Mapping insecticide resistance and characterization of resistance mechanisms in Anopheles arabiensis (Diptera: Culicidae) in Ethiopia

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Abstract

Background

The emergence and spread of insecticide resistance in the major African malaria vectors Anopheles gambiae ( s.s.) and An. arabiensis may compromise the current vector control interventions and threatens the global malaria control and elimination efforts.

Methods

Insecticide resistance was monitored in several study sites in Ethiopia from 2013 to 2015 using papers impregnated with discriminating concentrations of DDT, deltamethrin, bendiocarb, propoxur, malathion, fenitrothion and pirimiphos-methyl, following the WHO insecticide susceptibility test procedure. Mosquitoes sampled from different localities for WHO bioassay were morphologically identified as An. gambiae ( s.l.) using standard taxonomic keys. Samples were identified to species using species-specific polymerase chain reaction (PCR) and screened for the presence of target site mutations L1014F, L1014S and N1575Y in the voltage gated sodium channel ( VGSC) gene and G119S in the acethylcholinesterase ( AChE) gene using allele-specific PCR. Biochemical assays were performed to assess elevated levels of acetylcholinesterases, carboxylcholinesterases, glutathione-S-transferases (GSTs) and cytochrome P450s monooxygenases in wild populations of An. arabiensis, compared to the fully susceptible Sekoru An. arabiensis laboratory strain.

Results

Populations of An. arabiensis were resistant to DDT and deltamethrin but were susceptible to fenitrothion in all the study sites. Reduced susceptibility to malathion, pirimiphos-methyl, propoxur and bendiocarb was observed in some of the study sites. Knockdown resistance ( kdr L1014F) was detected in all mosquito populations with allele frequency ranging from 42 to 91%. Elevated levels of glutathione-S-transferases (GSTs) were detected in some of the mosquito populations. However, no elevated levels of monooxygenases and esterases were detected in any of the populations assessed.

Conclusions

Anopheles arabiensis populations from all surveyed sites in Ethiopia exhibited resistance against DDT and pyrethroids. Moreover, some mosquito populations exhibited resistance to propoxur and possible resistance to bendiocarb. Target site mutation kdr L1014F was detected in all mosquito populations while elevated levels of glutathione-S-transferases (GSTs) was detected in some mosquito populations. The reduced susceptibility of An. arabiensis to propoxur and bendiocarb, which are currently used for indoor residual spraying (IRS) in Ethiopia, calls for continuous resistance monitoring, in order to plan and implement evidence based insecticide resistance management.

Electronic supplementary material

The online version of this article (10.1186/s13071-017-2342-y) contains supplementary material, which is available to authorized users.

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Most cited references 47

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Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids.

H Ranson, B. Jensen, J. Vulule … (2000)

A field trial of permethrin-impregnated bednets and curtains was initiated in Western Kenya in 1990, and a strain of Anopheles gambiae showing reduced susceptibility to permethrin was colonized from this site in 1992. A leucine-phenylalanine substitution at position 1014 of the voltage-gated sodium channel is associated with resistance to permethrin and DDT in many insect species, including Anopheles gambiae from West Africa. We cloned and sequenced a partial sodium channel cDNA from the Kenyan permethrin-resistant strain and we identified an alternative substitution (leucine to serine) at the same position, which is linked to the inheritance of permethrin resistance in the F(2) progeny of genetic crosses between susceptible and resistant individuals. The diagnostic polymerase chain reaction (PCR) developed by Martinez-Torres et al. [(1998) Insect Mol Biol 7: 179-184] to detect kdr alleles in field populations of An. gambiae will not detect the Kenyan allele and hence reliance on this assay may lead to an underestimate of the prevalence of pyrethroid resistance in this species. We adapted the diagnostic PCR to detect the leucine-serine mutation and with this diagnostic we were able to demonstrate that this kdr allele was present in individuals collected from the Kenyan trial site in 1986, prior to the introduction of pyrethroid-impregnated bednets. The An. gambiae sodium channel was physically mapped to chromosome 2L, division 20C. This position corresponds to the location of a major quantitative trait locus determining resistance to permethrin in the Kenyan strain of An. gambiae.

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The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors.

M Weill, C. Malcolm, F. Chandre … (2004)

High insecticide resistance resulting from insensitive acetylcholinesterase (AChE) has emerged in mosquitoes. A single mutation (G119S of the ace-1 gene) explains this high resistance in Culex pipiens and in Anopheles gambiae. In order to provide better documentation of the ace-1 gene and the effect of the G119S mutation, we present a three-dimension structure model of AChE, showing that this unique substitution is localized in the oxyanion hole, explaining the insecticide insensitivity and its interference with the enzyme catalytic functions. As the G119S creates a restriction site, a simple PCR test was devised to detect its presence in both A. gambiae and C. pipiens, two mosquito species belonging to different subfamilies (Culicinae and Anophelinae). It is possibile that this mutation also explains the high resistance found in other mosquitoes, and the present results indicate that the PCR test detects the G119S mutation in the malaria vector A. albimanus. The G119S has thus occurred independently at least four times in mosquitoes and this PCR test is probably of broad applicability within the Culicidae family.

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Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem

Hilary Ranson, Hiba Abdallah, Athanase Badolo … (2009)

Background Insecticide resistance in malaria vectors is a growing concern in many countries which requires immediate attention because of the limited chemical arsenal available for vector control. The current extent and distribution of this resistance in many parts of the continent is unknown and yet such information is essential for the planning of effective malaria control interventions. Methods In 2008, a network was established, with financial support from WHO/TDR, to investigate the extent of insecticide resistance in malaria vectors in five African countries. Here, the results of bioassays on Anopheles gambiae sensu lato from two rounds of monitoring from 12 sentinel sites in three of the partner countries are reported. Results Resistance is very heterogeneous even over relatively small distances. Furthermore, in some sites, large differences in mortality rates were observed during the course of the malaria transmission season. Using WHO diagnostic doses, all populations from Burkina Faso and Chad and two of the four populations from Sudan were classified as resistant to permethrin and/or deltamethrin. Very high frequencies of DDT resistance were found in urban areas in Burkina Faso and Sudan and in a cotton-growing district in Chad. In areas where both An. gambiae s.s. and Anopheles arabiensis were present, resistance was found in both species, although generally at a higher frequency in An gambiae s.s. Anopheles gambiae s.l. remains largely susceptible to the organophosphate fenitrothion and the carbamate bendiocarb in the majority of the sentinel sites with the exception of two sites in Burkina Faso. In the cotton-growing region of Soumousso in Burkina Faso, the vector population is resistant to all four classes of insecticide available for malaria control. Conclusions Possible factors influencing the frequency of resistant individuals observed in the sentinel sites are discussed. The results of this study highlight the importance of standardized longitudinal insecticide resistance monitoring and the urgent need for studies to monitor the impact of this resistance on malaria vector control activities.

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Author and article information

Contributors

Eba Alemayehu: ebasimma@yahoo.com

Abebe Asale: abebea663@gmail.com

Kasahun Eba: kasahun.eba@ju.edu.et

Kefelegn Getahun: kefelegn.getahun@ju.edu.et

Kora Tushune: kora.tushune@ju.edu.et

Astrid Bryon: astrid.bryon@ugent.be

Evangelia Morou: evangelia.morou@liverpool.ac.uk

John Vontas: vontas@imbb.forth.gr

Thomas Van Leeuwen: thomas.vanleeuwen@ugent.be

Luc Duchateau: luc.duchateau@ugent.be

Delenasaw Yewhalaw: delenasawye@yahoo.com

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 2 September 2017

Publication date PMC-release: 2 September 2017

Publication date Collection: 2017

Volume: 10

Electronic Location Identifier: 407

Affiliations

[1 ]ISNI 0000 0001 2034 9160, GRID grid.411903.e, Department of Biology, College of Natural Sciences, , Jimma University, ; Jimma, Ethiopia

[2 ]ISNI 0000 0001 2034 9160, GRID grid.411903.e, Tropical and Infectious Diseases Research Center, Jimma University, ; Jimma, Ethiopia

[3 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Comparative Physiology and Biometrics, , University of Ghent, ; Ghent, Belgium

[4 ]ISNI 0000 0001 2034 9160, GRID grid.411903.e, Department of Geography and Environmental Studies, , Jimma University, ; Jimma, Ethiopia

[5 ]ISNI 0000 0001 2034 9160, GRID grid.411903.e, Department of Health Services Management, College of Health Sciences, , Jimma University, ; Jimma, Ethiopia

[6 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Crop Protection, , Ghent University, ; Ghent, Belgium

[7 ]ISNI 0000 0004 0576 3437, GRID grid.8127.c, Department of Biology, , University of Crete, ; Heraklion, Greece

[8 ]ISNI 0000 0004 0635 685X, GRID grid.4834.b, Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, ; Heraklion, Greece

[9 ]ISNI 0000 0001 0794 1186, GRID grid.10985.35, Department of Crop Science, Pesticide Science Lab, , Agricultural University of Athens, ; Athens, Greece

[10 ]ISNI 0000000084992262, GRID grid.7177.6, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, ; Amsterdam, The Netherlands

[11 ]ISNI 0000 0001 2034 9160, GRID grid.411903.e, Department of Medical Laboratory Sciences and Pathology, College of Health Sciences, , Jimma University, ; Jimma, Ethiopia

Article

Publisher ID: 2342

DOI: 10.1186/s13071-017-2342-y

PMC ID: 5581456

PubMed ID: 28865490

SO-VID: d8106272-1d4e-4d79-a014-71890a205968

License:

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.

History

Date received : 4 August 2016

Date accepted : 22 August 2017

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: malaria,insecticide resistance,anopheles arabiensis,resistance mechanisms,vector control,ethiopia

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ScienceOpen disciplines: Parasitology

Keywords: malaria, insecticide resistance, anopheles arabiensis, resistance mechanisms, vector control, ethiopia

Mapping insecticide resistance and characterization of resistance mechanisms in Anopheles arabiensis (Diptera: Culicidae) in Ethiopia

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Results

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Malaria vaccine development

Most cited references 47

Identification of a point mutation in the voltage-gated sodium channel gene of Kenyan Anopheles gambiae associated with resistance to DDT and pyrethroids.

The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors.

Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem

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