Noboru Minakawa

Changing Patterns of Malaria Epidemiology between 2002 and 2010 in Western Kenya: The Fall and Rise of Malaria

Background The impact of insecticide treated nets (ITNs) on reducing malaria incidence is shown mainly through data collection from health facilities. Routine evaluation of long-term epidemiological and entomological dynamics is currently unavailable. In Kenya, new policies supporting the provision of free ITNs were implemented nationwide in June 2006. To evaluate the impacts of ITNs on malaria transmission, we conducted monthly surveys in three sentinel sites with different transmission intensities in western Kenya from 2002 to 2010. Methods and Findings Longitudinal samplings of malaria parasite prevalence in asymptomatic school children and vector abundance in randomly selected houses were undertaken monthly from February 2002. ITN ownership and usage surveys were conducted annually from 2004 to 2010. Asymptomatic malaria parasite prevalence and vector abundances gradually decreased in all three sites from 2002 to 2006, and parasite prevalence reached its lowest level from late 2006 to early 2007. The abundance of the major malaria vectors, Anopheles funestus and An. gambiae, increased about 5–10 folds in all study sites after 2007. However, the resurgence of vectors was highly variable between sites and species. By 2010, asymptomatic parasite prevalence in Kombewa had resurged to levels recorded in 2004/2005, but the resurgence was smaller in magnitude in the other sites. Household ITN ownership was at 50–70% in 2009, but the functional and effective bed net coverage in the population was estimated at 40.3%, 49.4% and 28.2% in 2010 in Iguhu, Kombewa, and Marani, respectively. Conclusion The resurgence in parasite prevalence and malaria vectors has been observed in two out of three sentinel sites in western Kenya despite a high ownership of ITNs. The likely factors contributing to malaria resurgence include reduced efficacy of ITNs, insecticide resistance in mosquitoes and lack of proper use of ITNs. These factors should be targeted to avoid further resurgence of malaria transmission.

Unforeseen misuses of bed nets in fishing villages along Lake Victoria

BackgroundTo combat malaria, the Kenya Ministry of Health and nongovernmental organizations (NGOs) have distributed insecticide-treated nets (ITNs) for use over beds, with coverage for children under five years of age increasing rapidly. Nevertheless, residents of fishing villages have started to use these bed nets for drying fish and fishing in Lake Victoria. This study investigated the extent of bed net misuse in fishing villages.MethodsSeven fishing villages along the lake were surveyed to estimate how widely bed nets were being used for fishing and drying fish. Villagers were asked why they used the bed nets for such purposes.ResultsIn total, 283 bed nets were being used for drying fish. Of these, 239 were long-lasting insecticidal bed nets (LLIN) and 44 were non-long-lasting insecticidal bed nets (NLLIN). Further, 72 of the 283 bed nets were also being used for fishing. The most popular reasons were because the bed nets were inexpensive or free and because fish dried faster on the nets. LLINs were preferred to NLLINs for fishing and drying fish.ConclusionThere is considerable misuse of bed nets for drying fish and fishing. Many villagers are not yet fully convinced of the effectiveness of LLINs for malaria prevention. Such misuses may hamper the efforts of NGOs and governmental health organizations.

Effects of Larval Competitors and Predators on Oviposition Site Selection of Anopheles gambiae Sensu Stricto

Abstract We examined whether predators and competitors influence selection of oviposition sites by Anopheles gambiae Giles. Mosquitoes in cages laid significantly fewer eggs in rainwater conditioned with a predator (backswimmers, Notonecta sp.) than in unconditioned rainwater. Rainwater conditioned with a putative competitor (tadpoles, Xenopus sp.) also had fewer eggs than unconditioned rainwater. Similarly, mosquitoes laid significantly fewer eggs in rainwater conditioned with five and 50 An. gambiae larvae than in unconditioned rainwater. When larvae were present, significantly more eggs were laid in containers with five larvae than in containers with higher densities, but the differences in number of eggs laid were not significant among the densities of 40, 70, and 100 larvae. This study demonstrated that caged An. gambiae females avoid oviposition in habitats with supposed competitors and predators.

Plasmodium falciparum Spatial Analysis, Western Kenya Highlands

Parasite transmission is intense in the highlands, and these areas are vulnerable to epidemics.

Multimodal Pyrethroid Resistance in Malaria Vectors, Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus s.s. in Western Kenya

Anopheles gambiae s.s., Anopheles arabiensis, and Anopheles funestus s.s. are the most important species for malaria transmission. Pyrethroid resistance of these vector mosquitoes is one of the main obstacles against effective vector control. The objective of the present study was to monitor the pyrethroid susceptibility in the 3 major malaria vectors in a highly malaria endemic area in western Kenya and to elucidate the mechanisms of pyrethroid resistance in these species. Gembe East and West, Mbita Division, and 4 main western islands in the Suba district of the Nyanza province in western Kenya were used as the study area. Larval and adult collection and bioassay were conducted, as well as the detection of point mutation in the voltage-gated sodium channel (1014L) by using direct DNA sequencing. A high level of pyrethroid resistance caused by the high frequency of point mutations (L1014S) was detected in An. gambiae s.s. In contrast, P450-related pyrethroid resistance seemed to be widespread in both An. arabiensis and An. funestus s.s. Not a single L1014S mutation was detected in these 2 species. A lack of cross-resistance between DDT and permethrin was also found in An. arabiensis and An. funestus s.s., while An. gambiae s.s. was resistant to both insecticides. It is noteworthy that the above species in the same area are found to be resistant to pyrethroids by their unique resistance mechanisms. Furthermore, it is interesting that 2 different resistance mechanisms have developed in the 2 sibling species in the same area individually. The cross resistance between permethrin and DDT in An. gambiae s.s. may be attributed to the high frequency of kdr mutation, which might be selected by the frequent exposure to ITNs. Similarly, the metabolic pyrethroid resistance in An. arabiensis and An. funestus s.s. is thought to develop without strong selection by DDT.

The Indian Ocean Dipole and malaria risk in the highlands of western Kenya

Epidemics of malaria in the East African highlands in the last 2 decades have often been associated with climate variability, particularly the El Niño-Southern Oscillation (ENSO). However, there are other factors associated with malaria risk and there is increased interest in the influences of the Indian Ocean Dipole (IOD), a climate mode of coupled ocean–atmosphere variability, on East African rainfall. This study explores the relationship between IOD and the number of malaria patients in 7 hospitals from 2 districts in the western Kenyan highlands, controlling for the effects of ENSO. We examined temporal patterns (1982–2001) in the number of malaria cases in relation to the dipole mode index (DMI), defined as the difference in sea surface temperature anomaly between the western (10°S-10°N, 50°-70°E) and eastern (10°S-0°, 90°-110°E) tropical Indian Ocean. We used Poisson regression models, adjusted for ENSO index Niño 3 region (NINO3), seasonal and interannual variations. The number of malaria patients per month increased by 3.4%–17.9% for each 0.1 increase above a DMI threshold (3–4 months lag). Malaria cases increased by 1.4%–10.7% per month, for each 10 mm increase in monthly rainfall (2–3 months lag). In 6 of 7 places, there was no evidence of an association between NINO3 and the number of malaria cases after adjusting for the effect of DMI. This study suggests that the number of malaria cases in the western Kenyan highlands increases with high DMI in the months preceding hospital visits.

Community-wide benefits of targeted indoor residual spray for malaria control in the Western Kenya Highland

BackgroundInterest in indoor residual spray (IRS) has been rekindled in recent years, as it is increasingly considered to be a key component of integrated malaria management. Regular spraying of each human dwelling becomes less and less practical as the control area increases. Where malaria transmission is concentrated around focal points, however, targeted IRS may pose a feasible alternative to mass spraying. Here, the impact of targeted IRS was assessed in the highlands of western Kenya.MethodsIndoor residual spray using lambda-cyhalothrin insecticide was carried out during the last week of April 2005 in 1,100 targeted houses, located in the valley bottom areas of Iguhu village, Kakamega district of western Kenya. Although the uphill areas are more densely populated, valleys are believed to be malaria transmission hotspots. The aim of the study was to measurably reduce the vector density and malaria transmission in uphill areas by focusing control on these hotspots. A cohort of 1,058 children from 1-5 yrs of age was randomly selected from a 4 km by 6 km study area for the baseline malaria prevalence survey after pre-clearing malaria infections during the third week of April 2005, and the prevalence of Plasmodium infections was tested bi-weekly. Seasonal changes in mosquito densities 12 months before the IRS and 12 months after the IRS was monitored quarterly based on 300 randomly selected houses. Monthly parasitological surveys were also carried out in the same area with 129-661 randomly selected school children of age 6-13 yrs.ResultsThe result of monthly parasitological surveys indicated that malaria prevalence in school children was reduced by 64.4% in the intervention valley area and by 46.3% in the intervention uphill area after 12 months of follow-ups in contrast to nonintervention areas (valley or uphill). The cohort study showed an average of 4.5% fewer new infections biweekly in the intervention valley compare to nonintervention valley and the relative reduction in incidence rate by week 14 was 65.4%. The relative reduction in incidence rate in intervention uphill by week 14 was 46.4%. Anopheles gambiae densities were reduced by 96.8% and 51.6% in the intervention valley and intervention uphill, respectively, and Anopheles funestus densities were reduced by 85.3% and 69.2% in the intervention valley and intervention uphill, respectively.ConclusionVector control had significant indirect impact on the densely populated uphill areas when IRS was targeted to the high-risk valleys. Additionally, the wide-reaching benefits of IRS in reducing vector prevalence and disease incidence was observed for at least six months following spraying, suggesting targeted IRS as an effective tool in malaria control.

Land Use and Land Cover Changes and Spatiotemporal Dynamics of Anopheline Larval Habitats during a Four-Year Period in a Highland Community of Africa

Spatial and temporal variations in the distribution of anopheline larval habitats and land use and land cover (LULC) changes can influence malaria transmission intensity. This information is important for understanding the environmental determinants of malaria transmission heterogeneity, and it is critical to the study of the effects of environmental changes on malaria transmission. In this study, we investigated the spatial and temporal variations in the distribution of anopheline larval habitats and LULC changes in western Kenya highlands over a 4-year period. Anopheles gambiae complex larvae were mainly confined to valley bottoms during both the dry and wet seasons. Although An. gambiae larvae were located in man-made habitats where riparian forests and natural swamps had been cleared, Anopheles funestus larvae were mainly found in permanent habitats in pastures. The association between land cover type and occurrence of anopheline larvae was statistically significant. The distribution of anopheline positive habitats varied significantly between months, during the survey. In 2004, the mean density of An. gambiae was significantly higher during the month of May, whereas the density of An. funestus peaked significantly in February. Over the study period, major LULC changes occurred mostly in the valley bottoms. Overall, farmland increased by 3.9%, whereas both pastures and natural swamps decreased by 8.9% and 20.9%, respectively. The area under forest cover was decreased by 5.8%. Land-use changes in the study area are favorable to An. gambiae larval development, thereby risking a more widespread distribution of malaria vector habitats and potentially increasing malaria transmission in western Kenya highlands.

Indian Ocean Dipole drives malaria resurgence in East African highlands

Malaria resurgence in African highlands in the 1990s has raised questions about the underlying drivers of the increase in disease incidence including the role of El-Niño-Southern Oscillation (ENSO). However, climatic anomalies other than the ENSO are clearly associated with malaria outbreaks in the highlands. Here we show that the Indian Ocean Dipole (IOD), a coupled ocean-atmosphere interaction in the Indian Ocean, affected highland malaria re-emergence. Using cross-wavelet coherence analysis, we found four-year long coherent cycles between the malaria time series and the dipole mode index (DMI) in the 1990s in three highland localities. Conversely, we found a less pronounced coherence between malaria and DMI in lowland localities. The highland/lowland contrast can be explained by the effects of mesoscale systems generated by Lake Victoria on its climate basin. Our results support the need to consider IOD as a driving force in the resurgence of malaria in the East African highlands.

Reconsideration of Anopheles rivulorum as a vector of Plasmodium falciparum in western Kenya: some evidence from biting time, blood preference, sporozoite positive rate, and pyrethroid resistance.

BackgroundAnopheles gambiae, An. arabiensis, and An. funestus are widespread malaria vectors in Africa. Anopheles rivulorum is the next most widespread species in the An. funestus group. The role of An. rivulorum as a malaria vector has not been fully studied, although it has been found to be a minor or opportunistic transmitter of Plasmodium falciparum.MethodsMosquitoes were collected indoors over a 12-hour period using a light source attached to a rotating bottle collector in order to determine peak activity times and to provide DNA for meal source identification. Gravid female mosquitoes were collected indoors via an aspirator to generate F1 progeny for testing insecticidal susceptibility. Blood meal sources were identified using a multiplexed PCR assay for human and bovine cytochrome-B, and by matching sequences generated with primers targeting vertebrate and mammalian cytochrome-B segments to the Genbank database.ResultsAnopheles rivulorum fed on human blood in the early evening between 18:00 and 20:00, when insecticide-treated bed nets are not in use, and the presence of Plasmodium falciparum sporozoites in 0.70% of the An. rivulorum individuals tested was demonstrated. Susceptibility to permethrin, deltamethrin, and DDT is higher in An. rivulorum (84.8%, 91.4%, and 100%, respectively) than in An. funestus s.s. (36.8%, 36.4%, and 70%, respectively), whereas mortality rates for propoxur and fenitrothion were 100% for both species. Resistance to pyrethroids was very high in An. funestus s.s. and the potential of the development of high resistance was suspected in An. rivulorum.ConclusionGiven the tendency for An. rivulorum to be active early in the evening, the presence of P. falciparum in the species, and the potential for the development of pyrethroid resistance, we strongly advocate reconsideration of the latent ability of this species as an epidemiologically important malaria vector.