Harrysone Atieli

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.

Anopheline larval habitats seasonality and species distribution: a prerequisite for effective targeted larval habitats control programmes.

Background Larval control is of paramount importance in the reduction of malaria vector abundance and subsequent disease transmission reduction. Understanding larval habitat succession and its ecology in different land use managements and cropping systems can give an insight for effective larval source management practices. This study investigated larval habitat succession and ecological parameters which influence larval abundance in malaria epidemic prone areas of western Kenya. Methods and Findings A total of 51 aquatic habitats positive for anopheline larvae were surveyed and visited once a week for a period of 85 weeks in succession. Habitats were selected and identified. Mosquito larval species, physico-chemical parameters, habitat size, grass cover, crop cycle and distance to nearest house were recorded. Polymerase chain reaction revealed that An. gambiae s.l was the most dominant vector species comprised of An.gambiae s.s (77.60%) and An.arabiensis (18.34%), the remaining 4.06% had no amplification by polymerase chain reaction. Physico-chemical parameters and habitat size significantly influenced abundance of An. gambiae s.s (P = 0.024) and An. arabiensis (P = 0.002) larvae. Further, larval species abundance was influenced by crop cycle (P≤0.001), grass cover (P≤0.001), while distance to nearest houses significantly influenced the abundance of mosquito species larvae (r = 0.920;P≤0.001). The number of predator species influenced mosquito larval abundance in different habitat types. Crop weeding significantly influenced with the abundance of An.gambiae s.l (P≤0.001) when preceded with fertilizer application. Significantly higher anopheline larval abundance was recorded in habitats in pasture compared to farmland (P = 0.002). When habitat stability and habitat types were considered, hoof print were the most productive followed by disused goldmines. Conclusion These findings suggest that implementation of effective larval control programme should be targeted with larval habitats succession information when larval habitats are fewer and manageable. Crop cycles and distance from habitats to household should be considered as effective information in planning larval control.

Habitat stability and occurrences of malaria vector larvae in western Kenya highlands

BackgroundAlthough the occurrence of malaria vector larvae in the valleys of western Kenya highlands is well documented, knowledge of larval habitats in the uphill sites is lacking. Given that most inhabitants of the highlands actually dwell in the uphill regions, it is important to develop understanding of mosquito breeding habitat stability in these sites in order to determine their potential for larval control.MethodsA total of 128 potential larval habitats were identified in hilltops and along the seasonal streams in the Sigalagala area of Kakamega district, western Kenya. Water availability in the habitats was followed up daily from August 3, 2006 to February 23, 2007. A habitat is defined as stable when it remains aquatic continuously for at least 12 d. Mosquito larvae were observed weekly. Frequencies of aquatic, stable and larvae positive habitats were compared between the hilltop and seasonal stream area using χ2-test. Factors affecting the presence/absence of Anopheles gambiae larvae in the highlands were determined using multiple logistic regression analysis.ResultsTopography significantly affected habitat availability and stability. The occurrence of aquatic habitats in the hilltop was more sporadic than in the stream area. The percentage of habitat occurrences that were classified as stable during the rainy season is 48.76% and 80.79% respectively for the hilltop and stream area. Corresponding frequencies of larvae positive habitats were 0% in the hilltop and 5.91% in the stream area. After the rainy season, only 23.42% of habitat occurrences were stable and 0.01% larvae positive habitats were found in the hilltops, whereas 89.75% of occurrences remained stable in the stream area resulting in a frequency of 12.21% larvae positive habitats. The logistic regression analysis confirmed the association between habitat stability and larval occurrence and indicated that habitat surface area was negatively affecting the occurrence of An. gambiae larvae. While An. gambiae and An. funestus larvae occurred throughout the study period along the streams, a total of only 15 An. gambiae larvae were counted in the hilltops, and no An. funestus were found. Moreover, no larvae managed to develop into adults in the hilltops, and the density of adult An. gambiae was consistently low, averaging at 0.06 females per house per survey.ConclusionThe occurrence of malaria vector larvae in the hilltop area was uncommon as a result of the low availability and high instability of habitats. To optimize the cost-effectiveness of malaria interventions in the western Kenya highlands, larval control should be focused primarily along the streams, as these are likely the only productive habitats at high altitude.

Evaluation of universal coverage of insecticide-treated nets in western Kenya: field surveys

BackgroundMass distribution of insecticide-treated nets (ITNs) is a cost-effective way to achieve universal coverage, but maintaining this coverage is more difficult. In addition to commonly used indicators, evaluation of universal coverage should include coverage of effective nets and changes in coverage over time.MethodsLongitudinal and cross-sectional household ITN surveys were carried out from 2010 to 2013 in six locations representing a variety of settings across western Kenya. Five indicators were used to evaluate the current status of universal coverage: 1) ITN ownership – proportion of households that own at least one ITN, 2) access index – ratio of the number of family members over the number of ITNs owned by that household, 3) operational coverage – proportion of the at-risk population potentially covered by ITNs, assuming one ITN for every two people, 4) effective coverage – population coverage of effective ITNs, and 5) usage – proportion of the population that used ITNs the previous night.ResultsITN ownership and operational coverage increased substantially from 2010 to 2013, but this increase was mostly due to the 2011 mass distribution campaign. In 2013, household ITN ownership was on average 84.4% (95% CI [78.4, 90.5]) across the six study areas, and operational coverage was 83.2% (95% CI [72.5, 93.8]). The ITN access rate was 59.1% (95% CI [56.6, 61.7]), and 40.8% (95% CI [38.3, 43.4]) of the people at risk needed more nets to achieve universal coverage. About 88.5% (95% CI [86.1, 90.9]) of the ITNs were below three years old and 16.5% (95% CI [12.1, 20.9]) of the ITNs had hole(s). The estimated effective long-lasting insecticide-treated net (LLIN) coverage was 70.5% (95 CI [58.7, 82.3]). Approximately 18.4% (95% CI [15.5, 21.4]) of the ITNs were shared by more than three persons, and the population ITN usage rate was about 75-87%. The reason for not using ITNs was almost exclusively “net not available”.ConclusionCurrent methods of delivering ITNs, i.e., one mass campaign every five years and regular distribution of ITNs from health center can barely maintain the current effective coverage. Inaccessibility and loss of physical integrity of ITNs are major hindrances to achieving and maintaining universal coverage.

Modest additive effects of integrated vector control measures on malaria prevalence and transmission in western Kenya

BackgroundThe effect of integrating vector larval intervention on malaria transmission is unknown when insecticide-treated bed-net (ITN) coverage is very high, and the optimal indicator for intervention evaluation needs to be determined when transmission is low.MethodsA post hoc assignment of intervention-control cluster design was used to assess the added effect of both indoor residual spraying (IRS) and Bacillus-based larvicides (Bti) in addition to ITN in the western Kenyan highlands in 2010 and 2011. Cross-sectional, mass parasite screenings, adult vector populations, and cohort of active case surveillance (ACS) were conducted before and after the intervention in three study sites with two- to three-paired intervention-control clusters at each site each year. The effect of larviciding, IRS, ITNs and other determinants of malaria risk was assessed by means of mixed estimating methods.ResultsAverage ITN coverage increased from 41% in 2010 to 92% in 2011 in the study sites. IRS intervention had significant added impact on reducing vector density in 2010 but the impact was modest in 2011. The effect of IRS on reducing parasite prevalence was significant in 2011 but was seasonal specific in 2010. ITN was significantly associated with parasite densities in 2010 but IRS application was significantly correlated with reduced gametocyte density in 2011. IRS application reduced about half of the clinical malaria cases in 2010 and about one-third in 2011 compare to non-intervention areas.ConclusionCompared with a similar study conducted in 2005, the efficacy of the current integrated vector control with ITN, IRS, and Bti reduced three- to five-fold despite high ITN coverage, reflecting a modest added impact on malaria transmission. Additional strategies need to be developed to further reduce malaria transmission.

Insecticide-Treated Net Campaign and Malaria Transmission in Western Kenya: 2003–2015

Insecticide-treated nets (ITNs) are among the three major intervention measures that have reduced malaria transmission in the past decade. However, increased insecticide resistance in vectors, together with outdoor transmission, has limited the efficacy of the ITN scaling-up efforts. Observations on longitudinal changes in ITN coverage and its impact on malaria transmission allow policy makers to make informed adjustments to control strategies. We analyzed field surveys on ITN ownership, malaria parasite prevalence, and malaria vector population dynamics in seven sentinel sites in western Kenya from 2003 to 2015. We found that ITN ownership has increased from an average of 18% in 2003 to 85% in 2015. Malaria parasite prevalence in school children decreased by about 70% from 2003 to 2008 (the first mass distribution of free ITNs was in 2006) but has resurged by >50% since then. At the community level, use of ITNs reduced infections by 23% in 2008 and 43% in 2010, although the reduction was down to 25% in 2011. The indoor-resting density of the predominant vector, Anopheles gambiae, has been suppressed since 2007; however, Anopheles funestus populations have resurged and have increased 20-fold in some places since 2007. In conclusion, there is limited room for further increase in ITN coverage in western Kenya. The rebounding in malaria transmission highlights the urgent need of new or improved malaria control interventions so as to further reduce malaria transmission.

Impacts of Antimalarial Drugs on Plasmodium falciparum Drug Resistance Markers, Western Kenya, 2003–2015

Abstract. Antimalarial drug resistance has threatened global malaria control since chloroquine (CQ)-resistant Plasmodium falciparum emerged in Asia in the 1950s. Understanding the impacts of changing antimalarial drug policy on resistance is critical for resistance management. Plasmodium falciparum isolates were collected from 2003 to 2015 in western Kenya and analyzed for genetic markers associated with resistance to CQ (Pfcrt), sulfadoxine–pyrimethamine (SP) (Pfdhfr/Pfdhps), and artemether–lumefantrine (AL) (PfKelch13/Pfmdr1) antimalarials. In addition, household antimalarial drug use surveys were administered. Pfcrt 76T prevalence decreased from 76% to 6% from 2003 to 2015. Pfdhfr/Pfdhps quintuple mutants decreased from 70% in 2003 to 14% in 2008, but increased to near fixation by 2015. SP “super resistant” alleles Pfdhps 581G and 613S/T were not detected in the 2015 samples that were assessed. The Pfmdr1 N86-184F-D1246 haplotype associated with decreased lumefantrine susceptibility increased significantly from 4% in 2005 to 51% in 2015. No PfKelch13 mutations that have been previously associated with artemisinin resistance were detected in the study populations. The increase in Pfdhfr/Pfdhps quintuple mutants that associates with SP resistance may have resulted from the increased usage of SP for intermittent preventative therapy in pregnancy (IPTp) and for malaria treatment in the community. Prevalent Pfdhfr/Pfdhps mutations call for careful monitoring of SP resistance and effectiveness of the current IPTp program in Kenya. In addition, the commonly occurring Pfmdr1 N86-184F-D1246 haplotype associated with increased lumefantrine tolerance calls for surveillance of AL efficacy in Kenya, as well as consideration for a rotating artemisinin-combination therapy regimen.

Emerging Pyrethroid Resistance among Anopheles arabiensis in Kenya.

Abstract. Vector control programs, particularly in the form of insecticide-treated bed nets (ITNs), are essential for achieving malaria elimination goals. Recent reports of increasing knockdown resistance (kdr) mutation frequencies for Anopheles arabiensis in Western Kenya heightens the concern on the future effectiveness of ITNs in Kenya. We examined resistance in An. arabiensis populations across Kenya through kdr mutations and World Health Organization–recommended bioassays. We detected two kdr alleles, L1014F and L1014S. Kdr mutations were found in five of the 11 study sites, with mutation frequencies ranging from 3% to 63%. In two Western Kenya populations, the kdr L1014F allele frequency was as high as 10%. The L1014S frequency was highest at Chulaimbo at 55%. Notably, the kdr L1014F mutation was found to be associated with pyrethroid resistance at Port Victoria, but kdr mutations were not significantly associated with resistance at Chulaimbo, which had the highest kdr mutation frequency among all sites. This study demonstrated the emerging pyrethroid resistance in An. arabiensis and that pyrethroid resistance may be related to kdr mutations. Resistance monitoring and management are urgently needed for this species in Kenya where resistance is emerging and its abundance is becoming predominant. Kdr mutations may serve as a biomarker for pyrethroid resistance in An. arabiensis.