Larval habitat diversity and mosquito species distribution along the coast of Kenya.

Background: Management of arboviruses relies heavily on vector control. Implementation and sustenance of effective control measures requires regular surveillance of mosquito occurrences, species abundance and distribution. The current study evaluated larval habitat diversity and productivity, mosquito species diversity and distribution in selected sites along the coast of Kenya. Methods: A cross-sectional survey of mosquito breeding habitats, species diversity and distribution was conducted in urban, peri-urban and forested ecological zones in Mombasa and Kilifi counties. Results: A total of 13,009 immature mosquitoes were collected from 17 diverse aquatic habitats along the coast of Kenya. Larval productivity differed significantly (F (16, 243) = 3.21, P < 0.0001) among the aquatic habitats, with tyre habitats recording the highest larval population. Culex pipiens (50.17%) and Aedes aegypti (38.73%) were the dominant mosquito species in urban areas, while Ae. vittatus (89%) was the dominant species in forested areas.  In total, 4,735 adult mosquitoes belonging to 19 species were collected in Haller Park, Bamburi, Gede and Arabuko Sokoke forest. Urban areas supported higher densities of Ae. aegypti compared to peri-urban and forest areas, which, on the other hand, supported greater mosquito species diversity. Conclusions: High Ae. aegypti production in urban and peri-urban areas present a greater risk of arbovirus outbreaks. Targeting productive habitats of Aedes aegypti, such as discarded tyres, containers and poorly maintained drainage systems in urban areas and preventing human-vector contact in peri-urban and forested areas could have a significant impact on the prevalence of arboviruses along the coast of Kenya, forestalling the periodic outbreaks experienced in the region.

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.

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

BACKGROUND: Over 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. METHODS: Using 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. RESULTS: Results 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. CONCLUSION: Reductions 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.

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.

Mosquito species abundance and diversity in Malindi, Kenya and their potential implication in pathogen transmission.

Mosquitoes (Diptera: Culicidae) are important vectors of human disease-causing pathogens. Mosquitoes are found both in rural and urban areas. Deteriorating infrastructure, poor access to health, water and sanitation services, increasing population density, and widespread poverty contribute to conditions that modify the environment, which directly influences the risk of disease within the urban and peri-urban ecosystem. The objective of this study was to evaluate the mosquito vector abundance and diversity in urban, peri-urban, and rural strata in Malindi along the Kenya coast. The study was conducted in the coastal district of Malindi between January and December 2005. Three strata were selected which were described as urban, peri-urban, and rural. Sampling was done during the wet and dry seasons. Sampling in the wet season was done in the months of April and June to cover the long rainy season and in November and December to cover the short rainy season, while the dry season was between January and March and September and October. Adult mosquito collection was done using Pyrethrum Spray Collection (PSC) and Centers for Disease Control and Prevention (CDC) light traps inside houses and specimens were identified morphologically. In the three strata (urban, peri-urban, and rural), 78.5% of the total mosquito (n = 7,775) were collected using PSC while 18.1% (n = 1,795) were collected using the CDC light traps. Using oviposition traps, mosquito eggs were collected and reared in the insectary which yielded 329 adults of which 83.8% (n = 276) were Aedes aegypti and 16.2% (n = 53) were Culex quinquefasciatus. The mosquito distribution in the three sites varied significantly in each collection site. Anopheles gambiae, Anopheles funestus and Anopheles coustani were predominant in the rural stratum while C. quinquefasciatus was mostly found in urban and peri-urban strata. However, using PSC and CDC light trap collection techniques, A. aegypti was only found in urban strata. In the three strata, mosquitoes were mainly found in high numbers during the wet season. Further, A. gambiae, C. quinquefasciatus, and A. aegypti mosquitoes were found occurring together inside the houses. This in turn exposes the inhabitants to an array of mosquito-borne diseases including malaria, bancroftian filariasis, and arboviruses (dengue fever, Yellow fever, Rift Valley fever, Chikungunya fever, and West Nile Virus). In conclusion, our findings provide useful information for the design of integrated mosquito and disease control programs in East African environments.

Wide-scale application of Bti/Bs biolarvicide in different aquatic habitat types in urban and peri-urban Malindi, Kenya.

Larval control is a major component in mosquito control programs. This study evaluated the wide-scale application of Bti/Bs biolarvicide (Bacillus thuringiensis var. israelensis [Bti] and Bacillus sphaericus [Bs]) in different aquatic habitats in urban and peri-urban Malindi, Kenya. This study was done from June 2006 to December 2007. The urban and peri-urban area of Malindi town was mapped and categorized in grid cells of 1 km(2). A total of 16 1-km(2) cells were selected based on presence Community Based Organization dealing with malaria control within the cells. Each of the 16 1-km(2) cells was thoroughly searched for the presence of potential larval habitats. All habitats, whether positive or negative for larvae, were treated and rechecked 24 h (1 day), 6 days, and 10 days later for the efficacy of Bti/Bs. Weekly larval sampling was done to determine the mosquito larval dynamics in the aquatic habitats during the study period. Morphological identification of the mosquito larvae showed that Anopheles gambiae s.l. Giles was the most predominant species of the Anopheles and while in the culicines, Cx. quinquefasciatus Say was the predominant species. Anopheles larvae were all eliminated in habitats within a day post-application. For culicine larvae, 38.1% (n=8) of the habitat types responded within day 1 post-treatment and all the larvae were killed, they turned negative during the days of follow-up. Another 38.1% (n=8) of the habitat types had culicine larvae but turned negative by day 6, while three habitats (14.3%) had larvae by 6th day but turned negative by 10th day. However during this Bti/Bs application studies, two habitat types, house drainage and cesspits (9.5%), remained positive during the follow-up although the mosquito larvae were significantly reduced. Both early and late instars of Anopheles larvae immediately responded to Bti/Bs application and reached 100% mortality. The early and late instars of culicine responded to the Bti/Bs application but not as fast as the Anopheles larval instars. The early instars Culex, responded with 90.8% mortality at day 1 post-treatment, and the mortality was 99.9% at day 10. Similarly, the late instars Culex followed the same trend and exhibited same mortalities. The weekly sampling in the aquatic habitats showed that there was a 36.3% mosquito larval reduction in the aquatic habitats over the 18-months study period. In conclusion, Bti/Bs biolarvicide are useful in reducing the mosquito larval densities in a wide range of habitats which have a direct impact of adult mosquito populations.

Efficacy of vectobac DT and culinexcombi against mosquito larvae in unused swimming pools in Malindi, Kenya.

The efficacy and persistence of 2 bacterial larvicides, Vectobac-DT (Bacillus thuringiensis israelensis [Bti]) and CulinexCombi (Bti and Bacillus sphaericus [Bs]), were tested against Anopheles gambiae and Culex quinquefasciatus in temporarily unused swimming pools with rainwater in Malindi, Kenya. Pre- and posttreatment larval densities were recorded by sampling with the standard WHO dipping technique for 8 consecutive days. The larvicides were applied to the pools with a knapsack sprayer. The data showed that Vectobac-DT was highly effective against early instars of An. gambiae with 89% reduction within 24 h but not as effective against the early stages of Cx. quinquefasciatus with reduction of only 46%. CulinexCombi resulted in high mortalities to early instars of both species with over 97% reduction within 24 h, but showed a drastic reduction 48 h after application. Both Vectobac-DT and CulinexCombi were highly effective against late instars of both species, whereby Vectobac-DT persisted much longer than CulinexCombi. Anopheles gambiae was found to be more susceptible to both larvicides than Cx. quinquefasciatus. By their high efficacy and good persistence against mosquito larvae, both Vectobac-DT and CulinexCombi can be recommended for use in integrated mosquito control programs.

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

Mark-release-recapture (MRR) experiments were conducted with emerging Anopheles gambiae s.l. and Anophelesfunestus Giles at Jaribuni and Mtepeni in Kilifi, along the Kenyan Coast. Of 739 and 1246 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.

Spatial distribution and habitat characterisation of Anopheles larvae along the Kenyan coast.

BACKGROUND & OBJECTIVES: A study was conducted to characterise larval habitats and to determine spatial heterogeneity of the Anopheles mosquito larvae. The study was conducted from May to June 1999 in nine villages along the Kenyan coast. METHODS: Aquatic habitats were sampled by use of standard dipping technique. The habitats were characterised based on size, pH, distance to the nearest house, coverage of canopy, surface debris, algae and emergent plants, turbidity, substrate, and habitat type. RESULTS: A total of 110 aquatic habitats like stream pools (n=10); puddles (n=65); tire tracks (n=5); ponds (n=5) and swamps (n=25) were sampled in nine villages located in three districts of the Kenyan coast. A total of 7,263 Anopheles mosquito larvae were collected, 63.9% were early instars and 36.1% were late instars. Morphological identification of the III and IV instar larvae by use of microscopy yielded 90.66% (n=2377) Anopheles gambiae Complex, 0.88% (n=23) An. funestus, An. coustani 7.63% (n=200), An. rivulorum 0.42% (n=11), An. pharoensis 0.19% (n=5), An. swahilicus 0.08% (n=2), An. wilsoni 0.04% (n=1) and 0.11% (n=3) were unidentified. A subset of the An. gambiae Complex larvae identified morphologically, was further analysed using rDNA-PCR technique resulting in 68.22% (n=1290) An. gambiae s.s., 7.93% (n=150) An. arabiensis and 23.85% (n=451) An. merus. Multiple logistic regression model showed that emergent plants (p = 0.019), and floating debris (p = 0.038) were the best predictors of An. gambiae larval abundance in these habitats. INTERPRETATION & CONCLUSION: Habitat type, floating debris and emergent plants were found to be the key factors determining the presence of Anopheles larvae in the habitats. For effective larval control, the type of habitat should be considered and most productive habitat type be given a priority in the mosquito abatement programme.

Anopheles gambiae s.l. and Anopheles funestus mosquito distributions at 30 villages along the Kenyan coast.

This study investigated whether Anopheles gambiae s.l. and Anopheles funestus Giles mosquito populations were distributed randomly among houses on the coast of Kenya. Sample means and variances of mosquitoes were estimated from bimonthly pyrethrum spray collections at 30 villages from July 1997 through May 1998. In total, 5,476 An. gambiae s.l. and 3,461 An. funestus were collected. The number of An. gambiae s.l. collected was highest in November/December and lowest in May. The number of An. funestus collected was highest during September/October and lowest during May. As the density of mosquitoes decreased, there was a tendency toward randomness in the distribution. The proportion of An. gambiae s.l. and An. funestus mosquitoes collected per house for each sampling period also showed patterns of clustering, with 80% of An. gambiae s.l. collected from <30% of the houses and 80% of An. funestus collected from <20% of the total houses. The total number of mosquitoes collected from any one house ranged from 0 to 121 for An. gambiae s.l. and from 0 to 152 for An. funestus. This coupled with the results of the variance to mean ratio plots suggests extensive clustering in the distribution of An. gambiae s.l. and An. funestus mosquito populations throughout the year along the coast of Kenya.

Relationships between body size of anopheles mosquitoes and Plasmodium falciparum sporozoite rates along the Kenya coast.

The influence of body size of Anopheles gambiae s.s., Anopheles arabiensis, Anopheles merus, and Anopheles funestus on the transmission of Plasmodium falciparum was studied at 3 sites along the Kenyan coast. Adult mosquitoes were collected inside houses by pyrethrum spray collection (PSC) from April to September 2001. Wing length was measured microscopically to the nearest 0.01 mm as an index of mosquito body size. The P. falciparum circumsporozoite protein (CSP) was detected by enzyme-linked immunosorbent assay technique. A total of 1715 anopheline mosquitoes were collected, of which 785 (45.77%) were An. gambiae s.s., 54 (3.15%) An. arabiensis, An. merus 27 (1.57%), and 849 (49.5%) were An. funestus. The mean wing length for An. gambiae s.s. was 2.94 mm and that of An. funestus was 2.50 mm. There was no site-to-site variation in the body size of An. gambiae or An. funestus. There was no significant difference in wing length between sporozoite-infected and uninfected An. gambiae s.s., and the same was found for An. funestus. At the 3 rural coastal sites in Kenya, the efficiency of malaria parasite transmission does not appear to be influenced by variation in vector body size.

Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast.

The seasonal dynamics and spatial distributions of Anopheles mosquitoes and Plasmodium falciparum parasites were studied for one year at 30 villages in Malindi, Kilifi, and Kwale Districts along the coast of Kenya. Anopheline mosquitoes were sampled inside houses at each site once every two months and malaria parasite prevalence in local school children was determined at the end of the entomologic survey. A total of 5,476 Anopheles gambiae s.l. and 3,461 An. funestus were collected. Species in the An. gambiae complex, identified by a polymerase chain reaction, included 81.9% An. gambiae s.s., 12.8% An. arabiensis, and 5.3% An. merus. Anopheles gambiae s.s. contributed most to the transmission of P. falciparum along the coast as a whole, while An. funestus accounted for more than 50% of all transmission in Kwale District. Large spatial heterogeneity of transmission intensity (< 1 up to 120 infective bites per person per year) resulted in correspondingly large and significantly related variations in parasite prevalence (range = 38-83%). Thirty-two percent of the sites (7 of 22 sites) with malaria prevalences ranging from 38% to 70% had annual entomologic inoculation rates (EIR) less than five infective bites per person per year. Anopheles gambiae s.l. and An. funestus densities in Kwale were not significantly influenced by rainfall. However, both were positively correlated with rainfall one and three months previously in Malindi and Kilifi Districts, respectively. These unexpected variations in the relationship between mosquito populations and rainfall suggest environmental heterogeneity in the predominant aquatic habitats in each district. One important conclusion is that the highly non-linear relationship between EIRs and prevalence indicates that the consistent pattern of high prevalence might be governed by substantial variation in transmission intensity measured by entomologic surveys. The field-based estimate of entomologic parameters on a district level does not provide a sensitive indicator of transmission intensity in this study.

Blood-meal analysis for anopheline mosquitoes sampled along the Kenyan coast.

A total of 1,480 Anopheles gambiae sensu lato and 439 An. funestus, collected from 30 sites along the Kenyan coast, were tested by direct enzyme-linked immunosorbent assay (ELISA) for blood-meal identification. Overall, the enzyme-linked immunosorbent assay (ELISA) identified 92 and 87% of the samples tested in An. gambiae s.l. and An. funestus, respectively. Of these, human IgG was detected in 98.97% (n = 1,347) of An. gambiae s.l. and 99.48% (n = 379) of An. funestus. Only 14 (1.03%) of the An. gambiae s.l. had fed on other vertebrate hosts tested, which were bovines, chickens, and goats. Additionally, only 2 An. funestus had fed on goats. In all the 28 sites that had bloodfed mosquitoes, An. gambiae s.l. had a human blood index greater than 0.9. Twenty-five of these sites had a human blood index greater than 0.9 for An. funestus, while the other 3 sites had no bloodfed mosquitoes. The An. gambiae s.l. were tested by polymerase chain reaction (PCR) for species identification. A total of 338 were An. gambiae s.s., 79 were An. arabiensis, and 12 were An. merus. The human blood index was 0.96, 0.91, and 1.0 for An. gambiae s.s., An. arabiensis, and An. merus, respectively. The Plasmodium falciparum sporozoite infection rates were 6.2% for species in the An. gambiae complex and 3.7% for An. funestus. These results emphasize that An. funestus and members of the An. gambiae complex on the Kenyan coast are highly anthropophilic, with nearly all specimens feeding on humans during every blood meal. The results further demonstrated active transmission of P. falciparum sporozoites by the primary vector species. This study suggests that the use of insecticide-treated nets will be effective for controlling biting mosquitoes inside houses along the coast of Kenya.