Secondary malaria vectors in western Kenya include novel species with unexpectedly high densities and parasite infection rates

Abstract Background Malaria vector control has been implemented chiefly through indoor interventions targeting primary vectors resulting in population declines—pointing to a possible greater proportional contribution to transmission by secondary malaria vectors with their predominant exophagic and exophilic traits. With a historical focus on primary vectors, there is paucity of data on secondary malaria vectors in many countries in Africa. This study sought to determine the species compositions and bionomic traits, including proportions infected with Plasmodium falciparum and phenotypic insecticide resistance, of secondary vectors in three sites with high malaria transmission in Kisumu County, western Kenya. Methods Cross-sectional sampling of adult Anopheles was conducted using indoor and outdoor CDC light traps (CDC-LT) and animal-baited traps (ABTs) in Kakola-Ombaka and Kisian, while larvae were sampled in Ahero. Secondary vectors captured were exposed to permethrin using WHO bioassays and then analyzed by ELISA to test for proportions infected with P. falciparum sporozoites. All Anopheles were identified to species using morphological keys with a subset being molecularly identified using ITS2 and CO1 sequencing for species identification. Results Two morphologically identified secondary vectors captured—An. coustani and An. pharoensis—were determined to consist of four species molecularly. These included An. christyi, An. sp. 15 BSL-2014, an unidentified member of the An. coustani complex (An. cf. coustani) and a species similar to that of An. pharoensis and An. squamosus (An. cf. pharoensis). Standardized (Anopheles per trap per night) capture rates demonstrate higher proportions of secondary vectors across most trapping methods—with overall indoor and outdoor CDC-LTs and ABT captures composed of 52.2% (n = 93), 78.9% (n = 221) and 58.1% (n = 573) secondary vectors respectively. Secondary vectors were primarily caught outdoors. The overall proportion of secondary vectors with P. falciparum sporozoite was 0.63% (n = 5), with the unidentified species An. cf. pharoensis, determined to carry Plasmodium. Overall secondary vectors were susceptible to permethrin with a > 99% mortality rate. Conclusions Given their high densities, endophily equivalent to primary vectors, higher exophily and Plasmodium-positive proportions, secondary vectors may contribute substantially to malaria transmission. Unidentified species demonstrate the need for further morphological and molecular identification studies towards further characterization. Continued monitoring is essential for understanding their temporal contributions to transmission, the possible elevation of some to primary vectors and the development of insecticide resistance. Graphic Abstract

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Resting behaviour of malaria vectors in a highland and a lowland site of western Kenya: Implication on malaria vector control measures

10.1101/815175 ◽

2019 ◽

Author(s):

Maxwell G. Machani ◽

Eric Ochomo ◽

Fred Amimo ◽

Jackline Kosgei ◽

Stephen Munga ◽

...

Keyword(s):

Insecticide Resistance ◽

Vector Control ◽

Malaria Vector ◽

Control Measures ◽

Malaria Vectors ◽

Western Kenya ◽

Sporozoite Rate ◽

Resting Behaviour ◽

Outdoor Resting ◽

Indoor And Outdoor

AbstractBackgroundUnderstanding the interactions between increased insecticide resistance in field malaria vector populations and the subsequent resting behaviour patterns is important for planning adequate vector control measures in a specific context and sustaining the current vector interventions. The aim of this study was to investigate the resting behavior, host preference and infection with Plasmodium falciparum sporozoites by malaria vectors in different ecological settings of western Kenya with different levels of insecticide resistance.MethodsIndoor and outdoor resting Anopheline mosquitoes were sampled during the dry and rainy seasons in Kisian (lowland site) and Bungoma (highland site), both in western Kenya. WHO tube bioassay was used to determine levels of phenotypic resistance of first generation offspring (F1 progeny) of malaria vectors resting indoors and outdoors to deltamethrin. PCR-based molecular diagnostics were used for mosquito speciation, genotype for resistance mutations and to determine specific host blood meal origins. Enzyme-linked Immunosorbent Assay (ELISA) was used to determine mosquito sporozoite infections.ResultsOverall, 3,566 female Anopheles mosquitoes were collected with Anopheles gambiae s.l [In Bungoma, An. gambiae s.s (90.9%), An arabiensis (7.6%) and in Kisian, An. gambiae s.s (38.9%), An. arabiensis (60.2%)] being the most abundant species (74.7%) followed by An. funestus s.l (25.3%). The majority of An. gambiae s.l (85.4 and 58%) and An. funestus (96.6 and 91.1%) were caught resting indoors in Bungoma and Kisian respectively.Vgsc-1014S was observed at a slightly higher frequency in An. gambiae s.s hereafter(An. gambiae) resting indoor than outdoor (89.7 vs 84.6% and 71.5 vs 61.1%) in Bungoma and Kisian respectively. For An. arabiensis, Vgsc-1014S was 18.2% indoor and outdoor (17.9%) in Kisian. In Bungoma, the Vgsc-1014S was only detected in An. arabiensis resting indoors with a frequency of 10%. The Vgsc-1014F mutation was only present in An. gambiae resting indoors from both sites, but at very low frequencies in Kisian compared to Bungoma (0.8 and 9.2% respectively. In Bungoma, the sporozoite rates for An. funestus, An. gambiae, and An. arabiensis resting indoors were 10.9, 7.6 and 3.4 % respectively. For outdoor resting, An. gambiae and An. arabiensis in Bungoma, the sporozoite rates were 4.7 and 2.9 % respectively.Overall, in Bungoma, the sporozoite rate for indoor resting mosquitoes was 8.6% and 4.2% for outdoors. In Kisian the sporozoite rate was 0.9% for indoor resting An. gambiae. None of the outdoor collected mosquitoes in Kisian tested positive for sporozoite infections.ConclusionThe study reports high densities of insecticide-resistant An. gambiae and An. funestus resting indoors and the persistence of malaria transmission indoors with high entomological inoculation rates (EIR) regardless of the use of Long-lasting insecticidal nets (LLINs). These findings underline the difficulties of controlling malaria vectors resting and biting indoors using the current interventions. Supplemental vector control tools and implementation of sustainable insecticide resistance management strategies are needed in western Kenya.

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Insecticide resistance status of indoor and outdoor resting malaria vectors in a highland and lowland site in Western Kenya

10.1101/2020.10.05.326108 ◽

2020 ◽

Author(s):

Kevin O. Owuor ◽

Maxwell G. Machani ◽

Wolfgang R. Mukabana ◽

Stephen Munga ◽

Guiyun Yan ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Sub Saharan Africa ◽

Malaria Vectors ◽

Moderate Intensity ◽

Monooxygenase Activity ◽

Western Kenya ◽

Malaria Mosquitoes ◽

Outdoor Resting ◽

Indoor And Outdoor

AbstractBackgroundLong Lasting Insecticidal Nets (LLINs) and indoor residual spraying (IRS) represent powerful tools for controlling malaria vectors in sub-Saharan Africa. The success of these interventions relies on their capability to inhibit indoor feeding and resting of malaria mosquitoes. This study sought to understand the interaction of insecticide resistance with indoor and outdoor resting behavioral responses of malaria vectors from Western Kenya.MethodsThe status of insecticide resistance among indoor and outdoor resting anopheline mosquitoes was compared in Anopheles mosquitoes collected from Kisumu and Bungoma counties in Western Kenya. The level and intensity of resistance were measured using WHO-tube and CDC-bottle bioassays, respectively. The synergist piperonyl butoxide (PBO) was used to determine if metabolic activity (monooxygenase enzymes) explained the resistance observed. The mutations at the voltage-gated sodium channel (Vgsc) gene and Ace 1 gene were characterized using PCR methods. Microplate assays were used to measure levels of detoxification enzymes if present.ResultsA total of 1094 samples were discriminated within Anopheles gambiae s.l. and 289 within An. funestus s.l. In Kisian (Kisumu county), the dominant species was Anopheles arabiensis 75.2% (391/520) while in Kimaeti (Bungoma county) collections the dominant sibling species was Anopheles gambiae s.s 96.5% (554/574). The An. funestus s.l samples analysed were all An. funestus s.s from both sites. Pyrethroid resistance of An.gambiae s.l F1 progeny was observed in all sites. Lower mortality was observed against deltamethrin for the progeny of indoor resting mosquitoes compared to outdoor resting mosquitoes (Mortality rate: 37% vs 51%, P=0.044). The intensity assays showed moderate-intensity resistance to deltamethrin in the progeny of mosquitoes collected from indoors and outdoors in both study sites. In Kisian, the frequency of vgsc-L1014S and vgsc-L1014F mutation was 0.14 and 0.19 respectively in indoor resting malaria mosquitoes while those of the outdoor resting mosquitoes were 0.12 and 0.12 respectively. The ace 1 mutation was present in higher frequency in the F1 of mosquitoes resting indoors (0.23) compared to those of mosquitoes resting outdoors (0.12). In Kimaeti, the frequencies of vgsc-L1014S and vgsc-L1014F were 0.75 and 0.05 respectively for the F1 of mosquitoes collected indoors whereas those of outdoor resting ones were 0.67 and 0.03 respectively. The ace 1 G119S mutation was present in progeny of mosquitoes from Kimaeti resting indoors (0.05) whereas it was absent in those resting outdoors. Monooxygenase activity was elevated by 1.83 folds in Kisian and by 1.33 folds in Kimaeti for mosquitoes resting indoors than those resting outdoors respectively.ConclusionThe study recorded high phenotypic, metabolic and genotypic insecticide resistance in indoor resting populations of malaria vectors compared to their outdoor resting counterparts. The indication of moderate resistance intensity for the indoor resting mosquitoes is alarming as it could have an operational impact on the efficacy of the existing pyrethroid based vector control tools. The use of synergist (PBO) in LLINs may be a better alternative for widespread use in these regions recording high insecticide resistance.

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Insecticide resistance status of indoor and outdoor resting malaria vectors in a highland and lowland site in Western Kenya

PLoS ONE ◽

10.1371/journal.pone.0240771 ◽

2021 ◽

Vol 16 (3) ◽

pp. e0240771

Author(s):

Kevin O. Owuor ◽

Maxwell G. Machani ◽

Wolfgang R. Mukabana ◽

Stephen O. Munga ◽

Guiyun Yan ◽

...

Keyword(s):

Insecticide Resistance ◽

Anopheles Gambiae ◽

Sub Saharan Africa ◽

Malaria Vectors ◽

Moderate Intensity ◽

Monooxygenase Activity ◽

Western Kenya ◽

Malaria Mosquitoes ◽

Outdoor Resting ◽

Indoor And Outdoor

Background Long Lasting Insecticidal Nets (LLINs) and indoor residual spraying (IRS) represent powerful tools for controlling malaria vectors in sub-Saharan Africa. The success of these interventions relies on their capability to inhibit indoor feeding and resting of malaria mosquitoes. This study sought to understand the interaction of insecticide resistance with indoor and outdoor resting behavioral responses of malaria vectors from Western Kenya. Methods The status of insecticide resistance among indoor and outdoor resting anopheline mosquitoes was compared in Anopheles mosquitoes collected from Kisumu and Bungoma counties in Western Kenya. The level and intensity of resistance were measured using WHO-tube and CDC-bottle bioassays, respectively. The synergist piperonyl butoxide (PBO) was used to determine if metabolic activity (monooxygenase enzymes) explained the resistance observed. The mutations at the voltage-gated sodium channel (Vgsc) gene and Ace 1 gene were characterized using PCR methods. Microplate assays were used to measure levels of detoxification enzymes if present. Results A total of 1094 samples were discriminated within Anopheles gambiae s.l. and 289 within An. funestus s.l. In Kisian (Kisumu county), the dominant species was Anopheles arabiensis 75.2% (391/520) while in Kimaeti (Bungoma county) collections the dominant sibling species was Anopheles gambiae s.s 96.5% (554/574). The An. funestus s.l samples analysed were all An. funestus s.s from both sites. Pyrethroid resistance of An.gambiae s.l F1 progeny was observed in all sites. Lower mortality was observed against deltamethrin for the progeny of indoor resting mosquitoes compared to outdoor resting mosquitoes (Mortality rate: 37% vs 51%, P = 0.044). The intensity assays showed moderate-intensity resistance to deltamethrin in the progeny of mosquitoes collected from indoors and outdoors in both study sites. In Kisian, the frequency of vgsc-L1014S and vgsc-L1014F mutation was 0.14 and 0.19 respectively in indoor resting malaria mosquitoes while those of the outdoor resting mosquitoes were 0.12 and 0.12 respectively. The ace 1 mutation was present in higher frequency in the F1 of mosquitoes resting indoors (0.23) compared to those of mosquitoes resting outdoors (0.12). In Kimaeti, the frequencies of vgsc-L1014S and vgsc-L1014F were 0.75 and 0.05 respectively for the F1 of mosquitoes collected indoors whereas those of outdoor resting ones were 0.67 and 0.03 respectively. The ace 1 G119S mutation was present in progeny of mosquitoes from Kimaeti resting indoors (0.05) whereas it was absent in those resting outdoors. Monooxygenase activity was elevated by 1.83 folds in Kisian and by 1.33 folds in Kimaeti for mosquitoes resting indoors than those resting outdoors respectively. Conclusion The study recorded high phenotypic, metabolic and genotypic insecticide resistance in indoor resting populations of malaria vectors compared to their outdoor resting counterparts. The indication of moderate resistance intensity for the indoor resting mosquitoes is alarming as it could have an operational impact on the efficacy of the existing pyrethroid based vector control tools. The use of synergist (PBO) in LLINs may be a better alternative for widespread use in these regions recording high insecticide resistance.

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Insecticide resistance status of Anopheles arabiensis in irrigated and non-irrigated areas in western Kenya

Parasites & Vectors ◽

10.1186/s13071-021-04833-z ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Pauline Winnie Orondo ◽

Steven G. Nyanjom ◽

Harrysone Atieli ◽

John Githure ◽

Benyl M. Ondeto ◽

...

Keyword(s):

Insecticide Resistance ◽

Vector Control ◽

Anopheles Arabiensis ◽

Crop Protection ◽

Indoor Residual Spraying ◽

Malaria Vectors ◽

Western Kenya ◽

Animal Protection ◽

Selection Of ◽

Selection Of Resistance

Abstract Background Malaria control in Kenya is based on case management and vector control using long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS). However, the development of insecticide resistance compromises the effectiveness of insecticide-based vector control programs. The use of pesticides for agricultural purposes has been implicated as one of the sources driving the selection of resistance. The current study was undertaken to assess the status and mechanism of insecticide resistance in malaria vectors in irrigated and non-irrigated areas with varying agrochemical use in western Kenya. Methods The study was carried out in 2018–2019 in Homa Bay County, western Kenya. The bioassay was performed on adults reared from larvae collected from irrigated and non-irrigated fields in order to assess the susceptibility of malaria vectors to different classes of insecticides following the standard WHO guidelines. Characterization of knockdown resistance (kdr) and acetylcholinesterase-inhibiting enzyme/angiotensin-converting enzyme (Ace-1) mutations within Anopheles gambiae s.l. species was performed using the polymerase chain reaction (PCR) method. To determine the agricultural and public health insecticide usage pattern, a questionnaire was administered to farmers, households, and veterinary officers in the study area. Results Anopheles arabiensis was the predominant species in the irrigated (100%, n = 154) area and the dominant species in the non-irrigated areas (97.5%, n = 162), the rest being An. gambiae sensu stricto. In 2018, Anopheles arabiensis in the irrigated region were susceptible to all insecticides tested, while in the non-irrigated region reduced mortality was observed (84%) against deltamethrin. In 2019, phenotypic mortality was decreased (97.8–84% to 83.3–78.2%). In contrast, high mortality from malathion (100%), DDT (98.98%), and piperonyl butoxide (PBO)-deltamethrin (100%) was observed. Molecular analysis of the vectors from the irrigated and non-irrigated areas revealed low levels of leucine-serine/phenylalanine substitution at position 1014 (L1014S/L1014F), with mutation frequencies of 1–16%, and low-frequency mutation in the Ace-1R gene (0.7%). In addition to very high coverage of LLINs impregnated with pyrethroids and IRS with organophosphate insecticides, pyrethroids were the predominant chemical class of pesticides used for crop and animal protection. Conclusion Anopheles arabiensis from irrigated areas showed increased phenotypic resistance, and the intensive use of pesticides for crop protection in this region may have contributed to the selection of resistance genes observed. The susceptibility of these malaria vectors to organophosphates and PBO synergists in pyrethroids offers a promising future for IRS and insecticide-treated net-based vector control interventions. These findings emphasize the need for integrated vector control strategies, with particular attention to agricultural practices to mitigate mosquito resistance to insecticides. Graphic abstract

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Resting behaviour of malaria vectors in highland and lowland sites of western Kenya: Implication on malaria vector control measures

PLoS ONE ◽

10.1371/journal.pone.0224718 ◽

2020 ◽

Vol 15 (2) ◽

pp. e0224718 ◽

Cited By ~ 6

Author(s):

Maxwell G. Machani ◽

Eric Ochomo ◽

Fred Amimo ◽

Jackline Kosgei ◽

Stephen Munga ◽

...

Keyword(s):

Vector Control ◽

Malaria Vector ◽

Control Measures ◽

Malaria Vectors ◽

Malaria Vector Control ◽

Western Kenya ◽

Resting Behaviour

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Risk Factors Associated With House Entry of Malaria Vectors in an Area of Burkina Faso With High, Persistent Malaria Transmission and High Insecticide Resistance

10.21203/rs.3.rs-273831/v1 ◽

2021 ◽

Author(s):

Jean Baptiste Yaro ◽

Alfred Tiono ◽

Antoine Sanou ◽

Hyacinthe K Toe ◽

John Bradley ◽

...

Keyword(s):

Risk Factors ◽

Insecticide Resistance ◽

Burkina Faso ◽

Malaria Transmission ◽

Malaria Vector ◽

Negative Binomial ◽

Malaria Vectors ◽

Linear Mixed Effect Model ◽

Mixed Effect ◽

Factors Associated

Abstract Background: In rural Burkina Faso, the malaria vector An. gambiae s.l. is primarily thought to feed indoors at night. Identification of factors which influence mosquito house entry could lead to development of novel malaria vector control interventions. A study was therefore carried out to identify risk factors associated with house entry of An. gambiae s.l. in south-west Burkina Faso, an area of high insecticide resistance. Methods: Mosquitoes were sampled monthly during the malaria transmission season using CDC light traps in 252 houses from 10 villages, each house sleeping at least one child aged five to 15 years old. Putative risk factors for house entry of An. gambiae s.l. were measured, including socio-economic status, caregiver’s education and occupation, number of people sleeping in the same room as the child, use of anti-mosquito measures, house construction and fittings, proximity of mosquito aquatic habitats and presence of animals near the house. Mosquito counts were compared using a generalised linear mixed-effect model with negative binomial and log link function, adjusting for repeated collections. Results: 20,929 mosquitoes were caught, of which 16,270 (77.7%) were An. gambiae s.l. Of the 6,691 An. gambiae s.l. identified to species, 4,101 (61.3%) were An. gambiae and 2,590 (38.7%) An. coluzzii. Having an electricity supply (incidence rate ratio, IRR = 0.4, 95% CI = 0.3–0.7, p = 0.001) and a metal-roofed house (IRR, = 0.6, 95% CI = 0.4–1.0, p = 0.034) were associated with fewer malaria vectors inside the home. Conclusion: This study demonstrated that there were fewer An. gambiae s.l. in homes with electricity and a metal roof compared to those that did not. Brightly-lit, well-built houses with metal roofs may reduce entry of malaria mosquitoes compared to dimly-lit, poorly-built thatched roofed houses.

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Evaluating effectiveness of screening house eaves as an intervention for integrated vector management for malaria control in Nyabondo, Western Kenya.

10.21203/rs.2.18504/v1 ◽

2019 ◽

Author(s):

Peter Njoroge Ng'ang'a ◽

Collins Okoyo ◽

Charles Mbogo ◽

Clifford Maina Mutero

Keyword(s):

Malaria Transmission ◽

Malaria Prevalence ◽

Wire Mesh ◽

Control Group ◽

Cross Sectional ◽

Western Kenya ◽

Study Results ◽

Entry Points ◽

Mosquito Entry

Abstract BackgroundMosquito-proofing of houses with appropriate screens fixed at potential mosquito entry points is gaining greater recognition as a practical intervention for reducing malaria transmission indoors. The study aimed at evaluating the effectiveness of house eaves screening in preventing mosquito entry and malaria prevalence in Nyabondo, western Kenya. Methods160 houses were selected for the study, with half of them randomly chosen for screening at the eaves with fibre-glass coated wire mesh (experimental group) and the other half left without screening (control group). Randomization was carried out by use of computer-generated list, in permuted blocks of ten houses and 16 village blocks in the study site, with treatments in the ratio of 1:1. Cross-sectional baseline entomological and malaria parasitological data were collected before house eave screening. After the baseline period, series of sampling of indoor adult mosquitoes were conducted once a month in each village using CDC light traps. Three cross-sectional malaria parasitological surveys were also conducted at three month intervals after installation of the screens. The primary outcome measures were indoor Anopheles mosquito density and malaria parasite prevalence. ResultsA total of 15,286 mosquitoes were collected over the two years period using CDC light trap in 160 houses distributed over 16 study villages (mean = 4.35, SD = 11.48). Of all mosquitoes collected, 2,872 were anophelines (2,869 An. gambiae s.l., 1 An. funestus and 2 other anopheles). Overall, among An. gambiae collected, 92.6% were non-blood fed, 3.57% were blood fed and the remaining 0.47% were composed of gravid and half gravid females. Overall more mosquitoes were collected in the control than experimental arms of the study. Results from four cross-sectional prevalence surveys showed that screened houses recorded relatively low malaria prevalence rates compared to the control houses. Overall, malaria prevalence was 5.6% (95%CI: 4.2-7.5) N=1,918, with baseline survey recording 6.1% prevalence (95%CI: 3.9-9.4), n=481 and third follow-up survey recording 3.6% prevalence (95%CI: 2.0-6.8) n=494. At all the three follow-up survey points, house screening significantly reduced the malaria prevalence by 100% (p<0.001), 63.6% (p=0.026), and 100% (p<0.001) for first, second and third follow-ups surveys respectively. The house screening significantly reduced malaria prevalence by 54% (OR = 0.46, 95%CI: 0.24-0.87, p = 0.017). ConclusionsThe study demonstrated that house eave screening has potential to reduce indoor vector densities and malaria transmission in high transmission areas in Kenya.

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Monitoring of Insecticide Resistance in Anopheles culicifacies in Twelve Districts of Madhya Pradesh, Central India (2017–2019)

Journal of Tropical Medicine ◽

10.1155/2022/4404027 ◽

2022 ◽

Vol 2022 ◽

pp. 1-8

Author(s):

Ashok K. Mishra ◽

Praveen K Bharti ◽

Gyan Chand ◽

Aparup Das ◽

Himanshu Jayswar ◽

...

Keyword(s):

Insecticide Resistance ◽

Vector Control ◽

Indoor Residual Spraying ◽

Central India ◽

Control Programme ◽

Madhya Pradesh ◽

Control Measures ◽

Malaria Vectors ◽

Malaria Vector Control ◽

The Impact

Background. Indoor residual spraying (IRS) and long-lasting insecticidal nets (LLINs) are malaria vector control measures used in India, but the development of insecticide resistance poses major impediments for effective vector control strategies. As per the guidelines of the National Vector Borne Disease Control Programme (NVBDCP), the study was conducted in 12 districts of Madhya Pradesh to generate data on insecticide resistance in malaria vectors. Methods. The susceptibility tests were conducted on adult An. culicifacies as per the WHO standard technique with wild-caught mosquitoes. The blood-fed female mosquitoes were exposed in 3 to 4 replicates on each occasion to the impregnated papers with specified discriminating dosages of the insecticides (DDT: 4%, malathion: 5%, deltamethrin: 0.05%, and alphacypermethrin: 0.05%), for one hour, and mortality was recorded after 24-hour holding. Results. An. culicifacies was found resistant to DDT 4% in all the 12 districts and malathion in 11 districts. The resistance to alphacypermethrin was also observed in two districts, and possible resistance was found to alphacypermethrin in seven districts and to deltamethrin in eight districts, while the vector was found susceptible to both deltamethrin and alphacypermethrin in only 3 districts. Conclusion. An. culicifacies is resistant to DDT and malathion and has emerging resistance to pyrethroids, alphacypermethrin, and deltamethrin. Therefore, regular monitoring of insecticide susceptibility in malaria vectors is needed for implementing effective vector management strategies. However, studies to verify the impact of IRS with good coverage on the transmission of disease are required before deciding on the change of insecticide in conjunction with epidemiological data.

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Indoor and outdoor malaria transmission in two ecological settings in rural Mali: implications for vector control

Malaria Journal ◽

10.1186/s12936-021-03650-0 ◽

2021 ◽

Vol 20 (1) ◽

Author(s):

Moussa Keïta ◽

Sidy Doumbia ◽

Ibrahim Sissoko ◽

Mahamoudou Touré ◽

Sory Ibrahim Diawara ◽

...

Keyword(s):

Vector Control ◽

Malaria Transmission ◽

Control Strategies ◽

Indoor Residual Spraying ◽

Credible Interval ◽

Human Landing Catch ◽

Malaria Vector Control ◽

Anopheles Coluzzii ◽

Sporozoite Rate ◽

Indoor And Outdoor

Abstract Background Implementation and upscale of effective malaria vector control strategies necessitates understanding the multi-factorial aspects of transmission patterns. The primary aims of this study are to determine the vector composition, biting rates, trophic preference, and the overall importance of distinguishing outdoor versus indoor malaria transmission through a study at two communities in rural Mali. Methods Mosquito collection was carried out between July 2012 and June 2016 at two rural Mali communities (Dangassa and Koïla Bamanan) using pyrethrum spray-catch and human landing catch approaches at both indoor and outdoor locations. Species of Anopheles gambiae complex were identified by polymerase chain reaction (PCR). Enzyme-Linked -Immuno-Sorbent Assay (ELISA) were used to determine the origin of mosquito blood meals and presence of Plasmodium falciparum sporozoite infections. Results A total of 11,237 An. gambiae sensu lato (s.l.) were collected during the study period (5239 and 5998 from the Dangassa and Koïla Bamanan sites, respectively). Of the 679 identified by PCR in Dangassa, Anopheles coluzzii was the predominant species with 91.4% of the catch followed by An. gambiae (8.0%) and Anopheles arabiensis (0.6%). At the same time in Koïla Bamanan, of the 623 An. gambiae s.l., An. coluzzii accounted for 99% of the catch, An. arabiensis 0.8% and An. gambiae 0.2%. Human Blood Index (HBI) measures were significantly higher in Dangassa (79.4%; 95% Bayesian credible interval (BCI) [77.4, 81.4]) than in Koïla Bamanan (15.9%; 95% BCI [14.7, 17.1]). The human biting rates were higher during the second half of the night at both sites. In Dangassa, the sporozoite rate was comparable between outdoor and indoor mosquito collections. For outdoor collections, the sporozoite positive rate was 3.6% (95% BCI [2.1–4.3]) and indoor collections were 3.1% (95% BCI [2.4–5.0]). In Koïla Bamanan, the sporozoite rate was higher indoors at 4.3% (95% BCI [2.7–6.3]) compared with outdoors at 2.4% (95% BCI [1.1–4.2]). In Dangassa, corrected entomological inoculation rates (cEIRs) using HBI were 13.74 [95% BCI 9.21–19.14] infective bites/person/month (ib/p/m) at indoor, and 18.66 [95% BCI 12.55–25.81] ib/p/m at outdoor. For Koïla Bamanan, cEIRs were 1.57 [95% BCI 2.34–2.72] ib/p/m and 0.94 [95% BCI 0.43–1.64] ib/p/m for indoor and outdoor, respectively. EIRs were significantly higher at the Dangassa site than the Koïla Bamanan site. Conclusion The findings in this work may indicate the occurrence of active, outdoor residual malaria transmission is comparable to indoor transmission in some geographic settings. The high outdoor transmission patterns observed here highlight the need for additional strategies to combat outdoor malaria transmission to complement traditional indoor preventive approaches such as long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) which typically focus on resting mosquitoes.

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Comparative assessment of insecticide resistance phenotypes in two major malaria vectors, Anopheles funestus and Anopheles arabiensis in south-eastern Tanzania

Malaria Journal ◽

10.1186/s12936-020-03483-3 ◽

2020 ◽

Vol 19 (1) ◽

Author(s):

Polius G. Pinda ◽

Claudia Eichenberger ◽

Halfan S. Ngowo ◽

Dickson S. Msaky ◽

Said Abbasi ◽

...

Keyword(s):

Insecticide Resistance ◽

Malaria Transmission ◽

Anopheles Arabiensis ◽

Pyrethroid Resistance ◽

Anopheles Funestus ◽

Indoor Residual Spraying ◽

Sub Saharan Africa ◽

World Health ◽

Malaria Vectors ◽

South Eastern

Abstract Background Long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) have greatly reduced malaria transmission in sub-Saharan Africa, but are threatened by insecticide resistance. In south-eastern Tanzania, pyrethroid-resistant Anopheles funestus are now implicated in > 80% of malaria infections, even in villages where the species occurs at lower densities than the other vector, Anopheles arabiensis. This study compared the insecticide resistance phenotypes between the two malaria vectors in an area where pyrethroid-LLINs are widely used. Methods The study used the World Health Organization (WHO) assays with 1×, 5× and 10× insecticide doses to assess levels of resistance, followed by synergist bioassays to understand possible mechanisms of the observed resistance phenotypes. The tests involved adult mosquitoes collected from three villages across two districts in south-eastern Tanzania and included four insecticide classes. Findings At baseline doses (1×), both species were resistant to the two candidate pyrethroids (permethrin and deltamethrin), but susceptible to the organophosphate (pirimiphos-methyl). Anopheles funestus, but not An. arabiensis was also resistant to the carbamate (bendiocarb). Both species were resistant to DDT in all villages except in one village where An. arabiensis was susceptible. Anopheles funestus showed strong resistance to pyrethroids, surviving the 5× and 10× doses, while An. arabiensis reverted to susceptibility at the 5× dose. Pre-exposure to the synergist, piperonyl butoxide (PBO), enhanced the potency of the pyrethroids against both species and resulted in full susceptibility of An. arabiensis (> 98% mortality). However, for An. funestus from two villages, permethrin-associated mortalities after pre-exposure to PBO only exceeded 90% but not 98%. Conclusions In south-eastern Tanzania, where An. funestus dominates malaria transmission, the species also has much stronger resistance to pyrethroids than its counterpart, An. arabiensis, and can survive more classes of insecticides. The pyrethroid resistance in both species appears to be mostly metabolic and may be partially addressed using synergists, e.g. PBO. These findings may explain the continued persistence and dominance of An. funestus despite widespread use of pyrethroid-treated LLINs, and inform new intervention choices for such settings. In short and medium-term, these may include PBO-based LLINs or improved IRS with compounds to which the vectors are still susceptible.

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