and medium-term, these may include PBO-based LLINs or improved IRS with compounds to which the vectors are still susceptible.http://link.springer.com/article/10.1186/s12936-020-03483-3Insecticide resistanceAnopheles funestusPBOIfakara health instituteTanzania
spellingShingle Polius G. Pinda
Claudia Eichenberger
Halfan S. Ngowo
Dickson S. Msaky
Said Abbasi
Japhet Kihonda
Hamis Bwanaly
Fredros O. Okumu
Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania
Malaria Journal
Insecticide resistance
Anopheles funestus
PBO
Ifakara health institute
Tanzania
title Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania
title_full Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania
title_fullStr Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania
title_full_unstemmed Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania
title_short Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania
title_sort comparative assessment of insecticide resistance phenotypes in two major malaria vectors anopheles funestus and anopheles arabiensis in south eastern tanzania
topic Insecticide resistance
Anopheles funestus
PBO
Ifakara health institute
Tanzania
url http://link.springer.com/article/10.1186/s12936-020-03483-3
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