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

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

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

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

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

Increased proportions of outdoor feeding among residual malaria vector populations following increased use of insecticide-treated nets in rural Tanzania.

BACKGROUND: Insecticide-treated nets (ITNs) and indoor residual spraying (IRS) represent the front-line tools for malaria vector control globally, but are optimally effective where the majority of baseline transmission occurs indoors. In the surveyed area of rural southern Tanzania, bed net use steadily increased over the last decade, reducing malaria transmission intensity by 94%. METHODS: Starting before bed nets were introduced (1997), and then after two milestones of net use had been reached-75% community-wide use of untreated nets (2004) and then 47% use of ITNs (2009)-hourly biting rates of malaria vectors from the Anopheles gambiae complex and Anopheles funestus group were surveyed. RESULTS: In 1997, An. gambiae s.l. and An. funestus mosquitoes exhibited a tendency to bite humans inside houses late at night. For An. gambiae s.l., by 2009, nocturnal activity was less (p = 0.0018). At this time, the sibling species composition of the complex had shifted from predominantly An. gambiae s.s. to predominantly An. arabiensis. For An. funestus, by 2009, nocturnal activity was less (p = 0.0054) as well as the proportion biting indoors (p < 0.0001). At this time, An. funestus s.s. remained the predominant species within this group. As a consequence of these altered feeding patterns, the proportion (mean ± standard error) of human contact with mosquitoes (bites per person per night) occurring indoors dropped from 0.99 ± 0.002 in 1997 to 0.82 ± 0.008 in 2009 for the An. gambiae complex (p = 0.0143) and from 1.00 ± <0.001 to only 0.50 ± 0.048 for the An. funestus complex (p = 0.0004) over the same time period. CONCLUSIONS: High usage of ITNs can dramatically alter African vector populations so that intense, predominantly indoor transmission is replaced by greatly lowered residual transmission, a greater proportion of which occurs outdoors. Regardless of the underlying mechanism, the residual, self-sustaining transmission will respond poorly to further insecticidal measures within houses. Additional vector control tools which target outdoor biting mosquitoes at the adult or immature stages are required to complement ITNs and IRS

An improved mosquito electrocuting trap that safely reproduces epidemiologically relevant metrics of mosquito human-feeding behaviours as determined by human landing catch

Background: Reliable quantification of mosquito host—seeking behaviours is required to determine the efficacy of vector control methods. For malaria, the gold standard approach remains the risky human landing catch (HLC). Here compare the performance of an improved prototype of the mosquito electrocuting grid trap (MET) as a safer alternative with HLC for measuring malaria vector behaviour in Dar es Salaam, Tanzania. Methods: Mosquito trapping was conducted at three sites within Dar es Salaam representing a range of urbanicity over a 7-month period (December 2012–July 2013, 168 sampling nights). At each site, sampling was conducted in a block of four houses, with two houses being allocated to HLC and the other to MET on each night of study. Sampling was conducted both indoors and outdoors (from 19:00 to 06:00 each night) at all houses, with trapping method (HLC and MET) being exchanged between pairs of houses at each site using a crossover design. Results: The MET caught significantly more Anopheles gambiae sensu lato than the HLC, both indoors (RR [95 % confidence interval (CI)]) = 1.47 [1.23–1.76], P &lt; 0.0001 and outdoors = 1.38 [1.14–1.67], P &lt; 0.0001). The sensitivity of MET compared with HLC did not detectably change over the course of night for either An. gambiae s.l. (OR [CI]) = 1.01 [0.94–1.02], P = 0.27) or Culex spp. (OR [CI]) = 0.99 [0.99–1.0], P = 0.17) indoors and declined only slightly outdoors: An. gambiae s.l. (OR [CI]) = 0.92 [0.86–0.99], P = 0.04), and Culex spp. (OR [CI]) = 0.99 [0.98–0.99], P = 0.03). MET-based estimates of the proportions of mosquitoes caught indoors (P i ) or during sleeping hours (P fl ), as well as the proportion of human exposure to bites that would otherwise occurs indoors (π i ), were statistically indistinguishable from those based on HLC for An. gambiae s.l. (P = 0.43, 0.07 and 0.48, respectively) and Culex spp. (P = 0.76, 0.24 and 0.55, respectively). Conclusions: This improved MET prototype is highly sensitive tool that accurately quantifies epidemiologically-relevant metrics of mosquito biting densities, behaviours and human exposure distribution

Attribution of reductions in malaria prevalence in Dar es Salaam, Tanzania – Authors' reply

We thank Mathieu Maheu-Giroux and Marcia Castro for their Correspondence about our Article.1 Regarding concerns about the stepped-wedge design of the larviciding scale-up in our study, we agree and also note that scale-up was not randomised, but rather introduced earliest to the best-prepared wards. However, such compromises are normal and healthy in pragmatic assessments of effectiveness under realistic programmatic conditions, rather than efficacy under artificially controlled experimental conditions. As acknowledged in the discussion and emphasised in the title, we also agree that evidence for window screening impact is purely observational, and that long-overdue, cluster-randomised, experimentally controlled analyses of well developed delivery practices for both these supplementary vector control measures are urgently needed

Development and evaluation of mosquito-electrocuting traps as alternatives to the human landing catch technique for sampling host-seeking malaria vectors

Background The human landing catch (HLC) is the gold standard method for sampling host-seeking malaria vectors. However, the HLC is ethically questionable because it requires exposure of humans to potentially infectious mosquito bites. Methods Two exposure-free methods for sampling host-seeking mosquitoes were evaluated using electrocuting surfaces as potential replacements for HLC: (1) a previously evaluated, commercially available electrocuting grid (CA-EG) designed for killing flies, and (2) a custom-made mosquito electrocuting trap (MET) designed to kill African malaria vectors. The MET and the CA-EG were evaluated relative to the HLC in a Latin Square experiment conducted in the Kilombero Valley, Tanzania. The sampling consistency of the traps across the night and at varying mosquito densities was investigated. Estimates of the proportion of mosquitoes caught indoors (P i ), proportion of human exposure occurring indoors (π i ), and proportion of mosquitoes caught when most people are likely to be indoors (P fl ) were compared for all traps. Results Whereas the CA-EG performed poorly (<10 % of catch of HLC), sampling efficiency of the MET for sampling Anopheles funestus s.l. was indistinguishable from HLC indoors and outdoors. For Anopheles gambiae s.l., sampling sensitivity of MET was 20.9 % (95 % CI 10.3–42.2) indoors and 58.5 % (95 % CI 32.2–106.2) outdoors relative to HLC. There was no evidence of density-dependent sampling by the MET or CA-EG. Similar estimates of P i were obtained for An. gambiae s.l. and An. funestus s.l. from all trapping methods. The proportion of mosquitoes caught when people are usually indoors (P fl ) was underestimated by the CA-EG and MET for An. gambiae s.l., but similar to the HLC for An. funestus. Estimates of the proportion of human exposure occurring indoors (π i ) obtained from the CA-EG and MET were similar to the HLC for An. gambiae s.l., but overestimated for An. funestus. Conclusions The MET showed promise as an outdoor sampling tool for malaria vectors where it achieved >50 % sampling sensitivity relative to the HLC. The CA-EG had poor sampling sensitivity outdoors and inside. With further modification, the MET could provide an efficient and safer alternative to the HLC for the surveillance of mosquito vectors outdoors. Keywords: Mosquito electrocuting trap; Human landing catch; Mosquito behaviour; Vector sampling tools; Outdoor biting; Malaria; Anopheles arabiensis ; Anopheles gambiae s.l.; Anopheles funestus s.l