Malaria vectors in the Democratic Republic of the Congo: the mechanisms that confer insecticide resistance in  Anopheles gambiae  and  Anopheles funestus

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Abstract

Background

The Democratic Republic of the Congo (DRC) is characterized as a holoendemic malaria area with the main vectors being Anopheles funestus and members of the Anopheles gambiae complex. Due to political instability and socio-economic challenges in the region, knowledge of insecticide resistance status and resistance mechanisms in these vectors is limited. Mosquitoes were collected from a mining site in the north-eastern part of the country and, following identification, were subjected to extensive testing for the target-site and biochemical basis of resistance. Quantitative real-time PCR was used to assess a suite of 10 genes frequently involved in pyrethroid and dichlorodiphenyltrichloroethane (DDT) resistance in An. gambiae females and males. In An. funestus, gene expression microarray analysis was carried out on female mosquitoes.

Results

In both species, deltamethrin resistance was recorded along with high resistance and suspected resistance to DDT in An. gambiae and An. funestus, respectively. A total of 85% of An. gambiae carried the kdr mutations as either homozygous resistant (RR) (L1014S, L1014F or both) or heterozygous (RS), however only 3% carried the rdl mutant allele (RS) and no ace- 1 mutations were recorded. Synergist assays indicated a strong role for P450s in deltamethrin resistance in both species. In An. gambiae, analysis of transcription levels showed that the glutathione-S-transferase, GSTS1- 2, produced the highest fold change in expression (7.6-fold in females and 31-fold in males) followed by GSTE2, thioredoxin peroxidase ( TPX2), and cytochrome oxidases ( CYP6M2 and CYP6P1). All other genes tested produced fold change values below 2. Microarray analysis revealed significant over-transcription of cuticular proteins as well as CYP6M7, CYP6P9a and CYP6P9b in insecticide resistant An. funestus.

Conclusions

These data show that high levels of deltamethrin resistance in the main malaria vector species, conferred by enzymatic detoxification, are present in the DRC.

Electronic supplementary material

The online version of this article (10.1186/s12936-017-2099-y) contains supplementary material, which is available to authorized users.

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Most cited references 70

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

J Scott, W. BROGDON, F Collins (1993)

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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A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group.

L Koekemoer, L Kamau, R H Hunt … (2002)

Anopheles funestus Giles is a major malaria vector in Africa belonging to a group of species with morphologically similar characteristics. Morphological identification of members of the A. funestus group is difficult because of overlap of distinguishing characteristics in adult or immature stages as well as the necessity to rear isofemale lines to examine larval and egg characters. A rapid rDNA polymerase chain reaction (PCR) method has been developed to accurately identify five members of the A. funestus group. This PCR is based on species-specific primers in the ITS2 region on the rDNA to identify A. funestus (approximately 505bp), Anopheles vaneedeni Gillies and Coetzee (approximately 587bp), Anopheles rivulorum Leeson (approximately 411bp), Anopheles leesoni Evans (approximately 146bp), and Anopheles parensis Gillies (approximately 252bp).

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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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Author and article information

Contributors

Luisa Nardini: nardiniluisa1@gmail.com

Richard H. Hunt: richardhhunt@gmail.com

Yael L. Dahan-Moss: yaeld@nicd.ac.za

Nanette Christie: Nanette.christie@gmail.com

Riann N. Christian: riannc@nicd.ac.za

Maureen Coetzee: maureenc@nicd.ac.za

Lizette L. Koekemoer: lizettek@nicd.ac.za

Journal

Journal ID (nlm-ta): Malar J

Journal ID (iso-abbrev): Malar. J

Title: Malaria Journal

Publisher: BioMed Central (London )

ISSN (Electronic): 1475-2875

Publication date (Electronic): 7 November 2017

Publication date PMC-release: 7 November 2017

Publication date Collection: 2017

Volume: 16

Electronic Location Identifier: 448

Affiliations

[1 ]ISNI 0000 0004 1937 1135, GRID grid.11951.3d, Wits Research Institute for Malaria, School of Pathology, Faculty of Health Sciences, , University of the Witwatersrand, ; Johannesburg, 2000 South Africa

[2 ]ISNI 0000 0004 0630 4574, GRID grid.416657.7, Centre for Emerging, Zoonotic & Parasitic Diseases, , National Institute for Communicable Diseases, ; Johannesburg, 2131 South Africa

[3 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, Department of Genetics, Forestry and Agricultural Biotechnology Institute, , University of Pretoria, ; Pretoria, 0028 South Africa

Article

Publisher ID: 2099

DOI: 10.1186/s12936-017-2099-y

PMC ID: 5678590

PubMed ID: 29115954

SO-VID: f8723c76-a3af-4787-a69a-91301942d3e4

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 : 29 July 2017

Date accepted : 28 October 2017

Custom metadata

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: anopheles funestus,anopheles gambiae,deltamethrin resistance,kdr,metabolic resistance,p450s,gst

Data availability:

ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: anopheles funestus, anopheles gambiae, deltamethrin resistance, kdr, metabolic resistance, p450s, gst

Malaria vectors in the Democratic Republic of the Congo: the mechanisms that confer insecticide resistance in Anopheles gambiae and Anopheles funestus

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Most cited references 70

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

A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group.

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

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