Joseph M. Mwangangi

Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years

BackgroundOver the past 20 years, numerous studies have investigated the ecology and behaviour of malaria vectors and Plasmodium falciparum malaria transmission on the coast of Kenya. Substantial progress has been made to control vector populations and reduce high malaria prevalence and severe disease. The goal of this paper was to examine trends over the past 20 years in Anopheles species composition, density, blood-feeding behaviour, and P. falciparum sporozoite transmission along the coast of Kenya.MethodsUsing data collected from 1990 to 2010, vector density, species composition, blood-feeding patterns, and malaria transmission intensity was examined along the Kenyan coast. Mosquitoes were identified to species, based on morphological characteristics and DNA extracted from Anopheles gambiae for amplification. Using negative binomial generalized estimating equations, mosquito abundance over the period were modelled while adjusting for season. A multiple logistic regression model was used to analyse the sporozoite rates.ResultsResults show that in some areas along the Kenyan coast, Anopheles arabiensis and Anopheles merus have replaced An. gambiae sensu stricto (s.s.) and Anopheles funestus as the major mosquito species. Further, there has been a shift from human to animal feeding for both An. gambiae sensu lato (s.l.) (99% to 16%) and An. funestus (100% to 3%), and P. falciparum sporozoite rates have significantly declined over the last 20 years, with the lowest sporozoite rates being observed in 2007 (0.19%) and 2008 (0.34%). There has been, on average, a significant reduction in the abundance of An. gambiae s.l. over the years (IRR = 0.94, 95% CI 0.90–0.98), with the density standing at low levels of an average 0.006 mosquitoes/house in the year 2010.ConclusionReductions in the densities of the major malaria vectors and a shift from human to animal feeding have contributed to the decreased burden of malaria along the Kenyan coast. Vector species composition remains heterogeneous but in many areas An. arabiensis has replaced An. gambiae as the major malaria vector. This has important implications for malaria epidemiology and control given that this vector predominately rests and feeds on humans outdoors. Strategies for vector control need to continue focusing on tools for protecting residents inside houses but additionally employ outdoor control tools because these are essential for further reducing the levels of malaria transmission.

Impact of insecticide-treated bed nets on malaria transmission indices on the south coast of Kenya

BackgroundBesides significantly reducing malaria vector densities, prolonged usage of bed nets has been linked to decline of Anopheles gambiae s.s. relative to Anopheles arabiensis, changes in host feeding preference of malaria vectors, and behavioural shifts to exophagy (outdoor biting) for the two important malaria vectors in Africa, An. gambiae s.l. and Anopheles funestus. In southern coastal Kenya, bed net use was negligible in 1997-1998 when Anopheles funestus and An. gambiae s.s. were the primary malaria vectors, with An. arabiensis and Anopheles merus playing a secondary role. Since 2001, bed net use has increased progressively and reached high levels by 2009-2010 with corresponding decline in malaria transmission.MethodsTo evaluate the impact of the substantial increase in household bed net use within this area on vector density, vector composition, and human-vector contact, indoor and outdoor resting mosquitoes were collected in the same region during 2009-2010 using pyrethrum spray catches and clay pots for indoor and outdoor collections respectively. Information on bed net use per sleeping spaces and factors influencing mosquito density were determined in the same houses using Poisson regression analysis. Species distribution was determined, and number of mosquitoes per house, human-biting rates (HBR), and entomological inoculation rate (EIR) were compared to those reported for the same area during 1997-1998, when bed net coverage had been minimal.ResultsCompared to 1997-1998, a significant decline in the relative proportion of An. gambiae s.s. among collected mosquitoes was noted, coupled with a proportionate increase of An. arabiensis. Following > 5 years of 60-86% coverage with bed nets, the density, human biting rate and EIR of indoor resting mosquitoes were reduced by more than 92% for An. funestus and by 75% for An. gambiae s.l. In addition, the host feeding choice of both vectors shifted more toward non-human vertebrates. Besides bed net use, malaria vector abundance was also influenced by type of house construction and according to whether one sleeps on a bed or a mat (both of these are associated with household wealth). Mosquito density was positively associated with presence of domestic animals.ConclusionsThese entomological indices indicate a much reduced human biting rate and a diminishing role of An. gambiae s.s. in malaria transmission following high bed net coverage. While increasing bed net coverage beyond the current levels may not significantly reduce the transmission potential of An. arabiensis, it is anticipated that increasing or at least sustaining high bed net coverage will result in a diminished role for An. funestus in malaria transmission.

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

BackgroundStudies were conducted between April 2004 and February 2006 to determine the blood-feeding pattern of Anopheles mosquitoes in Mwea Kenya.MethodsSamples 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.ResultsA 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.ConclusionThese 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.

Estimating dispersal and survival of Anopheles gambiae and Anopheles funestus along the Kenyan coast by using mark-release-recapture methods.

Abstract Mark-release-recapture (MRR) experiments were conducted with emerging Anopheles gambiae s.l. and Anopheles funestus Giles at Jaribuni and Mtepeni in Kilifi, along the Kenyan Coast. Of 739 and 1,246 Anopheles released at Jaribuni and Mtepeni, 24.6 and 4.33% were recaptured, respectively. The daily survival probability was 0.96 for An. funestus and 0.95 for An. gambiae in Jaribuni and 0.83 and 0.95, respectively, in Mtepeni. The maximum flight distance recorded was 661 m. The high survival probability of An. gambiae and An. funestus estimated accounts for the continuous transmission of malaria along the Kenyan coast. This study also shows that the release of young, emergent female Anopheles improves the recapture rates and may be a better approach to MRR studies.

Environmental factors associated with the distribution of Anopheles arabiensis and Culex quinquefasciatus in a rice agro-ecosystem in Mwea, Kenya

ABSTRACT Studies were conducted between May and June, 2006 to investigate the environmental factors affecting the distribution of An. arabiensis Patton and Culex quinquefasciatus Say in Mwea, Kenya. The sampling unit comprised all nonpaddy aquatic habitats and ten randomly selected paddies and canals located within a 200 m radius from the periphery of the study site. Thirteen physico-chemical variables were recorded for each sampling site in each sampling occasion and a sample of mosquito larvae and other aquatic invertebrates collected. The non-paddy aquatic habitats identified included pools and marshes. Morphological identification of 1,974 mosquito larvae yielded four species dominated by Cx. quinquefasciatus (73.2%) and An. arabiensis (25.0%). Pools were associated with significantly higher Cx. quinquefasciatus larval abundance and less diversity of other aquatic invertebrates compared with other habitat types. In contrast, the abundance of An. arabiensis did not differ significantly among habitat types. Culex quinquefasciatus habitats had higher water conductivity and exhibited a higher abundance of other aquatic invertebrates than An. arabiensis habitats. Chi-square analysis indicated that the two species were more likely to coexist in the same habitats than would be expected by chance alone. Anopheles arabiensis larvae were positively associated with dissolved oxygen and adults of family Haliplidae and negatively associated with emergent vegetation and Heptageniidae larvae. Culex quinquefasciatus larvae were positively associated with dissolved oxygen, total dissolved solids, Chironomidae larvae, and Microvelidae adults and negatively associated with emergent vegetation. These findings suggest that both biotic and abiotic factors play a significant role in niche partitioning among Cx. quinquefasciatus and An. arabiensis, a factor that should be considered when designing an integrated vector control program.

Wind direction and proximity to larval sites determines malaria risk in Kilifi District in Kenya

Studies of the fine-scale spatial epidemiology of malaria consistently identify malaria hotspots, comprising clusters of homesteads at high transmission intensity. These hotspots sustain transmission, and may be targeted by malaria-control programmes. Here we describe the spatial relationship between the location of Anopheles larval sites and human malaria infection in a cohort study of 642 children, aged 1–10-years-old. Our data suggest that proximity to larval sites predict human malaria infection, when homesteads are upwind of larval sites, but not when homesteads are downwind of larval sites. We conclude that following oviposition, female Anophelines fly upwind in search for human hosts and, thus, malaria transmission may be disrupted by targeting vector larval sites in close proximity, and downwind to malaria hotspots.

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

BackgroundThe 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.MethodsAnopheles 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.ResultsA 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.ConclusionsThis 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.

Mosquito Species Succession and Physicochemical Factors Affecting Their Abundance in Rice Fields in Mwea, Kenya

Abstract The succession of mosquito species and abiotic factors affecting their distribution and abundance in rice (Oryza spp.) fields was investigated over a 16-wk rice growing cycle covering the period between January and May 2006. Fifteen experimental rice plots were sampled for mosquito larvae and characterized based on rice height, number of tillers, floating vegetation cover, water depth, water temperature, turbidity, salinity, pH, dissolved oxygen, total dissolved solids, and conductivity. Microscopic identification of 3,025 larvae yielded nine mosquito species predominated by Anopheles arabiensis Patton (45.0%), Culex quinquefasciatus Say (35.8%), Anopheles pharoensis Theobald (9.0%) and Ficalbia splendens Theobald (7.1%). Other species, including Anopheles rufipes Gough, Anopheles coustani Laveran, Anonopheles maculipalpis Giles, Culex annulioris Theobald, and Culex poicilipes Theobald made up 3.1% of the total collection. Anopheles gambiae s.l., Cx. quinquefasciatus, and An. pharoensis occurred throughout the cycle, but they were more abundant up to 4 wk posttransplanting with peaks after fertilizer application. As rice plants became established, three groups of mosquitoes were recognized: the first groups included An. rufipes, Fl. splendens, and Cx. annulioris, which occurred throughout much of the second half of the rice cycle, whereas the second group included Cx. poicilipes, which was found in the middle of the rice cycle. An. coustani and An. maculipalpis formed the third group occurring toward the end of the cycle. Dissolved oxygen, number of tillers, and rice height were negatively associated with the abundance of An. arabiensis and Cx. quinquefasciatus larvae. In addition, Cx. quinquefasciatus also was associated with water depth (−ve) and turbidity (+ve). Abundance of An. pharoensis larvae was significantly associated with water temperature (+ve), the number of tillers (−ve), and rice height (−ve), whereas Fl. splendens was significantly associated with the number of tillers (+ve). The results demonstrate a complex nature of the interactions between some of the factors in the ecosystem and mosquito species abundance and calls for time-dependent and species-specific mosquito control operations.

Concomitant infections of Plasmodium falciparum and Wuchereria bancrofti on the Kenyan coast

Background Anopheles gambiae s.l. and An. funestus are important vectors of malaria and bancroftian filariasis, which occur as co-endemic infections along the Kenyan Coast. However, little is known about the occurrence and prevalence of concomitant infections of the two diseases in mosquito and human populations in these areas. This study reports the prevalence of concomitant infections of Plasmodium falciparum and Wuchereria bancrofti in mosquito and human populations in Jilore and Shakahola villages in Malindi, Kenya. Methods Mosquitoes were sampled inside houses by pyrethrum spray sheet collection (PSC) while blood samples were collected by finger prick technique at the end of entomological survey. Results A total of 1,979 female Anopheles mosquitoes comprising of 1,919 Anopheles gambiae s.l and 60 An. funestus were collected. Concomitant infections of P. falciparum sporozoites and filarial worms occurred in 1.1% and 1.6% of An. gambiae s.l collected in Jilore and Shakahola villages respectively. Wuchereria-infected mosquitoes had higher sporozoite rates compared to non-infected mosquitoes, but multiple infections appeared to reduce mosquito survivorship making transmission of such infections rare. None of the persons examined in Shakahola (n = 107) had coinfections of the two parasites, whereas in Jilore (n = 94), out of the 4.3% of individuals harbouring both parasites, 1.2% had P. falciparum gametocytes and microfilariae and could potentially infect the mosquito with both parasites simultaneously. Conclusion Concerted efforts should be made to integrate the control of malaria and bancroftian filariasis in areas where they co-exist.

Evaluation of Four Sampling Techniques for Surveillance of Culex quinquefasciatus (Diptera: Culicidae) and Other Mosquitoes in African Rice Agroecosystems

Abstract Field studies were conducted in a rice, Oryza sativa L., agroecosystem in Mwea Kenya to compare the efficiency of CO2-baited Centers for Disease Control (CDC) light traps against nonbaited CDC light traps and gravid traps against oviposition traps in outdoor collection of Culex quinquefasciatus Say (Diptera: Culicidae) and other mosquitoes. Collectively, 21 mosquito species from the genera Culex, Anopheles, Mansonia, Ficalbia, and Aedes were captured during the 10-wk study period. Cx. quinquefasciatus was the predominant species in all trap types with proportions ranging from 57% in the nonbaited CDC light traps to 95% in the gravid traps. Significantly higher numbers of Cx. quinquefasciatus and Culex annulioris Theobald were collected in the CO2-baited CDC light traps than in the nonbaited CDC light traps, but the numbers of other mosquito species, including malaria vectors Anopheles arabiensis Patton and Anopheles funestus Giles did not differ significantly between the two trap types. More Cx. quinquefasciatus females were collected in grass infusion-baited gravid traps than egg rafts of this species in oviposition traps containing the same infusion. Although most mosquitoes captured in CO2-baited and nonbaited CDC light traps were unfed, most of those collected in gravid traps were gravid. From these findings, it is concluded that at least in the rice-growing area of Mwea Kenya, CO2-baited CDC light traps in conjunction with gravid traps can be used in monitoring of Cx. quinquefasciatus both for control and disease surveillance.