Monitoring malaria vector densities and behaviours in Tanzania

Malaria remains the most important parasite-related public health problem globally, with the majority of burden occurring in sub Saharan Africa. Increased political and financial support has resulted in rapid scale up of malaria prevention measures, so that disease burden has been substantially reduced in many African countries. However, behavioural change by malaria vector populations, so that a greater proportion of human exposure to bites occurs outdoors, threatens to undermine the impact of malaria control with existing front line interventions such as insecticide treated nets (ITNs) and indoors residual spraying (IRS) because both act indoors. Also, progress towards lower transmission levels poses substantive entomological monitoring challenges because most standard methods fail to detect low levels of vector density and malaria transmission. The overall goal of this study was to enhance understanding of the potential and limitations of ITNs for reducing malaria transmission by outdoor biting mosquitoes, and to develop a safe, sensitive, practical and effective malaria vector surveillance tool that enables sustained entomologic monitoring of intervention impact. An existing mathematical model was adapted to examine the possibility that ITNs can achieve community suppression of malaria transmission exposure, even when mosquitoes avoid them by feeding on people while they are outdoors. Simulations indicated that ITNs may provide useful levels of community suppression of malaria transmission, even when outdoor biting rates exceed indoor biting rates and slightly more than half of bites occurred at times and places when using ITNs is not feasible. This suggests that ITNs should not be deprioritized as a malaria control tool simply because local vector species prefer to feed outdoors. Nevertheless, complementary interventions that target outdoor- and early-biting mosquitoes should be prioritized, especially for going beyond malaria control to achieve elimination. Cross over and Latin Squares experimental designs were used to compare the sensitivity of multiple trapping techniques for catching malaria vectors, under conditions of both high and low mosquito density, in rural Kilombero and urban Dar es Salaam, respectively. A new tent style trapping device called the Ifakara Tent Trap was successfully developed and proved to be safe and more efficacious than any other commonly used alternative to human landing catch for catching Anopheles gambiae s.l. in the low transmission setting of urban Dar es Salaam. Its sampling efficiency appeared to be independent of vector density in a rural setting with high mosquito abundance but increased as mosquito densities decreased in an urban area of low mosquito density where it exceeded that of HLC at lowest densities. This density- dependence of the trap implies that this tool may have particular potential for monitoring malaria in low transmission settings. It was also demonstrated to be effective when used by unsupervised community members under programmatic conditions and it is currently the only technique used for routine adult mosquito surveillance by the Urban Malaria Control Programme of Dar es Salaam. However, it cannot be used to determine how bites upon humans are distributed between indoor and outdoor exposure components

Identification of Entomological Drivers for Persisting High Malaria Transmission in Ruangwa District Lindi Region Tanzania

High malaria prevalence remains a major problem, despite high coverage rates of malaria control interventions. The study was carried out to investigate entomological factors responsible for malaria high malaria transmission in Ruangwa district. Three villages were selected from three wards of Ruangwa district; Mnacho and Chienjere.  Likangara represented low, Nandagara moderate and Chienjere high malaria prevalence’s. In each village six houses with open eaves were selected for mosquito collection both indoors and outdoors using Human Landing Catches. A total of 2532 female mosquitoes were collected. Malaria vectors constituted 26.66 % (An.gambiae s.l 680(26.35); An.funestus 8 (0.31) and An.coustani s.l 3 (0.11%).while non –malaria vectors accounted for 73.26 (Culex sp. 1854 (73.2%) Aedes sp. 1 (0.03%). Most mosquito abundance was dominant in Chienjere 932 (37%), followed by Likangara 820 (31%) and the least was Nandagara composed of 780 (31%). Out of 688 anophelines subjected for PCR speciation, An.gambiae s.s was relatively higher 297 (43%) compared to An.arabiensis 278 (40%), An.funestus s.s 6 (0.87%) and unamplified 107 (16%). The high abundance of Anopheles mosquitoes was observed in rainy season 553 (95.18%) as compared to dry season 28 (4.82%). An.gambiae s.s and An.arabiensis species are responsible for maintaining high prevalence of malaria even in the absence of other vectors. An. coustani has an epidemiological concern since it is important vector in neighboring country of Kenya and Zambia. The findings provide useful information that would enable to plan and innovative and effective malaria control strategies in the district

Insecticide-Treated Nets Can Reduce Malaria Transmission by Mosquitoes Which Feed Outdoors

Insecticide treated nets (ITNs) represent a powerful means for controlling malaria in Africa because the mosquito vectors feed primarily indoors at night. The proportion of human exposure that occurs indoors, when people are asleep and can conveniently use ITNs, is therefore very high. Recent evidence suggests behavioral changes by malaria mosquito populations to avoid contact with ITNs by feeding outdoors in the early evening. We adapt an established mathematical model of mosquito behavior and malaria transmission to illustrate how ITNs can achieve communal suppression of malaria transmission exposure, even where mosquito evade them and personal protection is modest. We also review recent reports from Tanzania to show that conventional mosquito behavior measures can underestimate the potential of ITNs because they ignore the importance of human movements

Impregnating hessian strips with the volatile pyrethroid transfluthrin prevents outdoor exposure to vectors of malaria and lymphatic filariasis in urban Dar es Salaam, Tanzania

Background Semi-field trials using laboratory-reared Anopheles arabiensis have shown that, delivering the volatile pyrethroid transfluthrin by absorption into hessian strips, consistently provided > 99 % human protective efficacy against bites for 6 months without retreating. Here the impact of this approach upon human exposure to wild populations of vectors for both malaria and filariasis under full field conditions is assessed for the first time. Methods Transfluthrin-treated and untreated strips were placed around human volunteers conducting human landing catch in an outdoor environment in urban Dar es Salaam, where much human exposure to malaria and filariasis transmission occurs outdoors. The experiment was replicated 9 times at 16 outdoor catching stations in 4 distinct locations over 72 working nights between May and August 2012. Results Overall, the treated hessian strips conferred 99 % protection against An. gambiae (1 bite versus 159) and 92 % protection against Culex spp. (1478 bites versus 18,602). No decline in efficacy over the course of the study could be detected for the very sparse populations of An. gambiae (P = 0.32) and only a slow efficacy decline was observed for Culex spp. (P < 0.001), with protection remaining satisfactory over 3 months after strip treatment. Diversion of mosquitoes to unprotected humans in nearby houses was neither detected for An. gambiae (P = 0.152) nor for Culex spp. (Relative rate, [95 % CI] = 1.03, [0.95, 1.11], P = 0.499). Conclusion While this study raises more questions than it answers, the presented evidence of high protection over long periods suggest this technology may have potential for preventing outdoor transmission of malaria, lymphatic filariasis and other vector-borne pathogens

Impacts of climate change on malaria vector control in Africa

There has been extensive consideration of how climate change may impact the distribution of vector-borne diseases; with a particular focus on malaria risk in Africa. Such analyses primarily consider how the ‘malaria map’ will shift in response to changes in the environmental determinants of transmission, but rarely consider the equally if not more important question of whether climate change will impact the effectiveness of vector control measures. Here we hypothesize that the efficacy and ability to implement core vector control interventions for malaria could be significantly impacted by climate change due to direct and indirect impacts on mosquito vectors and interventions. We review current knowledge on the environmental dependency of current core interventions for malaria vector control including Insecticide Treated Nets, Indoor Residual Spraying and larviciding. We explore how anticipated changes in temperature, rainfall and humidity could impact vector ecology, behaviour and resistance mechanisms; and the knock on effects of these changes for intervention efficacy. Finally we review potential indirect impacts of climate change on the ability to finance, implement and sustain vector control; with a focus on changes in human behaviour, land use, socioeconomic conditions and health systems. We conclude by highlighting the need to build ‘climate-proof’ strategies into future vector control planning

Most outdoor malaria transmission by behaviourally-resistant Anopheles arabiensis is mediated by mosquitoes that have previously been inside houses

Background Anopheles arabiensis is stereotypical of diverse vectors that mediate residual malaria transmission globally, because it can feed outdoors upon humans or cattle, or enter but then rapidly exit houses without fatal exposure to insecticidal nets or sprays. Methods Life histories of a well-characterized An. arabiensis population were simulated with a simple but process-explicit deterministic model and relevance to other vectors examined through sensitivity analysis. Results Where most humans use bed nets, two thirds of An. arabiensis blood feeds and half of malaria transmission events were estimated to occur outdoors. However, it was also estimated that most successful feeds and almost all (>98 %) transmission events are preceded by unsuccessful attempts to attack humans indoors. The estimated proportion of vector blood meals ultimately obtained from humans indoors is dramatically attenuated by availability of alternative hosts, or partial ability to attack humans outdoors. However, the estimated proportion of mosquitoes old enough to transmit malaria, and which have previously entered a house at least once, is far less sensitive to both variables. For vectors with similarly modest preference for cattle over humans and similar ability to evade fatal indoor insecticide exposure once indoors, >80 % of predicted feeding events by mosquitoes old enough to transmit malaria are preceded by at least one house entry event, so long as ≥40 % of attempts to attack humans occur indoors and humans outnumber cattle ≥4-fold. Conclusions While the exact numerical results predicted by such a simple deterministic model should be considered only approximate and illustrative, the derived conclusions are remarkably insensitive to substantive deviations from the input parameter values measured for this particular An. arabiensis population. This life-history analysis, therefore, identifies a clear, broadly-important opportunity for more effective suppression of residual malaria transmission by An. arabiensis in Africa and other important vectors of residual transmission across the tropics. Improved control of predominantly outdoor residual transmission by An. arabiensis, and other modestly zoophagic vectors like Anopheles darlingi, which frequently enter but then rapidly exit from houses, may be readily achieved by improving existing technology for killing mosquitoes indoors

Suppression of malaria vector densities and human infection prevalence associated with scale-up of mosquito-proofed housing in Dar es Salaam, Tanzania: re-analysis of an observational series of parasitological and entomological surveys.

BACKGROUND In the city of Dar es Salaam, Tanzania, rapid and spontaneous scale-up of window screening occurred through purely horizontal commercial distribution systems without any public subsidies or promotion. Scale-up of window screening coincided with a planned evaluation of programmatic, vertically managed scale-up of regular larvicide application as an intervention against malaria vectors and transmission. We aimed to establish whether scale-up of window screening was associated with suppression of mosquito populations, especially for malaria vectors that strongly prefer humans as their source of blood. METHODS This study was a re-analysis of a previous observational series of epidemiological data plus new analyses of previously partly reported complementary entomological data, from Dar es Salaam. Between 2004 and 2008, six rounds of cluster-sampled, rolling, cross-sectional parasitological and questionnaire surveys were done in urban Dar es Salaam to assess the effect of larviciding and other determinants of malaria risk, such as use of bed nets and antimalarial drugs, socioeconomic status, age, sex, travel history, mosquito-proofed housing, and spending time outdoors. The effects of scaled-up larvicide application and window screening were estimated by fitting generalised linear mixed models that allowed for both spatial variation between survey locations and temporal autocorrelation within locations. We also conducted continuous longitudinal entomological surveys of outdoor human biting rates by mosquitoes and experimental measurements of mosquito host preferences. FINDINGS Best-fit models of Plasmodium falciparum malaria infection prevalence among humans were largely consistent with the results of the previous analyses. Re-analysis of previously reported epidemiological data revealed that most of the empirically fitted downward time trend in P falciparum malaria prevalence over the course of the study (odds ratio [OR] 0·04; 95% CI 0·03-0·06; p<0·0001), which was not previously reported numerically or attributed to any explanatory factor, could be plausibly explained by association with an upward trend in city-wide window screening coverage (OR 0·07; 0·05-0·09; p<0·0001) and progressive rollout of larviciding (OR 0·50; 0·41-0·60; p<0·0001). Increasing coverage of complete window screening was also associated with reduced biting densities of all taxonomic groups of mosquitoes (all p<0·0001), especially the Anopheles gambiae complex (relative rate [RR] 0·23; 95% CI 0·16-0·33) and Anopheles funestus group (RR 0·08; 0·04-0·16), which were confirmed as the most efficient vectors of malaria with strong preferences for humans over cattle. Larviciding was also associated with reduced biting densities of all mosquito taxa (p<0·0001), to an extent that varied consistently with the larvicide targeting scheme and known larval ecology of each taxon. INTERPRETATION Community-wide mosquito proofing of houses might deliver greater impacts on vector populations and malaria transmission than previously thought. The spontaneous nature of the scale-up observed here is also encouraging with regards to practicality, acceptability, and affordability in low-income settings. FUNDING United States Agency for International Development, Bill & Melinda Gates Foundation, Wellcome Trust, and Valent BioSciences LLC

Heritability of biting time behaviours in the major African malaria vector Anopheles arabiensis

Background: The use of insecticide-treated nets for malaria control has been associated with shifts in mosquito vector feeding behaviour including earlier and outdoor biting on humans. The relative contribution of phenotypic plasticity and heritability to these behavioural shifts is unknown. Elucidation of the mechanisms behind these shifts is crucial for anticipating impacts on vector control. Methods: A novel portable semi-field system (PSFS) was used to experimentally measure heritability of biting time in the malaria vector Anopheles arabiensis in Tanzania. Wild An. arabiensis from hourly collections using the human landing catch (HLC) method were grouped into one of 3 categories based on their time of capture: early (18:00–21:00), mid (22:00–04:00), and late (05:00–07:00) biting, and placed in separate holding cages. Mosquitoes were then provided with a blood meal for egg production and formation of first filial generation (F1). The F1 generation of each biting time phenotype category was reared separately, and blood fed at the same time as their mothers were captured host-seeking. The resultant eggs were used to generate the F2 generation for use in heritability assays. Heritability was assessed by releasing F2 An. arabiensis into the PSFS, recording their biting time during a human landing catch and comparing it to that of their F0 grandmothers. Results: In PSFS assays, the biting time of F2 offspring (early: 18:00–21:00, mid: 22:00–04:00 or late: 05:00–07:00) was significantly positively associated with that of their wild-caught F0 grandmothers, corresponding to an estimated heritability of 0.110 (95% CI 0.003, 0.208). F2 from early-biting F0 were more likely to bite early than F2 from mid or late-biting F0. Similarly, the probability of biting late was higher in F2 derived from mid and late-biting F0 than from early-biting F0. Conclusions: Despite modest heritability, our results suggest that some of the variation in biting time is attributable to additive genetic variation. Selection can, therefore, act efficiently on mosquito biting times, highlighting the need for control methods that target early and outdoor biting mosquitoes

Seasonal variation in abundance and blood meal sources of primary and secondary malaria vectors within Kilombero Valley, Southern Tanzania

Background: Existing control tools have significantly reduced malaria over the past two decades. However, progress has been stalled due to increased resistance in primary vectors and the increasing role of secondary vectors. This study aimed to investigate the impact of seasonal change on primary and secondary vector abundance and host preference. Understanding the impact of seasonal dynamics of primary and secondary vectors on disease transmission will inform effective strategies for vector management and control.Methods: Vector abundance was measured through longitudinal collection of mosquitoes, conducted monthly during the wet and dry seasons, in Sagamaganga, a village in the Kilombero Valley, Tanzania. Mosquitoes were collected indoors using CDC light traps and backpack aspirators, and outdoors using resting buckets baited with cattle urine. In addition, a direct measure of host preference was taken monthly using human-and cattle-baited mosquito electrocuting traps. A host census was conducted to provide an indirect measure of host preference together with monthly blood meal source analysis. All collected mosquitoes were assayed for Plasmodium sporozoites.Results: A total of 2828 anophelines were collected, of which 78.5% and 21.4%, were primary and secondary vectors, respectively. The abundance of the primary vectors, Anopheles arabiensis and Anopheles funestus, and of the secondary vectors varied seasonally. Indirect measures of host preference indicated that all vectors varied blood meal choice seasonally, with the direct measure confirming this for An. arabiensis. All anopheline mosquitoes tested negative for sporozoites.Conclusions: At the study location, the abundance of both primary and secondary vectors changed seasonally. Indirect and direct measures of host preference demonstrated that An. arabiensis varied from being zoophilic to being more opportunistic during the wet and dry seasons. A similar trend was observed for the other vectors