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. 2019 Feb 19;14(2):e0212024.
doi: 10.1371/journal.pone.0212024. eCollection 2019.

Spatial and temporal development of deltamethrin resistance in malaria vectors of the Anopheles gambiae complex from North Cameroon

Stanislas Elysée Mandeng  1   2 , Herman Parfait Awono-Ambene  1 , Jude D Bigoga  3 , Wolfgang Eyisap Ekoko  1   4 , Jérome Binyang  2 , Michael Piameu  1   5 , Lili Ranaise Mbakop  1   2 , Betrand Nono Fesuh  6 , Narcisse Mvondo  2 , Raymond Tabue  3   7 , Philippe Nwane  1 , Rémy Mimpfoundi  2 , Jean Claude Toto  1 , Immo Kleinschmidt  8   9 , Tessa Bellamy Knox  10 , Abraham Peter Mnzava  11 , Martin James Donnelly  12 , Etienne Fondjo  7 , Josiane Etang  1   13   14
Affiliations

Spatial and temporal development of deltamethrin resistance in malaria vectors of the Anopheles gambiae complex from North Cameroon

Stanislas Elysée Mandeng et al. PLoS One. .

Abstract

The effectiveness of insecticide-based malaria vector control interventions in Africa is threatened by the spread and intensification of pyrethroid resistance in targeted mosquito populations. The present study aimed at investigating the temporal and spatial dynamics of deltamethrin resistance in An. gambiae s.l. populations from North Cameroon. Mosquito larvae were collected from 24 settings of the Garoua, Pitoa and Mayo Oulo Health Districts (HDs) from 2011 to 2015. Two to five days old female An. gambiae s.l. emerging from larval collections were tested for deltamethrin resistance using the World Health Organization's (WHO) standard protocol. Sub samples of test mosquitoes were identified to species using PCR-RFLP and genotyped for knockdown resistance alleles (Kdr 1014F and 1014S) using Hot Ligation Oligonucleotide Assay (HOLA). All the tested mosquitoes were identified as belonging to the An. gambiae complex, including 3 sibling species mostly represented by Anopheles arabiensis (67.6%), followed by Anopheles coluzzii (25.4%) and Anopheles gambiae (7%). Deltamethrin resistance frequencies increased significantly between 2011 and 2015, with mosquito mortality rates declining from 70-85% to 49-73% in the three HDs (Jonckheere-Terstra test statistic (JT) = 5638, P< 0.001), although a temporary increase of mortality rates (91-97%) was seen in the Pitoa and Mayo Oulo HDs in 2012. Overall, confirmed resistance emerged in 10 An. gambiae s.l. populations over the 24 field populations monitored during the study period, from 2011 to 2015. Phenotypic resistance was mostly found in urban settings compared with semi-urban and rural settings (JT = 5282, P< 0.0001), with a spatial autocorrelation between neighboring localities. The Kdr 1014F allelic frequencies in study HDs increased from 0-30% in 2011 to 18-61% in 2014-2015 (JT = 620, P <0.001), especially in An. coluzzii samples. The overall frequency of the Kdr 1014S allele was 0.1%. This study revealed a rapid increase and widespread deltamethrin resistance frequency as well as Kdr 1014F allelic frequencies in An. gambiae s.l. populations over time, emphasizing the urgent need for vector surveillance and insecticide resistance management strategies in Cameroon.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Map of North Cameroon showing study Health Districts (HDs) and clusters.
The red chart encloses cluster of the Garoua HD (LAN: Lainde II; OUL: Ouro lawane; PLA: Plateau; DJM: Djamboutou; OUG: Ourogarga; KAN: Kanadi I; KAD: Kanadi II; MBI: Mbilga; OUH: Ouro housso; KOL: Kollere). The green chart encloses cluster of the Pitoa HD (PEN: Pene; BOL: Boulgou; LOM: Lombou; MBO: Mbolom; NAB: Nassarao-be; BEC: Be-centre; GUI: Guizigare). The Blue chart encloses cluster of the Mayo Oulo HD (DOU: Doumou; BOS: Bossoum; DOR: Dourbeye; MAY: Mayo oulo; MAB: Maboni; MAT: Matra; BAL: Bala).
Fig 2
Fig 2. Distribution of species among An. gambiae s.l. samples from 2011 to 2015.
Fig 3
Fig 3. Temporal evolution of An. arabiensis, An. coluzzii and An. gambiae species proportions across the Garoua, Mayo Oulo and Pitoa Health districts (2011–2015).
Fig 4
Fig 4. Spatial and temporal distribution of deltamethrin resistance in the study sites (2011–2015).
Fig 5
Fig 5. Spatial and temporal distribution of mortality rate (TM 24) and Tkd50 (knockdown times) according to the ecological features (2011–2015).
Ru: rural settings; Peri-Urb: peri-urban settings; Urb: urban settings. Tkd50: time of knock-down for 50% tested mosquitoes; TM24: mortality rates 24 hours post exposure to insecticide.
Fig 6
Fig 6. Temporal evolution of deltamethrin resistance in the study health districts (2011–2015).
TM24: mortality rates 24 hours post exposure to insecticide.
Fig 7
Fig 7. Variations in frequencies of knockdown resistance (Kdr L1014F) allele in An. gambiae s.l. populations (2011–2015).
Fig 8
Fig 8. Multiple factor analysis (MFA): Representation of the individuals (localities) and variables on the first plane.
Individual factor map showing the interaction between localities and years, coloured according to health districts (left). Correlation circle (right) is for the following sets of quantitative data: mortality rates, Kdr L1014F allele, species composition, and year. Health district was added as a supplementary variable. The analysis on the sets of data over the 5 years study period were done in localities were all the sets of data were available. TM24: TM24: mortality rates 24 hours post exposure to insecticides; per.arbien: percentage of An. arabiensis; per coluzz:percentage of An. coluzzii; per.gamb: percentage of An. gambiae: col1014F: allelic frequency of Kdr L1014F in An. coluzzii; Col L1014F: allelic frequency of Kdr L1014F in An. coluzzii; Ara L1014F: allelic frequency of Kdr L1014F in An. arabiensis; Gab 1014F: allelic frequency of Kdr L1014F in An. gambiae.
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