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.     

Influence of soil quality in the larval habitat on development of Anopheles gambiae Giles.

Larval ecology is an important aspect of the population dynamics of anopheline mosquitoes (Diptera: Culicidae), the vectors of malaria. Anopheles larvae live in pools of stagnant water and adult fitness may be correlated with the nutritional conditions under which larvae develop. A study was conducted in Mbita, Western Kenya, to investigate how properties of the soil substrate of Anopheles gambiae breeding pools can influence development of this mosquito species. An. gambiae eggs from an established colony were dispensed into experimental plastic troughs containing soil samples from a range of natural Anopheles larval habitats and filtered Lake Victoria water. The duration of larval development (8-15 days), pupation rate (0-79%), and adult body size (20.28-26.91 mm3) varied among different soil types. The total organic matter (3.61-21.25%), organic carbon (0.63-7.18%), and total nitrogen (0.06-0.58%) levels of the soils were positively correlated with pupation rate and negatively correlated with development time and adult body size.     

Resistance of early midgut stages of natural Plasmodium falciparum parasites to high temperatures in experimentally infected Anopheles gambiae (Diptera: Culicidae)

We studied the effects of high temperature, 30 and 32 versus 27 C on early Plasmodium falciparum development in Anopheles gambiae experimentally infected with gametocytes from 30 volunteers with mean density of 264.1 gametocytes/microl blood (range: 16-1,536/microl). From several batches of mosquitoes, fed by membrane feeding, midguts of individual mosquitoes were dissected at 24 hr for ookinete enumeration and at 7 days to quantify oocysts. There were temperature-related differences in mean ookinete intensity per mosquito midgut, with 9.71 +/- 1.6 at 27 C, 9.85 +/- 2.32 at 30 C, and 3.89 +/- 0.81 at 32 C. The prevalence of oocyst infection decreased with an increase in temperatures from 15.9 to 8.5 to 6.4% at 27, 30, and 32 C, respectively. The average oocyst intensities for the infected mosquitoes increased with temperatures from 2.9 at 27 C to 3.5 at 30 C, and to 3.3 at 32 C. However, the success of infections was reduced at 30 and 32 C, and resulted in greater losses during consecutive inter-stage parasite development. The most significant impact of high temperatures occurred at the transition between macrogametocytes and ookinetes, whereas the transition between ookinetes and oocysts apparently was not affected. In contrast to other reports, exposure of mosquitoes infected with natural parasites to high temperatures did not eliminate preoocyst stages, as has been observed from laboratory studies using the NF-54 strain of P. falciparum. This observation of parasite resistance to high temperatures is consistent with the natural situation in tropical environments where perennial malaria transmission occurs during hot dry seasons.     

Dynamics of gene introgression in the African malaria vector Anopheles gambiae

Anopheles gambiae is a major malaria vector in Africa and a popular model species for a variety of ecological, evolutionary, and genetic studies on vector control. Genetic manipulation of mosquito vectorial capacity is a promising new weapon for the control of malaria. However, the release of exotic transgenic mosquitoes will bring in novel alleles in addition to the parasite-inhibiting genes, which may have unknown effects on the local population. Therefore, it is necessary to develop methodologies that can be used to evaluate the spread rate of introduced genes in A. gambiae. In this study, the effects and dynamics of genetic introgression between two geographically distinct A. gambiae populations from western Kenya (Mbita) and eastern Tanzania (Ifakara) were investigated with amplified fragment length polymorphisms (AFLPs) and microsatellite markers. Microsatellites and polymorphic cDNA markers revealed a large genetic differentiation between the two populations (average F(ST) = 0.093, P < 0.001). When the two strains were crossed in random mating between the two populations, significant differences in the rate of genetic introgression were found in the mixed populations. Allele frequencies of 18 AFLP markers (64.3%) for Mbita and of 26 markers (92.9%) for Ifakara varied significantly from F5 to F20. This study provides basic information on how a mosquito release program would alter the genetic makeup of natural populations, which is critical for pilot field testing and ecological risk evaluation of transgenic mosquitoes.     

The association between distance to water pipes and water bodies positive for anopheline mosquitoes (Diptera: Culicidae) in the urban community of Malindi, Kenya.

The increasing risk of mosquito-borne diseases in African urban environments has been partly attributed to failed planning and resource underdevelopment. Though engineered systems may reduce mosquito proliferation, there are few studies describing this relationship. This study investigates how engineered systems such as roads and piped water systems affect the odds of anopheline immatures (i.e., larvae and pupae) occurring in water bodies located in Malindi, Kenya. Anopheles gambiae s.s. (Giles), An. arabiensis (Patton), and An. merus (Dointz) were identified in urban Malindi, with Anopheles gambiae s.s. being the predominant species identified. The Breslow-Day test was used to explore interactions among independent variables. Logistic regression was used to test whether water bodies positive for anopheline immatures are associated with engineered systems, while controlling for potential confounding and interaction effects associated with urban water body characteristics. Water bodies more than 100 m from water pipes were 13 times more likely to have anopheline immatures present, compared to water bodies that were less than 100 m from water pipes (OR = 13.54, 95% CI: 3.15-58.23). Roads were not significantly associated with water bodies positive for anopheline immatures. Statistical interaction was detected between water body substrate type and distance to water pipes. This study provides insight into how water pipes influence the distribution of water bodies positive with immature anophelines in urban environments.     

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

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 non-paddy 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.     

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.     

Quantitative trait loci controlling refractoriness to Plasmodium falciparum in natural Anopheles gambiae mosquitoes from a malaria-endemic region in western Kenya

Natural anopheline populations exhibit much variation in ability to support malaria parasite development, but the genetic mechanisms underlying this variation are not clear. Previous studies in Mali, West Africa, identified two quantitative trait loci (QTL) in Anopheles gambiae mosquitoes that confer refractoriness (failure of oocyst development in mosquito midguts) to natural Plasmodium falciparum parasites. We hypothesize that new QTL may be involved in mosquito refractoriness to malaria parasites and that the frequency of natural refractoriness genotypes may be higher in the basin region of Lake Victoria, East Africa, where malaria transmission intensity and parasite genetic diversity are among the highest in the world. Using field-derived F2 isofemale families and microsatellite marker genotyping, two loci significantly affecting oocyst density were identified: one on chromosome 2 between markers AG2H135 and AG2H603 and the second on chromosome 3 near marker AG3H93. The first locus was detected in three of the five isofemale families studied and colocalized to the same region as Pen3 and pfin1 described in other studies. The second locus was detected in two of the five isofemale families, and it appears to be a new QTL. QTL on chromosome 2 showed significant additive effects while those on chromosome 3 exhibited significant dominant effects. Identification of P. falciparum-refractoriness QTL in natural An. gambiae mosquitoes is critical to the identification of the genes involved in malaria parasite transmission in nature and for understanding the coevolution between malaria parasites and mosquito vectors.