A prospective cohort study of Plasmodium falciparum malaria in three sites of Western Kenya.

BACKGROUND: Malaria in western Kenya is currently characterized by sustained high Plasmodial transmission and infection resurgence, despite positive responses in some areas following intensified malaria control interventions since 2006. This study aimed to evaluate long-term changes in malaria transmission profiles and to assess patterns of asymptomatic malaria infections in school children aged 5-15 years at three sites in western Kenya with heterogeneous malaria transmission and simultaneous malaria control interventions. METHODS: The study was conducted from 2018 to 2019 and is based on data taken every third year from 2005 to 2014 during a longitudinal parasitological and mosquito adult surveillance and malaria control programme that was initiated in 2002 in the villages of Kombewa, Iguhu, and Marani. Plasmodium spp. infections were determined using microscopy. Mosquito samples were identified to species and host blood meal source and sporozoite infections were assayed using polymerase chain reaction. RESULTS: Plasmodium falciparum was the only malaria parasite evaluated during this study (2018-2019). Asymptomatic malaria parasite prevalence in school children decreased in all sites from 2005 to 2008. However, since 2011, parasite prevalence has resurged by > 40% in Kombewa and Marani. Malaria vector densities showed similar reductions from 2005 to 2008 in all sites, rose steadily until 2014, and decreased again. Overall, Kombewa had a higher risk of infection compared to Iguhu (χ2 = 552.52, df = 1, P < 0.0001) and Marani (χ2 = 1127.99, df = 1, P < 0.0001). There was a significant difference in probability of non-infection during malaria episodes (log-rank test, χ2 = 617.59, df = 2, P < 0.0001) in the study sites, with Kombewa having the least median time of non-infection during malaria episodes. Gender bias toward males in infection was observed (χ2 = 27.17, df = 1, P < 0.0001). The annual entomological inoculation rates were 5.12, 3.65, and 0.50 infective bites/person/year at Kombewa, Iguhu, and Marani, respectively, during 2018 to 2019. CONCLUSIONS: Malaria prevalence in western Kenya remains high and has resurged in some sites despite continuous intervention efforts. Targeting malaria interventions to those with asymptomatic infections who serve as human reservoirs might decrease malaria transmission and prevent resurgences. Longitudinal monitoring enables detection of changes in parasitological and entomological profiles and provides core baseline data for the evaluation of vector interventions and guidance for future planning of malaria control.

Malaria vector bionomics and transmission in irrigated and non-irrigated sites in western Kenya.

Irrigation not only helps to improve food security but also creates numerous water bodies for mosquito production. This study assessed the effect of irrigation on malaria vector bionomics and transmission in a semi-arid site with ongoing malaria vector control program. The effectiveness of CDC light traps in the surveillance of malaria vectors was also evaluated relative to the human landing catches (HLCs) method. Adult mosquitoes were sampled in two study sites representing irrigated and non-irrigated agroecosystems in western Kenya using a variety of trapping methods. The mosquito samples were identified to species and assayed for host blood meal source and Plasmodium spp. sporozoite infection using polymerase chain reaction. Anopheles arabiensis was the dominant malaria vector in the two study sites and occurred in significantly higher densities in irrigated study site compared to the non-irrigated study site. The difference in indoor resting density of An. arabiensis during the dry and wet seasons was not significant. Other species, including An. funestus, An. coustani, and An. pharoensis, were collected. The An. funestus indoor resting density was 0.23 in irrigated study site while almost none of this species was collected in the non-irrigated study site. The human blood index (HBI) for An. arabiensis in the irrigated study site was 3.44% and significantly higher than 0.00% for the non-irrigated study site. In the irrigated study site, the HBI of An. arabiensis was 3.90% and 5.20% indoor and outdoor, respectively. The HBI of An. funestus was 49.43% and significantly higher compared to 3.44% for An. arabiensis in the irrigated study site. The annual entomologic inoculation rate for An. arabiensis in the irrigated study site was 0.41 and 0.30 infective bites/person/year indoor and outdoor, respectively, whereas no transmission was observed in the non-irrigated study site. The CDC light trap performed consistently with HLC in terms of vector density. These findings demonstrate that irrigated agriculture may increase the risk of malaria transmission in irrigated areas compared to the non-irrigated areas and highlight the need to complement the existing malaria vector interventions with novel tools targeting the larvae and both indoor and outdoor biting vector populations.

Current status of insecticide resistance among malaria vectors in Kenya.

BACKGROUND: Insecticide resistance has emerged as one of the major challenges facing National Malaria Control Programmes in Africa. A well-coordinated national database on insecticide resistance (IRBase) can facilitate the development of effective strategies for managing insecticide resistance and sustaining the effectiveness of chemical-based vector control measures. The aim of this study was to assemble a database on the current status of insecticide resistance among malaria vectors in Kenya. METHODS: Data was obtained from published literature through PubMed, HINARI and Google Scholar searches and unpublished literature from government reports, research institutions reports and malaria control programme reports. Each data source was assigned a unique identification code and entered into Microsoft Excel 2010 datasheets. Base maps on the distribution of insecticide resistance and resistance mechanisms among malaria vectors in Kenya were generated using ArcGIS Desktop 10.1 (ESRI, Redlands, CA, USA). RESULTS: Insecticide resistance status among the major malaria vectors in Kenya was reported in all the four classes of insecticides including pyrethroids, carbamates, organochlorines and organophosphates. Resistance to pyrethroids has been detected in Anopheles gambiae (s.s.), An. arabiensis and An. funestus (s.s.) while resistance to carbamates was limited to An. gambiae (s.s.) and An. arabiensis. Resistance to the organochlorine was reported in An. gambiae (s.s.) and An. funestus (s.s.) while resistance to organophosphates was reported in An. gambiae (s.l.) only. The mechanisms of insecticide resistance among malaria vectors reported include the kdr mutations (L 1014S and L 1014F) and elevated activity in carboxylesterase, glutathione S-transferases (GST) and monooxygenases. The kdr mutations L 1014S and L 1014F were detected in An. gambiae (s.s.) and An. arabiensis populations. Elevated activity of monooxygenases has been detected in both An. arabiensis and An. gambiae (s.s.) populations while the elevated activity of carboxylesterase and GST has been detected only in An. arabiensis populations. CONCLUSIONS: The geographical maps show the distribution of insecticide resistance and resistance mechanisms among malaria vectors in Kenya. The database generated will provide a guide to intervention policies and programmes in the fight against malaria.

The role of Anopheles arabiensis and Anopheles coustani in indoor and outdoor malaria transmission in Taveta District, Kenya.

BACKGROUND: The scaling up of malaria vector control efforts in Africa has resulted in changing the malaria vectorial systems across different ecological settings. In view of the ongoing trends in vector population dynamics, abundance, species composition and parasite infectiousness, there is a need to understand vector distribution and their contribution to malaria transmission to facilitate future planning of control strategies. We studied indoor and outdoor malaria transmission dynamics and vector population variability of Anopheles mosquitoes in Taveta district along the Kenyan Coast. METHODS: Anopheles mosquitoes were collected indoors and outdoors in 4 ecologically different villages using CDC light traps (both indoor and outdoor) and aspiration method (day resting indoors; DRI) methods. Mosquitoes were examined for infection with P. falciparum sporozoites and blood feeding preferences using enzyme linked immunosorbent assay (ELISA). The An. gambiae and An. funestus complexes were identified by PCR technique to determine the sibling species composition. RESULTS: A total of 4,004 Anopheles mosquitoes were collected consisting of 34.9%% (n = 1,397) An. gambiae s.1., 28.1% (n = 1,124) An. funestus s.l., 33.5% (n = 1,340) An. coustani and 3.6% (n = 143) An. pharoensis. A total of 14,654 culicine mosquitoes were collected, mainly Cx. quinquefasciatus. Of the total Anopheles collected, 3,729 were tested for P. falciparum sporozoite infection. The sporozoite transmission was found to be occurring both indoors and outdoors. The overall sporozoite infectivity was 0.68% (n = 2,486) indoors and 1.29% (n = 1,243) outdoors. Indoor and outdoor sporozoite infectivity and the vectorial systems varied across the 4 ecological villages. Entomological inoculation rates for the 4 villages indicate that there was site-to-site variation. In the 4 villages, Mwarusa had the highest EIRs with An. arabiensis, An. funestus and An. coustani contributing to 23.91, 11.96 and 23.91 infectious bites per person per year ib/p/year respectively. In Kiwalwa and Njoro outdoor EIR was significantly higher than indoors. CONCLUSIONS: This study shows that malaria transmission is occurring both indoors and outdoors. The main vectors are An. arabiensis, An. funestus and An. coustani indoors while An. coustani is playing a major role in outdoor transmission. Effective malaria control programmes, should therefore include tools that target both indoor and outdoor transmission.

Larval density dependence in Anopheles gambiae s.s., the major African vector of malaria.

Anopheles gambiae sensu stricto is the most important vector of malaria in Africa although relatively little is known about the density-dependent processes determining its population size. Mosquito larval density was manipulated under semi-natural conditions using artificial larval breeding sites placed in the field in coastal Kenya; two experiments were conducted: one manipulating the density of a single cohort of larvae across a range of densities and the other employing fewer densities but with the treatments crossed with four treatments manipulating predator access. In the first experiment, larval survival, development rate and the size of the adult mosquito all decreased with larval density (controlling for block effects between 23% and 31% of the variance in the data could be explained by density). In the second experiment, the effects of predator manipulation were not significant, but again we observed strong density dependence in larval survival (explaining 30% of the variance). The results are compared with laboratory studies of A. gambiae larval competition and the few other studies conducted in the field, and the consequences for malaria control are discussed.

Contribution of different aquatic habitats to adult Anopheles arabiensis and Culex quinquefasciatus (Diptera: Culicidae) production in a rice agroecosystem in Mwea, Kenya.

Studies were conducted to determine the contribution of diverse larval habitats to adult Anopheles arabiensis Patton and Culex quinquefasciatus Say production in a rice land agro-ecosystem in Mwea, Kenya. Two sizes of cages were placed in different habitat types to investigate the influence of non-mosquito invertebrates on larval mortalities and the contribution of each habitat type to mosquito productivities, respectively. These emergence traps had fine netting material covers to prevent adult mosquitoes from ovipositing in the area covered by the trap and immature mosquitoes from entering the cages. The emergence of Anopheles arabiensis in seeps, tire tracks, temporary pools, and paddies was 10.53%, 17.31%, 12.50%, and 2.14%, respectively, while the corresponding values for Cx. quinquefasciatus were 16.85% in tire tracks, 8.39% in temporary pools, and 5.65% in the paddies from 0.125 m3 cages during the study. Cages measuring 1 m3 were placed in different habitat types which included paddy, swamp, marsh, ditch, pool, and seep to determine larval habitat productivity. An. arabiensis was the predominant anopheline species (98.0%, n = 232), although a few Anopheles coustani Laveran (2.0%, n = 5) emerged from the habitats. The productivity for An. arabiensis larvae was 6.0 mosquitoes per m2 for the temporary pools, 5.5 for paddy, 5.4 for marsh, 2.7 for ditch, and 0.6 for seep. The Cx. quinquefasciatus larval habitat productivity was 47.8 mosquitoes per m2 for paddies, 35.7 for ditches, 11.1 for marshes, 4.2 for seeps, 2.4 for swamps, and 1.0 for temporary pools. Pools, paddy, and marsh habitat types were the most productive larval habitats for An. arabiensis while paddy, ditch, and marsh were the most productive larval habitats for Cx. quinquefasciatus. The most common non-mosquito invertebrate composition in the cages included Dytiscidae, Notonectidae, Belostomatidae, and Ephemerellidae, and their presence negatively affected the number of emergent mosquitoes from the cages. In conclusion, freshly formed habitats are the most productive aquatic habitats, while old and more permanent habitats are the least productive due to natural regulation of mosquito immatures.

Host choice and multiple blood feeding behaviour of malaria vectors and other anophelines in Mwea rice scheme, Kenya.

BACKGROUND: Studies were conducted between April 2004 and February 2006 to determine the blood-feeding pattern of Anopheles mosquitoes in Mwea Kenya. METHODS: Samples were collected indoors by pyrethrum spay catch and outdoors by Centers for Disease Control light traps and processed for blood meal analysis by an Enzyme-linked Immunosorbent Assay. RESULTS: A total of 3,333 blood-fed Anopheles mosquitoes representing four Anopheles species were collected and 2,796 of the samples were assayed, with Anopheles arabiensis comprising 76.2% (n = 2,542) followed in decreasing order by Anopheles coustani 8.9% (n = 297), Anopheles pharoensis 8.2% (n = 272) and Anopheles funestus 6.7% (n = 222). All mosquito species had a high preference for bovine (range 56.3-71.4%) over human (range 1.1-23.9%) or goat (0.1-2.2%) blood meals. Some individuals from all the four species were found to contain mixed blood meals. The bovine blood index (BBI) for An. arabiensis was significantly higher for populations collected indoors (71.8%), than populations collected outdoors (41.3%), but the human blood index (HBI) did not differ significantly between the two populations. In contrast, BBI for indoor collected An. funestus (51.4%) was significantly lower than for outdoor collected populations (78.0%) and the HBI was significantly higher indoors (28.7%) than outdoors (2.4%). Anthropophily of An. funestus was lowest within the rice scheme, moderate in unplanned rice agro-ecosystem, and highest within the non-irrigated agro-ecosystem. Anthropophily of An. arabiensis was significantly higher in the non-irrigated agro-ecosystem than in the other agro-ecosystems. CONCLUSION: These findings suggest that rice cultivation has an effect on host choice by Anopheles mosquitoes. The study further indicate that zooprophylaxis may be a potential strategy for malaria control, but there is need to assess how domestic animals may influence arboviruses epidemiology before adapting the strategy.

Survival of immature Anopheles arabiensis (Diptera: Culicidae) in aquatic habitats in Mwea rice irrigation scheme, central Kenya.

BACKGROUND: The survivorship and distribution of Anopheles arabiensis larvae and pupae was examined in a rice agro-ecosystem in Mwea Irrigation Scheme, central Kenya, from August 2005 to April 2006, prior to implementation of larval control programme. METHODS: Horizontal life tables were constructed for immatures in semi-field condition. The time spent in the various immature stages was determined and survival established. Vertical life tables were obtained from five paddies sampled by standard dipping technique. RESULTS: Pre-adult developmental time for An. arabiensis in the trays in the experimental set up in the screen house was 11.85 days from eclosion to emergence. The mean duration of each instar stage was estimated to be 1.40 days for first instars, 2.90 days for second instars, 1.85 days for third instars, 3.80 days for fourth instars and 1.90 days for pupae. A total of 590 individuals emerged into adults, giving an overall survivorship from L1 to adult emergence of 69.4%. A total of 4,956 An. arabiensis immatures were collected in 1,400 dips throughout the sampling period. Of these, 55.9% were collected during the tillering stage, 42.5% during the transplanting period and 1.6% during the land preparation stage. There was a significant difference in the An. arabiensis larval densities among the five stages. Also there was significant variation in immature stage composition for each day's collection in each paddy. These results indicate that the survival of the immatures was higher in some paddies than others. The mortality rate during the transplanting was 99.9% and at tillering was 96.6%, while the overall mortality was 98.3%. CONCLUSION: The survival of An. arabiensis immatures was better during the tillering stage of rice growth. Further the survival of immatures in rice fields is influenced by the rice agronomic activities including addition of nitrogenous fertilizers and pesticides. For effective integrated vector management, the application of larvicides should target An. arabiensis larvae at the tillering stage (early vegetative stage of rice) when their survival in the aquatic habitats is high to significantly reduce them and the larvicides should be long-lasting to have a significant impact on the malaria vector productivity on the habitats.

Spatially targeting Culex quinquefasciatus aquatic habitats on modified land cover for implementing an Integrated Vector Management (IVM) program in three villages within the Mwea Rice Scheme, Kenya.

BACKGROUND: Continuous land cover modification is an important part of spatial epidemiology because it can help identify environmental factors and Culex mosquitoes associated with arbovirus transmission and thus guide control intervention. The aim of this study was to determine whether remotely sensed data could be used to identify rice-related Culex quinquefasciatus breeding habitats in three rice-villages within the Mwea Rice Scheme, Kenya. We examined whether a land use land cover (LULC) classification based on two scenes, IKONOS at 4 m and Landsat Thematic Mapper at 30 m could be used to map different land uses and rice planted at different times (cohorts), and to infer which LULC change were correlated to high density Cx. quinquefasciatus aquatic habitats. We performed a maximum likelihood unsupervised classification in Erdas Imagine V8.7 and generated three land cover classifications, rice field, fallow and built environment. Differentially corrected global positioning systems (DGPS) ground coordinates of Cx. quinquefasciatus aquatic habitats were overlaid onto the LULC maps generated in ArcInfo 9.1. Grid cells were stratified by levels of irrigation (well-irrigated and poorly-irrigated) and varied according to size of the paddy. RESULTS: Total LULC change between 1988-2005 was 42.1 % in Kangichiri, 52.8 % in Kiuria and and 50.6 % Rurumi. The most frequent LULC changes was rice field to fallow and fallow to rice field. The proportion of aquatic habitats positive for Culex larvae in LULC change sites was 77.5% in Kangichiri, 72.9% in Kiuria and 73.7% in Rurumi. Poorly - irrigated grid cells displayed 63.3% of aquatic habitats among all LULC change sites. CONCLUSION: We demonstrate that optical remote sensing can identify rice cultivation LULC sites associated with high Culex oviposition. We argue that the regions of higher Culex abundance based on oviposition surveillance sites reflect underlying differences in abundance of larval habitats which is where limited control resources could be concentrated to reduce vector larval abundance.