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      Insecticidal decay effects of long-lasting insecticide nets and indoor residual spraying on Anopheles gambiae and Anopheles arabiensis in Western Kenya

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          Abstract

          Background

          Indoor residual spraying (IRS) and long-lasting insecticidal nets (LLINs) are the first-line tools for malaria prevention and control in Africa. Vector resistance to insecticides has been extensively studied, however the insecticidal effects of the nets and sprayed walls on pyrethroid resistant mosquitoes has not been studied thoroughly. We evaluated the bioefficacy of LLINs of different ages and lambda-cyhalothrin (ICON 10cs) on the sprayed mud walls for a period of time on malaria vector survivorship.

          Methods

          WHO tube bioassay was performed using diagnostic doses of lambda-cyhalothrin (0.05 %), permethrin (0.75 %) and deltamethrin (0.05 %). Cone bioassays were conducted on netting materials from 0 to 3 years old long-lasting insecticide-impregnated nets. Wall bioassays were performed monthly on mud slabs sprayed with lambdacyhalothrin over a period of seven months. All bioassays used An. gambiae mosquitoes collected from the field and the laboratory susceptible reference Kisumu strain. Concentration of the insecticides on the netting materials was examined using the gas chromatography method. Mosquitoes were identified to species level using PCR and genotyped for the kdr gene mutation frequencies.

          Results

          WHO bioassays results showed that populations from five sites were highly resistant to the pyrethroids (mortalities ranged from 52.5 to 75.3 %), and two sites were moderately resistant to these insecticides (80.4 – 87.2 %). Homozygote kdr mutations of L1014S ranged from 73 to 88 % in An. gambiae s.s. dominant populations whereas L1014S mutation frequencies were relatively low (7–31 %) in An. arabiensis dominant populations. There was a significant decrease ( P < 0.05) in mosquito mortality with time after the spray with both lambda-cyhalothrin (75 % mortality after six months) and with the age of LLINs (60 % mortality after 24 month). Field collected mosquitoes were able to survive exposure to both IRS and LLINs even with newly sprayed walls (86.6–93.5 % mortality) and new LLINs (77.5–85.0 % mortality), Wild mosquitoes collected from the field had significantly lower mortality rates to LLINs (59.6–85.0 %) than laboratory reared susceptible strain (100 %). Insecticide concentration decreased significantly from 0.14 μg/ml in the new nets to 0.077 μg/ml in nets older than 18 months ( P < 0.05).

          Conclusion

          This study confirms that insecticide decay and developing levels of resistance have a negative contribution to reduced efficacy of ITN and IRS in western Kenya. These factors contribute to decreased efficacy of pyrethroid insectides in ongoing malaria control programs. In order to mitigate against the impact of insecticide resistance and decay it is important to follow the WHO policy to provide the residents with new LLINs every three years of use while maintaining a high level of LLINs coverage and usage. There is also need for urgent development and deployment of non-pyrethroid based vector control tools.

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          Most cited references56

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          Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction.

          A ribosomal DNA-polymerase chain reaction (PCR) method has been developed for species identification of individuals of the five most widespread members of the Anopheles gambiae complex, a group of morphologically indistinguishable sibling mosquito species that includes the major vectors of malaria in Africa. The method, which is based on species-specific nucleotide sequences in the ribosomal DNA intergenic spacers, may be used to identify both species and interspecies hybrids, regardless of life stage, using either extracted DNA or fragments of a specimen. Intact portions of a mosquito as small as an egg or the segment of one leg may be placed directly into the PCR mixture for amplification and analysis. The method uses a cocktail of five 20-base oligonucleotides to identify An. gambiae, An. arabiensis, An. quadriannnulatus, and either An. melas in western Africa or An. melas in eastern and southern Africa.
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            Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province, Kenya

            Background High coverage of insecticide-treated bed nets in Asembo and low coverage in Seme, two adjacent communities in western Nyanza Province, Kenya; followed by expanded coverage of bed nets in Seme, as the Kenya national malaria programme rolled out; provided a natural experiment for quantification of changes in relative abundance of two primary malaria vectors in this holoendemic region. Both belong to the Anopheles gambiae sensu lato (s.l.) species complex, namely A. gambiae sensu stricto (s.s.) and Anopheles arabiensis. Historically, the former species was proportionately dominant in indoor resting collections of females. Methods Data of the relative abundance of adult A. gambiae s.s. and A. arabiensis sampled from inside houses were obtained from the literature from 1970 to 2002 for sites west of Kisumu, Kenya, to the region of Asembo ca. 50 km from the city. A sampling transect was established from Asembo (where bed net use was high due to presence of a managed bed net distribution programme) eastward to Seme, where no bed net programme was in place. Adults of A. gambiae s.l. were sampled from inside houses along the transect from 2003 to 2009, as were larvae from nearby aquatic habitats, providing data over a nearly 40 year period of the relative abundance of the two species. Relative proportions of A. gambiae s.s. and A. arabiensis were determined for each stage by identifying species by the polymerase chain reaction method. Household bed net ownership was measured with surveys during mosquito collections. Data of blood host choice, parity rate, and infection rate for Plasmodium falciparum in A. gambiae s.s. and A. arabiensis were obtained for a sample from Asembo and Seme from 2005. Results Anopheles gambiae s.s. adult females from indoor collections predominated from 1970 to 1998 (ca. 85%). Beginning in 1999, A. gambiae s.s decreased proportionately relative to A. arabiensis, then precipitously declined to rarity coincident with increased bed net ownership as national bed net distribution programmes commenced in 2004 and 2006. By 2009, A. gambiae s.s. comprised proportionately ca. 1% of indoor collections and A. arabiensis 99%. In Seme compared to Asembo in 2003, proportionately more larvae were A. gambiae s.s., larval density was higher, and more larval habitats were occupied. As bed net use rose in Seme, the proportion of A. gambiae larvae declined as well. These trends continued to 2009. Parity and malaria infection rates were lower in both species in Asembo (high bed net use) compared to Seme (low bed net use), but host choice did not vary within species in both communities (predominantly cattle for A. arabiensis, humans for A. gambiae s.s.). Conclusions A marked decline of the A. gambiae s.s. population occurred as household ownership of bed nets rose in a region of western Kenya over a 10 year period. The increased bed net coverage likely caused a mass effect on the composition of the A. gambiae s.l. species complex, resulting in the observed proportionate increase in A. arabiensis compared to its closely related sibling species, A. gambiae s.s. These observations are important in evaluating the process of regional malaria elimination, which requires sustained vector control as a primary 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.

              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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                Author and article information

                Contributors
                cludwin3@gmail.com
                zhoug@uci.edu
                mbugi_jp@yahoo.com
                jsimbauni@yahoo.com
                yaw_afrane@yahoo.com
                ednaototo@gmail.com
                etemesi2012@yahoo.com
                machani.maxiwe2011@gmail.com
                githeko@yahoo.com
                guiyuny@uci.edu
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                14 November 2015
                14 November 2015
                2015
                : 8
                : 588
                Affiliations
                [ ]Centre for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya
                [ ]Departments of Zoological Sciences, Kenyatta University, Nairobi, Kenya
                [ ]Department of Medical Laboratory Sciences, Masinde Muliro University of Science and Technology, Kakamega, Kenya
                [ ]Program in Public Health, University of California, Irvine, CA 92697 USA
                Article
                1194
                10.1186/s13071-015-1194-6
                4644290
                25561160
                f4592e6f-f84c-4bd2-885a-6dd8c70b955e
                © Wanjala et al. 2015

                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
                : 4 August 2015
                : 31 October 2015
                Categories
                Research
                Custom metadata
                © The Author(s) 2015

                Parasitology
                malaria,insecticidal decay,insecticide resistance,indoor residual spraying,long-lasting insecticide nets

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