Plasmodium falciparum transmission and aridity: a Kenyan experience from the dry lands of Baringo and its implications for Anopheles arabiensis control.

BACKGROUND: The ecology of malaria vectors particularly in semi-arid areas of Africa is poorly understood. Accurate knowledge on this subject will boost current efforts to reduce the burden of malaria in sub-Saharan Africa. The objective of this study was to describe the dynamics of malaria transmission in two model semi-arid sites (Kamarimar and Tirion) in Baringo in Kenya. METHODS: Adult mosquitoes were collected indoors by pyrethrum spray collections (PSC) and outdoors by Centers for Disease Control (CDC) light traps and identified to species by morphological characteristics. Sibling species of Anopheles gambiae complex were further characterized by rDNA. PCR and enzyme-linked immuno-sorbent assays (ELISA) were used to test for Plasmodium falciparum circumsporozoite proteins and host blood meal sources respectively. RESULTS: Anopheles arabiensis was not only the most dominant mosquito species in both study sites but also the only sibling species of An. gambiae s.l. present in the area. Other species identified in the study area were Anopheles funestus, Anopheles pharoensis and Anopheles coustani. For Kamarimar but not Tirion, the human blood index (HBI) for light trap samples was significantly higher than for PSC samples (Kamarimar, 0.63 and 0.11, Tirion, 0.48 and 0.43). The HBI for light trap samples was significantly higher in Kamarimar than in Tirion while that of PSC samples was significantly higher in Tirion than in Kamarimar. Entomological inoculation rates (EIR) were only detected for one month in Kamarimar and 3 months in Tirion. The number of houses in a homestead, number of people sleeping in the house, quality of the house, presence or absence of domestic animals, and distance to the animal shelter and the nearest larval habitat were significant predictors of An. arabiensis occurrence. CONCLUSION: Malaria transmission in the study area is seasonal with An. arabiensis as the dominant vector. The fact this species feeds readily on humans and domestic animals suggest that zooprophylaxis may be a plausible malaria control strategy in semi-arid areas of Africa. The results also suggest that certain household characteristics may increase the risk of malaria transmission.

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.

Hydrological modeling of geophysical parameters of arboviral and protozoan disease vectors in Internally Displaced People camps in Gulu, Uganda.

BACKGROUND: The aim of this study was to determine if remotely sensed data and Digital Elevation Model (DEM) can test relationships between Culex quinquefasciatus and Anopheles gambiae s.l. larval habitats and environmental parameters within Internally Displaced People (IDP) campgrounds in Gulu, Uganda. A total of 65 georeferenced aquatic habitats in various IDP camps were studied to compare the larval abundance of Cx. quinquefasciatus and An. gambiae s.l. The aquatic habitat dataset were overlaid onto Land Use Land Cover (LULC) maps retrieved from Landsat imagery with 150 m x 150 m grid cells stratified by levels of drainage. The LULC change was estimated over a period of 14 years. Poisson regression analyses and Moran's I statistics were used to model relationships between larval abundance and environmental predictors. Individual larval habitat data were further evaluated in terms of their covariations with spatial autocorrelation by regressing them on candidate spatial filter eigenvectors. Multispectral QuickBird imagery classification and DEM-based GIS methods were generated to evaluate stream flow direction and accumulation for identification of immature Cx. quinquefasciatus and An. gambiae s.l. and abundance. RESULTS: The main LULC change in urban Gulu IDP camps was non-urban to urban, which included about 71.5 % of the land cover. The regression models indicate that counts of An. gambiae s.l. larvae were associated with shade while Cx. quinquefasciatus were associated with floating vegetation. Moran's I and the General G statistics for mosquito density by species and instars, identified significant clusters of high densities of Anopheles; larvae, however, Culex are not consistently clustered. A stepwise negative binomial regression decomposed the immature An. gambiae s.l. data into empirical orthogonal bases. The data suggest the presence of roughly 11% to 28 % redundant information in the larval count samples. The DEM suggest a positive correlation for Culex (0.24) while for Anopheles there was a negative correlation (-0.23) for a local model distance to stream. CONCLUSION: These data demonstrate that optical remote sensing; geostatistics and DEMs can be used to identify parameters associated with Culex and Anopheles aquatic habitats.

Diversity of riceland mosquitoes and factors affecting their occurrence and distribution in Mwea, Kenya.

Knowledge of mosquito species diversity, occurrence, and distribution is an essential component of vector ecology and a guiding principle to formulation and implementation of integrated vector management programs. A 12-month entomological survey was conducted to determine the diversity of riceland mosquitoes and factors affecting their occurrence and distribution at 3 sites targeted for malaria vector control in Mwea, Kenya. Adult mosquitoes were sampled indoors by pyrethrum spray catch and outdoors by the Centers for Disease Control and Prevention light traps. Mosquitoes were then morphologically identified to species using taxonomic keys. The characteristics of houses sampled for indoor resting mosquitoes, including number of people sleeping in each house the night preceding collection, presence of bed nets, location of the house, size of eaves, wall type, presence of cattle and distance of the house to the cowshed, and proximity to larval habitats, were recorded. Of the 191,378 mosquitoes collected, 95% were identified morphologically to species and comprised 25 species from 5 genera. Common species included Anopheles arabiensis (53.5%), Culex quinquefasciatus (35.5%), An. pharoensis (4.7%), An. coustani (2.5%), and An. funestus (1.6%). Shannon's species diversity and evenness indices did not differ significantly among the 3 study sites. There was a marked house-to-house variation in the average number of mosquitoes captured. The number of people sleeping in the house the night preceding collection, size of eaves, distance to the cowshed, and the nearest larval habitat were significant predictors of occurrence of either or both An. arabiensis and Cx. quinquefasciatus. The peak abundance of An. arabiensis coincided with land preparation and the first few weeks after transplanting of rice seedlings, and that of Cx. quinquefasciatus coincided with land preparation, late stage of rice development, and short rains. After transplanting of rice seedlings, the populations of Cx. quinquefasciatus were collected more outdoors than indoors, suggesting a shift from endophily to exophily. These results demonstrate that irrigated rice cultivation has a strong impact on mosquito species occurrence, distribution, abundance, and behavior, and that certain house characteristics increase the degree of human-vector contact.

Distribution of mosquito larvae within the paddy and its implication in larvicidal application in Mwea rice irrigation scheme, Central Kenya.

Distribution of mosquito larvae in inundated rice fields is poorly known despite its profound implications in implementation of vector control programs. Based on oviposition behavior of gravid females and biotic and abiotic conditions of the rice field, distribution of mosquito larvae within the paddy may vary greatly. As a guide to implementation of mosquito vector control program targeting the aquatic stages in the rice fields in Mwea, studies were conducted to determine the distribution of mosquito larvae within the paddy. Twenty-eight cages measuring 50 cm3 were distributed randomly within the paddy during the transplanting stage of the rice growth cycle, and were examined twice per week up to the flowering stage to determine mosquito oviposition pattern. A total of 17,218 mosquito larvae were collected at the periphery and a further 17,570 at the center of the paddy. These comprised 7,461 larvae from the genus Anopheles and 27,327 from genus Culex. The number of pupae collected at the periphery was 1,004 and 1.5 times greater than the number collected at the center. Significantly higher counts of Anopheles larvae were collected at the center (1.00 +/- 0.11) than at the periphery (0.55 +/- 0.05) of the paddy during transplanting stage, but the difference was not significant during the tillering stage. In contrast, significantly higher numbers of Culex larvae were collected from the periphery (3.09 +/- 0.39) than at the center (2.81 +/- 0.24) of the paddy. More pupae were also collected at the center than at the periphery of the paddy. These findings indicate the distribution of Anopheles and Culex larvae in rice fields to be nonrandom; however, for successful achievement of an integrated vector control program targeting the diverse mosquito fauna occurring in rice fields, there is need to target the whole paddy for larvicidal application.

Larval habitat dynamics and diversity of Culex mosquitoes in rice agro-ecosystem in Mwea, Kenya.

Introduction of irrigation projects in developing nations has often been blamed for aggravating the problem of mosquito-borne diseases by creating ideal larval habitats for vector mosquitoes. However, whereas several studies have demonstrated the relationship between malaria vectors and irrigation, little work has been done on culicine mosquitoes despite their potential in transmission of filariasis and arboviruses and their significant biting nuisance in these areas. This study examined the diversity of Culex mosquito fauna and their larval habitats at two sites (Murinduko and Kiamachiri) in Mwea, Kenya over a 12-month period. The habitat types present at each site within a 200-meter radius around the study village, including randomly selected paddies and canals, were sampled every two weeks to examine the relationship between vegetation cover, water depth, turbidity, and Culex larval counts. Ten culicine species belonging to four genera were identified, with 73.1% of the total collection comprising of Culex duttoni and Cx. quinquefasciatus. Other species collected included Cx. annulioris, Cx. poicilipes, Cx. cinereus, Cx. tigripes, Cx. trifilatus, Aedes spp., Coquilettidia fuscopennata, and Ficalbia splendens. Murinduko was more diverse than Kiamachiri in terms of species richness (10 versus 7 species) and larval habitat diversity (11 versus 8 habitat types). Paddies, canals, and rain pools were the most diverse habitats in terms of species richness, and ditches, rock pools, and tree holes were the least diverse. Principal component and correlation analyses showed a strong association between three Culex species and the measured habitat characteristics. Culex poicilipes was strongly associated with floating vegetation, Cx. annulioris with clean water containing emergent vegetation, and Cx. quinquefasciatus was associated with turbid water. Seasonal changes in larval counts in water reservoirs and pool and ditch habitats were closely associated with rainfall. These findings provide important information on larval habitat preference for different Culex species, which will be useful in designing and implementation of larval control operations.

Environmental covariates of Anopheles arabiensis in a rice agroecosystem in Mwea, Central Kenya.

Water quality of aquatic habitats is an important determinant of female mosquito oviposition and successful larval development. This study examined the influence of environmental covariates on Anopheles arabiensis mosquito abundance in the Mwea Irrigation Scheme, Central Province of Kenya, prior to implementation of a malaria vector control program. Experimental rice plots were used to examine the environmental covariates responsible for regulating abundance and diversity of the aquatic stages of malaria vectors. Mosquito larval sampling and water quality analysis were done weekly from the flooding stage to the rice maturation stage. Sampling for mosquito larvae was conducted using standard dipping technique. During each larval collection, environmental covariates such as pH, temperature, conductivity, salinity, dissolved oxygen, water depth, and rice stage were measured. Anopheles arabiensis larval density was highest between 1 wk before transplanting and 4 wk after transplanting with peaks at weeks 0, 3, and 8. The fluctuation in values of the various environmental covariates showed characteristic patterns in different rice growth phases depending on the changes taking place due to the agronomic practices. Using a backward linear regression model, the factors that were found to be associated with abundance of An. arabiensis larvae at any of the rice growing phases included the following: dissolved oxygen, pH, turbidity, water depth, rice height, number of rice tillers, salinity, conductivity, and temperature. The environmental covariates associated with abundance of An. arabiensis were associated with early vegetative stage of the rice growth. For effective control of developmental stages of mosquito larvae, the application of larvicides should be done at the vegetative stage and the larvicides should persist until the beginning of the reproductive stage of the rice.

A grid-based infrastructure for ecological forecasting of rice land Anopheles arabiensis aquatic larval habitats.

BACKGROUND: For remote identification of mosquito habitats the first step is often to construct a discrete tessellation of the region. In applications where complex geometries do not need to be represented such as urban habitats, regular orthogonal grids are constructed in GIS and overlaid on satellite images. However, rice land vector mosquito aquatic habitats are rarely uniform in space or character. An orthogonal grid overlaid on satellite data of rice-land areas may fail to capture physical or man-made structures, i.e paddies, canals, berms at these habitats. Unlike an orthogonal grid, digitizing each habitat converts a polygon into a grid cell, which may conform to rice-land habitat boundaries. This research illustrates the application of a random sampling methodology, comparing an orthogonal and a digitized grid for assessment of rice land habitats. METHODS: A land cover map was generated in Erdas Imagine V8.7 using QuickBird data acquired July 2005, for three villages within the Mwea Rice Scheme, Kenya. An orthogonal grid was overlaid on the images. In the digitized dataset, each habitat was traced in Arc Info 9.1. All habitats in each study site were stratified based on levels of rice stage RESULTS: The orthogonal grid did not identify any habitat while the digitized grid identified every habitat by strata and study site. An analysis of variance test indicated the relative abundance of An. arabiensis at the three study sites to be significantly higher during the post-transplanting stage of the rice cycle. CONCLUSION: Regions of higher Anopheles abundance, based on digitized grid cell information probably reflect underlying differences in abundance of mosquito habitats in a rice land environment, which is where limited control resources could be concentrated to reduce vector abundance.

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.

Dry season ecology of Anopheles gambiae complex mosquitoes at larval habitats in two traditionally semi-arid villages in Baringo, Kenya.

BACKGROUND: Pre-adult stages of malaria vectors in semi-arid areas are confronted with highly variable and challenging climatic conditions. The objective of this study was to determine which larval habitat types are most productive in terms of larval densities in the dry and wet seasons within semi-arid environments, and how vector species productivity is partitioned over time. METHODS: Larval habitats were mapped and larvae sampled longitudinally using standard dipping techniques. Larvae were identified to species level morphologically using taxonomic keys and to sub-species by polymerase chain reaction (PCR) methods. Physical characteristics of larval habitats, including water depth, turbidity, and presence of floating and emergent vegetation were recorded. Water depth was measured using a metal ruler. Turbidity, pH, conductivity, dissolved oxygen, temperatures salinity and total dissolved solids (TDS) were measured in the field using the hand-held water chemistry meters. RESULTS: Mean larval densities were higher in the dry season than during the wet season but the differences in density were not statistically significant (F = 0.04, df = 1, p = 0.8501). Significantly higher densities of larvae were collected in habitats that were shaded and holding turbid, temporary and still water. Presence of emergent or floating vegetation, habitat depth, habitat size and habitat distance to the nearest house did not significantly affect larval density in both villages. There was a weakly positive relationship between larval density and salinity (r = 0.19, p < 0.05), conductivity (r = 0.05, p = 0.45) and total dissolved solids (r = 0.17, p < 0.05). However, the relationship between water temperature and larval density was weakly negative (r = 0.15, p = 0.35). All statistical tests were significant at alpha = 0.05. CONCLUSION: Breeding of malaria vector mosquitoes in Baringo is driven by predominantly human-made and permanent breeding sites in which Anopheles arabiensis and Anopheles funestus breed at a low level throughout the year. Permanent water sources available during the dry season serve as inocula by providing "larval seed" to freshly formed rain-fed habitats during the rainy season. The highly localized and focal nature of breeding sites in these semi-desert environments provides a good opportunity for targeted larval control since the habitats are few, well-defined and easily traceable.

Spatiotemporal dynamics of immature culicines (subfamily Culicinae) and their larval habitats in Mwea Rice Scheme, Kenya.

An ecological study was conducted at three study sites in Mwea Rice Scheme, Kenya to identify the diverse aquatic habitats in which culicine mosquitoes thrived and to explore the best strategies for mosquito control in the area. During the 11-month study period, ten habitat categories and 11 culicine species mainly dominated by Culex quinquefasciatus (72.0%) and Culex annulioris (17.9%) were identified from pupae and late instars larval samples. Two of the 11 culicine species, Ficalbia (Mimomyia) plumosa and Uranotaenia spp., have not been reported previously in the study area. Rurumi had more habitat types than either of the other study sites but the least number of mosquito species. In contrast, Karima had the least number of habitat types but significantly higher density of early instars than the other study sites. The relative abundance of late instars and pupae did not vary significantly among study sites. The contribution of different habitat types to larval production varied markedly between seasons and among study sites. Paddies and canals were perennial contributors of culicine mosquito larvae while the other habitat types were important mainly during the wet season. Some habitat types such as ditches, seeps, marshes, and fishpond were absent in some study sites but of great significance in other study sites. C. quinquefasciatus was positively associated with turbidity at all study sites and also negatively associated with emergent vegetation and distance to the nearest homestead in Karima, emergent vegetation in Kiuria, and other aquatic invertebrates in Rurumi. C. annulioris was positively associated with emergent vegetation at all study sites and also with depth in Kiuria. These findings indicate that besides rice fields and associated habitats, a diversity of other aquatic habitats contribute to culicine adult mosquito production in the study area and that environmental factors that determine the occurrence of a particular mosquito species may vary significantly even among areas of similar land use. This information is critical when designing and implementing mosquito larval control programs.