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      Multiple Insecticide Resistance: An Impediment to Insecticide-Based Malaria Vector Control Program

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          Abstract

          Background

          Indoor Residual Spraying (IRS), insecticide-treated nets (ITNs) and long-lasting insecticidal nets (LLINs) are key components in malaria prevention and control strategy. However, the development of resistance by mosquitoes to insecticides recommended for IRS and/or ITNs/LLINs would affect insecticide-based malaria vector control. We assessed the susceptibility levels of Anopheles arabiensis to insecticides used in malaria control, characterized basic mechanisms underlying resistance, and evaluated the role of public health use of insecticides in resistance selection.

          Methodology/Principal findings

          Susceptibility status of An. arabiensis was assessed using WHO bioassay tests to DDT, permethrin, deltamethrin, malathion and propoxur in Ethiopia from August to September 2009. Mosquito specimens were screened for knockdown resistance ( kdr) and insensitive acetylcholinesterase (ace-1 R) mutations using AS-PCR and PCR-RFLP, respectively. DDT residues level in soil from human dwellings and the surrounding environment were determined by Gas Chromatography with Electron Capture Detector. An. arabiensis was resistant to DDT, permethrin, deltamethrin and malathion, but susceptible to propoxur. The West African kdr allele was found in 280 specimens out of 284 with a frequency ranged from 95% to 100%. Ace-1 R mutation was not detected in all specimens scored for the allele. Moreover, DDT residues were found in soil samples from human dwellings but not in the surrounding environment.

          Conclusion

          The observed multiple-resistance coupled with the occurrence of high kdr frequency in populations of An. arabiensis could profoundly affect the malaria vector control programme in Ethiopia. This needs an urgent call for implementing rational resistance management strategies and integrated vector control intervention.

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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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              A ribosomal RNA gene probe differentiates member species of the Anopheles gambiae complex.

              F Collins, M. A. Mendez, M. O. Rasmussen … (1987)
              A 0.59 kilobase DNA fragment cloned from an rDNA cistron of the mosquito Anopheles gambiae can be used as a probe to differentiate between A. gambiae, A. arabiensis, and A. melas, three morphologically identical sibling species in the A. gambiae complex which otherwise can be reliably distinguished only by polytene chromosome banding patterns. Although all are important (and often sympatric) African malaria vectors, their relative roles in malaria transmission have thus far been difficult to assess. The probe, an EcoRI-SalI fragment from the 3' end of the 28S beta coding region of the cistron, is present in all three species, but the species differ uniquely with respect to the location of an EcoRI site in the nontranscribed spacer (NTS) downstream of the fragment. We have routinely used the probe to identify A. gambiae complex mosquitoes to species on the basis of genomic DNA extracted from individual air dried specimens. A single mosquito abdomen provides more than sufficient DNA for the assay, and neither eggs nor a bloodmeal in the abdomen interfere with DNA yield. Moreover, the DNA extraction procedure does not degrade the bloodmeal IgG, so the residual protein pellet can be used to identify the mosquito bloodmeal source. Since the rDNA cistron organization as detected by the probe does not differ between male and female mosquitoes, the probe can be used for either sex. Preliminary experiments show that the probe is equally useful for mosquito larvae and pupae.
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2011
                Publication date (Electronic): 12 January 2011
                Volume: 6
                Issue: 1
                Electronic Location Identifier: e16066
                Affiliations
                [1 ]Department of Biology, Jimma University, Jimma, Ethiopia
                [2 ]Department of Environmental Health, Jimma University, Jimma, Ethiopia
                [3 ]Department of Chemistry, Jimma University, Jimma, Ethiopia
                [4 ]Department of Plant Science, Jimma University, Jimma, Ethiopia
                [5 ]Department of Crop Protection Chemistry, Ghent University, Ghent, Belgium
                [6 ]Department of Parasitology, Institute of Tropical Medicine, Antwerp, Belgium
                [7 ]Department of Physiology and Biometrics, Ghent University, Ghent, Belgium
                [8 ]Institute for Health and Society, Public Health School, Université Catholique de Louvain, Brussels, Belgium
                New Mexico State University, United States of America
                Author notes

                Conceived and designed the experiments: DY FW. Performed the experiments: L. Denis. Analyzed the data: YG WS PS L. Duchateau NS. Wrote the paper: DY FW. Critically reviewed the manuscript: WVB MC DAT.

                Article
                Publisher ID: PONE-D-10-01626
                DOI: 10.1371/journal.pone.0016066
                PMC ID: 3020220
                PubMed ID: 21264325
                SO-VID: 1b8def8c-2696-4836-9491-e16b4a3c0483
                Copyright © Yewhalaw et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                Date received : 10 September 2010
                Date accepted : 6 December 2010
                Page count
                Pages: 7
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Microbiology
                Subject: Vector Biology
                Subject: Anopheles
                Subject: Mosquitoes
                Subject: Population Biology
                Subject: Population Genetics
                Subject: Mutation
                Subject: Zoology
                Subject: Entomology
                Subject: Parasitology
                Subject: Medicine
                Subject: Epidemiology
                Subject: Infectious Disease Epidemiology
                Subject: Infectious Diseases
                Subject: Parasitic Diseases
                Subject: Malaria
                Subject: Plasmodium Falciparum
                Subject: Plasmodium Vivax
                Subject: Leishmaniasis
                Subject: Lymphatic Filariasis
                Subject: Onchocerciasis
                Subject: Protozoan Infections
                Subject: Schistosomiasis
                Subject: Soil-Transmitted Helminths
                Subject: Infectious Disease Control
                Subject: Vectors and Hosts
                Subject: Public Health
                Subject: Disease Ecology
                Subject: Environmental Health
                Subject: Toxicology
                Subject: Toxic Agents

                ScienceOpen disciplines: Uncategorized
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                ScienceOpen disciplines: Uncategorized

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