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BACKGROUND: This is the second in a series of three articles documenting the geographical distribution of 41 dominant vector species (DVS) of human malaria. The first paper addressed the DVS of the Americas and the third will consider those of the Asian Pacific Region. Here, the DVS of Africa, Europe and the Middle East are discussed. The continent of Africa experiences the bulk of the global malaria burden due in part to the presence of the An. gambiae complex. Anopheles gambiae is one of four DVS within the An. gambiae complex, the others being An. arabiensis and the coastal An. merus and An. melas. There are a further three, highly anthropophilic DVS in Africa, An. funestus, An. moucheti and An. nili. Conversely, across Europe and the Middle East, malaria transmission is low and frequently absent, despite the presence of six DVS. To help control malaria in Africa and the Middle East, or to identify the risk of its re-emergence in Europe, the contemporary distribution and bionomics of the relevant DVS are needed. RESULTS: A contemporary database of occurrence data, compiled from the formal literature and other relevant resources, resulted in the collation of information for seven DVS from 44 countries in Africa containing 4234 geo-referenced, independent sites. In Europe and the Middle East, six DVS were identified from 2784 geo-referenced sites across 49 countries. These occurrence data were combined with expert opinion ranges and a suite of environmental and climatic variables of relevance to anopheline ecology to produce predictive distribution maps using the Boosted Regression Tree (BRT) method. CONCLUSIONS: The predicted geographic extent for the following DVS (or species/suspected species complex*) is provided for Africa: Anopheles (Cellia) arabiensis, An. (Cel.) funestus*, An. (Cel.) gambiae, An. (Cel.) melas, An. (Cel.) merus, An. (Cel.) moucheti and An. (Cel.) nili*, and in the European and Middle Eastern Region: An. (Anopheles) atroparvus, An. (Ano.) labranchiae, An. (Ano.) messeae, An. (Ano.) sacharovi, An. (Cel.) sergentii and An. (Cel.) superpictus*. These maps are presented alongside a bionomics summary for each species relevant to its control.

BACKGROUND: Global maps, in particular those based on vector distributions, have long been used to help visualise the global extent of malaria. Few, however, have been created with the support of a comprehensive and extensive evidence-based approach. METHODS: Here we describe the generation of a global map of the dominant vector species (DVS) of malaria that makes use of predicted distribution maps for individual species or species complexes. RESULTS: Our global map highlights the spatial variability in the complexity of the vector situation. In Africa, An. gambiae, An. arabiensis and An. funestus are co-dominant across much of the continent, whereas in the Asian-Pacific region there is a highly complex situation with multi-species coexistence and variable species dominance. CONCLUSIONS: The competence of the mapping methodology to accurately portray DVS distributions is discussed. The comprehensive and contemporary database of species-specific spatial occurrence (currently available on request) will be made directly available via the Malaria Atlas Project (MAP) website from early 2012.

  [...]these studies are difficult to compare and impossible to synthesize globally. Records of the presence or absence of a DVS at a particular site and on a particular date were entered into the database so that information collected at different times from a locality was documented. Because abundance data have not been reported using methods that can be readily standardized across entomological surveys, only presence and absence data were used to generate the maps.\\n It is clear that subregional ecological diversity, coupled with the behavioural plasticity of many DVS, will require that any maps, and associated bionomics information provided, be interpreted and acted on cautiously with local expert knowledge.

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.

The Anopheles stephensi mosquito is an invasive malaria vector recently reported in Djibouti, Ethiopia, Sudan, Somalia, Nigeria, and Ghana. The World Health Organization has called on countries in Africa to increase surveillance efforts to detect and report this vector and institute appropriate and effective control mechanisms. In Kenya, the Division of National Malaria Program conducted entomological surveillance in counties at risk for An. stephensi mosquito invasion. In addition, the Kenya Medical Research Institute conducted molecular surveillance of all sampled Anopheles mosquitoes from other studies to identify An. stephensi mosquitoes. We report the detection and confirmation of An. stephensi mosquitoes in Marsabit and Turkana Counties by using endpoint PCR and morphological and sequence identification. We demonstrate the urgent need for intensified entomological surveillance in all areas at risk for An. stephensi mosquito invasion, to clarify its occurrence and distribution and develop tailored approaches to prevent further spread.

Background Integrated vector management (IVM) remains a key strategy in the fight against vector-borne diseases including malaria. However, impacts of the strategy should be regularly monitored based on feedback obtained through research. The objective of this study was to assess the impact of IVM for malaria control in Botor-Tolay district, southwestern Ethiopia after three years (2016–2018) of IVM implementation. Method Prior to the implementation of IVM, a survey of socio-demographic, malaria burden, and communities’ perception towards malaria control was conducted in 200 households selected at random from 12 villages using standard questionnaire. Households were revisited after three years of project implementation for impact assessment. Compiled malaria case data was obtained from district health bureau for the three years period of the study while adult mosquito collection was conducted during each year using CDC light traps. Monthly larval mosquito collections were made each year using standard dipping method. Community education and mobilization (CEM) was made through different community-based structures. Results The proportion of respondents who sought treatment in health facilities showed a significant increase from 76% in 2015 to 90% in 2018( P  < 0.001). An average of 6.3 working and 2.3 school days were lost per year in a household due to parents and children falling sick with malaria. Malaria costs in a household in Botor-Tolay averaged 13.3 and 4.5 USD per episode for medical treatment and transportation respectively. Significantly fewer adult mosquitoes were collected in 2018 (0.37/house/trap-night) as compared to 2015 (0.73/house/trap-night) ( P  < .001). Malaria cases significantly declined in 2018 (262) when compared to the record in 2015 (1162) ( P  < 0.001). Despite improved human behavioral changes towards mosquito and malaria control, there were many setbacks too. These include reluctance to seek treatment in a timely manner, low user compliance of LLINs and low net repairing habit. Conclusion The coordinated implementation of community-based education, environmental management, larviciding together with main core vector control interventions in Botor-Tolay district in Southwestern Ethiopia have contributed to significant decline in malaria cases reported from health facilities. However, commitment to seeking treatment by people with clinical symptoms of malaria and to repair of damaged mosquito nets remained low.

Background The rapid and widespread evolution of insecticide resistance has emerged as one of the major challenges facing malaria control programs in sub-Saharan Africa. Understanding the insecticide resistance status of mosquito populations and the underlying mechanisms of insecticide resistance can inform the development of effective and site-specific strategies for resistance prevention and management. The aim of this study was to investigate the insecticide resistance status of Anopheles gambiae ( s.l. ) mosquitoes from coastal Kenya. Methods Anopheles gambiae ( s.l. ) larvae sampled from eight study sites were reared to adulthood in the insectary, and 3- to 5-day-old non-blood-fed females were tested for susceptibility to permethrin, deltamethrin, dichlorodiphenyltrichloroethane (DDT), fenitrothion and bendiocarb using the standard World Health Organization protocol. PCR amplification of rDNA intergenic spacers was used to identify sibling species of the An. gambiae complex. The An. gambiae ( s.l. ) females were further genotyped for the presence of the L1014S and L1014F knockdown resistance (kdr) mutations by real-time PCR. Results Anopheles arabiensis was the dominant species, accounting for 95.2% of the total collection, followed by An. gambiae ( s.s. ), accounting for 4.8%. Anopheles gambiae ( s.l. ) mosquitoes were resistant to deltamethrin, permethrin and fenitrothion but not to bendiocarb and DDT. The L1014S kdr point mutation was detected only in An. gambiae ( s.s. ), at a low allelic frequency of 3.33%, and the 1014F kdr mutation was not detected in either An. gambiae ( s.s. ) or An. arabiensis . Conclusion The findings of this study demonstrate phenotypic resistance to pyrethroids and organophosphates and a low level of the L1014S kdr point mutation that may partly be responsible for resistance to pyrethroids. This knowledge may inform the development of insecticide resistance management strategies along the Kenyan Coast. Graphical Abstract

Background Malaria prevention in Africa is mainly through the use of long-lasting insecticide treated nets (LLINs). The objective of the study was to assess the effect of supplementing LLINs with either larviciding with Bacillus thuringiensis israelensis (Bti) or community education and mobilization (CEM), or with both interventions in the context of integrated vector management (IVM). Methods The study involved a factorial, cluster-randomized, controlled trial conducted in Malindi and Nyabondo sites in Kenya and Tolay site in Ethiopia, to assess the impact of the following four intervention options on mosquitoes and malaria prevalence: LLINs only (arm 1); LLINs and Bti (arm 2); LLINs and CEM (arm 3); and, LLINs combined with Bti and CEM (arm 4). Between January 2013 and December 2015, CDC light traps were used to sample adult mosquitoes during the second, third and fourth quarter of each year in 10 houses in each of 16 villages at each of the three study sites. Larvae were sampled once a fortnight from potential mosquito-breeding habitats using standard plastic dippers. Cross-sectional malaria parasite prevalence surveys were conducted involving a total of 11,846 primary school children during the 3-year period, including 4800 children in Tolay, 3000 in Malindi and 4046 in Nyabondo study sites. Results Baseline relative indoor anopheline density was 0.11, 0.05 and 0.02 mosquitoes per house per night in Malindi, Tolay and Nyabondo sites, respectively. Nyabondo had the highest recorded overall average malaria prevalence among school children at 32.4%, followed by Malindi with 5.7% and Tolay 1.7%. There was no significant reduction in adult anopheline density at each of the three sites, which could be attributed to adding of the supplementary interventions to the usage of LLINs. Malaria prevalence was significantly reduced by 50% in Tolay when using LLINs coupled with application of Bti, community education and mobilization. The two other sites did not reveal significant reduction of prevalence as a result of combining LLINs with any of the other supplementary interventions. Conclusion Combining LLINs with larviciding with Bti and CEM further reduced malaria infection in a low prevalence setting in Ethiopia, but not at sites with relatively higher prevalence in Kenya. More research is necessary at the selected sites in Kenya to periodically determine the suite of vector control interventions and broader disease management strategies, which when integrated would further reduce adult anopheline populations and malaria prevalence beyond what is achieved with LLINs.

Background Mosquito-proofing of houses using wire mesh screens is gaining greater recognition as a practical intervention for reducing exposure to malaria transmitting mosquitoes. Screening potentially protects all persons sleeping inside the house against transmission of mosquito-borne diseases indoors. The study assessed the effectiveness of house eaves screening in reducing indoor vector densities and malaria prevalence in Nyabondo, western Kenya. Methods 160 houses were selected for the study, with half of them randomly chosen for eaves screening with fibre-glass coated wire mesh (experimental group) and the other half left without screening (control group). Randomization was carried out by use of computer-generated list in permuted blocks of ten houses and 16 village blocks, with half of them allocated treatment in a ratio of 1:1. Cross-sectional baseline entomological and parasitological data were collected before eave screening. After baseline data collection, series of sampling of indoor adult mosquitoes were conducted once a month in each village using CDC light traps. Three cross-sectional malaria parasitological surveys were conducted at three month intervals after installation of the screens. The primary outcome measures were indoor Anopheles mosquito density and malaria parasite prevalence. Results A total of 15,286 mosquitoes were collected over the two year period using CDC light traps in 160 houses distributed over 16 study villages (mean mosquitoes = 4.35, SD = 11.48). Of all mosquitoes collected, 2,872 (18.8%) were anophelines (2,869 Anopheles gambiae sensu lato, 1 Anopheles funestus and 2 other Anopheles spp ). Overall, among An. gambiae collected, 92.6% were non-blood fed, 3.57% were blood fed and the remaining 0.47% were composed of gravid and half gravid females. More indoor adult mosquitoes were collected in the control than experimental arms of the study. Results from cross-sectional parasitological surveys showed that screened houses recorded relatively low malaria parasite prevalence rates compared to the control houses. Overall, malaria prevalence was 5.6% (95% CI: 4.2–7.5) n = 1,918, with baseline prevalence rate of 6.1% (95% CI: 3.9–9.4), n = 481 and 3 rd follow-up survey prevalence of 3.6% (95% CI: 2.0–6.8) n = 494. At all the three parasitological follow-up survey points, house screening significantly reduced the malaria prevalence by 100% ( p  < 0.001), 63.6% ( p  = 0.026), and 100% ( p  < 0.001) in the 1st, 2nd and 3rd follow-up surveys respectively. Conclusions The study demonstrated that house eave screening has potential to reduce indoor vector densities and malaria prevalence in high transmission areas.

The use of MALDI-TOF MS for mosquito identification and surveillance is routinely used in developed countries as an affordable alternative to molecular methods. However, in low- and middle-income countries (LMIC) where mosquito-borne diseases carry the greatest burden, the method is not commonly employed. Using the Kenyan national malaria program (NMCP) as a case study, we compared the costs of current methods used for malaria vector surveillance to those that would be incurred if MALDI-TOF MS were used instead. A deterministic decision tree analytic model was developed to systematically calculate the costs associated with materials and labour, and time-to-results for two workflows, i.e., current molecular methods versus MALDI-TOF MS. The analysis assumed an annual sample size of 15,000 mosquitoes (representing the average number of mosquitoes analysed annually by the Kenyan NMCP) processed at a local laboratory in Kenya. We estimate that if the Kenyan national entomological surveillance program shifted sample processing completely to MALDI-TOF MS, it would result in 74.48% net time saving, up to 84% on material costs and 77% on labour costs, resulting in an overall direct cost savings of 83%. Adoption of MALDI-TOF MS for malaria vector surveillance can result in substantial time and cost savings. The ease of performance, the rapid turn-around time, and the modest cost per sample may bring a paradigm shift in routine entomological surveillance in Africa.