Community-owned resource persons for malaria vector control: enabling factors and challenges in an operational programme in Dar es Salaam, United Republic of Tanzania.

BACKGROUND: Community participation in vector control and health services in general is of great interest to public health practitioners in developing countries, but remains complex and poorly understood. The Urban Malaria Control Program (UMCP) in Dar es Salaam, United Republic of Tanzania, implements larval control of malaria vector mosquitoes. The UMCP delegates responsibility for routine mosquito control and surveillance to community-owned resource persons (CORPs), recruited from within local communities via the elected local government. METHODS: A mixed method, cross-sectional survey assessed the ability of CORPs to detect mosquito breeding sites and larvae, and investigated demographic characteristics of the CORPs, their reasons for participating in the UMCP, and their work performance. Detection coverage was estimated as the proportion of wet habitats found by the investigator which had been reported by CORP. Detection sensitivity was estimated as the proportion of wet habitats found by the CORPS which the investigator found to contain Anopheles larvae that were also reported to be occupied by the CORP. RESULTS: The CORPs themselves perceived their role as professional rather than voluntary, with participation being a de facto form of employment. Habitat detection coverage was lower among CORPs that were recruited through the program administrative staff, compared to CORPs recruited by local government officials or health committees (Odds Ratio = 0.660, 95% confidence interval = [0.438, 0.995], P = 0.047). Staff living within their areas of responsibility had > 70% higher detection sensitivity for both Anopheline (P = 0.016) and Culicine (P = 0.012): positive habitats compared to those living outside those same areas. DISCUSSION AND CONCLUSIONS: Improved employment conditions as well as involving the local health committees in recruiting individual program staff, communication and community engagement skills are required to optimize achieving effective community participation, particularly to improve access to fenced compounds. A simpler, more direct, less extensive community-based surveillance system in the hands of a few, less burdened, better paid and maintained program personnel may improve performance and data quality

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

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

Measuring, manipulating and exploiting behaviours of adult mosquitoes to optimise malaria vector control impact.

Residual malaria transmission can persist despite high coverage with effective long-lasting insecticidal nets (LLINs) and/or indoor residual spraying (IRS), because many vector mosquitoes evade them by feeding on animals, feeding outdoors, resting outdoors or rapidly exiting from houses after entering them. However, many of these behaviours that render vectors resilient to control with IRS and LLINs also make them vulnerable to some emerging new alternative interventions. Furthermore, vector control measures targeting preferred behaviours of mosquitoes often force them to express previously rare alternative behaviours, which can then be targeted with these complementary new interventions. For example, deployment of LLINs against vectors that historically fed predominantly indoors on humans typically results in persisting transmission by residual populations that survive by feeding outdoors on humans and animals, where they may then be targeted with vapour-phase insecticides and veterinary insecticides, respectively. So while the ability of mosquitoes to express alternative behaviours limits the impact of LLINs and IRS, it also creates measurable and unprecedented opportunities for deploying complementary additional approaches that would otherwise be ineffective. Now that more diverse vector control methods are finally becoming available, well-established entomological field techniques for surveying adult mosquito behaviours should be fully exploited by national malaria control programmes, to rationally and adaptively map out new opportunities for their effective deployment

Evaluation of personal protection afforded by repellent-treated sandals against mosquito bites in south-eastern Tanzania

Outdoor and early evening mosquito biting needs to be addressed if malaria elimination is to be achieved. While indoor-targeted interventions, such as insecticide-treated nets and indoor residual spraying, remain essential, complementary approaches that tackle persisting outdoor transmission are urgently required to maximize the impact. Major malaria vectors principally bite human hosts around the feet and ankles. Consequently, this study investigated whether sandals treated with efficacious spatial repellents can protect against outdoor biting mosquitoes. Sandals affixed with hessian bands measuring 48 cm treated with 0.06 g, 0.10 g and 0.15 g of transfluthrin were tested in large cage semi-field and full field experiments. Sandals affixed with hessian bands measuring 240 cm and treated with 0.10 g and 0.15 g of transfluthrin were also tested semi field experiments. Human landing catches (HLC) were used to assess reduction in biting exposure by comparing proportions of mosquitoes landing on volunteers wearing treated and untreated sandals. Sandals were tested against insectary reared Anopheles arabiensis mosquitoes in semi-field experiments and against wild mosquito species in rural Tanzania. In semi-field tests, sandals fitted with hessian bands measuring 48 cm and treated with 0.15 g, 0.10 g and 0.06 g transfluthrin reduced mosquito landings by 45.9%, (95% confidence interval (C.I.) 28-59%), 61.1% (48-71%), and 25.9% (9-40%), respectively compared to untreated sandals. Sandals fitted with hessian bands measuring 240 cm and treated with 0.15 g and 0.10 g transfluthrin reduced mosquito landings by 59% (43-71%) and 64% (48-74%), respectively. In field experiments, sandals fitted with hessian bands measuring 48 cm and treated with 0.15 g transfluthrin reduced mosquito landings by 70% (60-76%) against Anopheles gambiae sensu lato, and 66.0% (59-71%) against all mosquito species combined. Transfluthrin-treated sandals conferred significant protection against mosquito bites in semi-field and field settings. Further evaluation is recommended for this tool as a potential complementary intervention against malaria. This intervention could be particularly useful for protecting against outdoor exposure to mosquito bites. Additional studies are necessary to optimize treatment techniques and substrates, establish safety profiles and determine epidemiological impact in different settings

Reduced human-biting preferences of the African malaria vectors Anopheles arabiensis and Anopheles gambiae in an urban context: controlled, competitive host-preference experiments in Tanzania

Background Host preference is a critical determinant of human exposure to vector-borne infections and the impact of vector control interventions. Widespread use of long-lasting insecticide-treated nets (LLINs) and indoor residual spraying (IRS) across sub-Saharan Africa, which protect humans against mosquitoes, may select for altered host preference traits of malaria vectors over the long term. Here, the host preferences of Anopheles arabiensis and Anopheles gambiae sensu stricto (s.s.) were experimentally assessed in the field, using direct host-preference assays in two distinct ecological settings in Tanzania. Methods Eight Ifakara Tent Trap (ITT), four baited with humans and four with bovine calves, were simultaneously used to catch malaria vectors in open field sites in urban and rural Tanzania. The numbers of mosquitoes collected in human-baited traps versus calf-baited traps were used to estimate human feeding preference for each site's vector species. Results The estimated proportion [95% confidence interval (CI)] of mosquitoes attacking humans rather than cattle was 0.60 [0.40, 0.77] for An. arabiensis in the rural setting and 0.61 [0.32, 0.85] for An. gambiae s.s. in the urban setting, indicating no preference for either host in both cases (P = 0.32 and 0.46, respectively) and no difference in preference between the two (Odds Ratio (OR) [95%] = 0.95 [0.30, 3.01], P = 0.924). However, only a quarter of An. arabiensis in the urban setting attacked humans (0.25 [0.09, 0.53]), indicating a preference for cattle that approached significance (P = 0.08). Indeed, urban An. arabiensis were less likely to attack humans rather than cattle when compared to the same species in the rural setting (OR [95%] = 0.21 [0.05, 0.91], P = 0.037). Conclusion Urban An. arabiensis had a stronger preference for cattle than the rural population and urban An. gambiae s.s. showed no clear preference for either humans or cattle. In the urban setting, both species exhibited stronger tendencies to attack cattle than previous studies of the same species in rural contexts. Cattle keeping may, therefore, particularly limit the impact of human-targeted vector control interventions in Dar es Salaam and perhaps in other African towns and cities

Topographic mapping of the interfaces between human and aquatic mosquito habitats to enable barrier targeting of interventions against malaria vectors.

Geophysical topographic metrics of local water accumulation potential are freely available and have long been known as high-resolution predictors of where aquatic habitats for immature mosquitoes are most abundant, resulting in elevated densities of adult malaria vectors and human infection burden. Using existing entomological and epidemiological survey data, here we illustrate how topography can also be used to map out the interfaces between wet, unoccupied valleys and dry, densely populated uplands, where malaria vector densities and infection risk are focally exacerbated. These topographically identifiable geophysical boundaries experience disproportionately high vector densities and malaria transmission risk, because this is where mosquitoes first encounter humans when they search for blood after emerging or ovipositing in the valleys. Geophysical topographic indicators accounted for 67% of variance for vector density but for only 43% for infection prevalence, so they could enable very selective targeting of interventions against the former but not the latter (targeting ratios of 5.7 versus 1.5 to 1, respectively). So, in addition to being useful for targeting larval source management to wet valleys, geophysical topographic indicators may also be used to selectively target adult mosquitoes with insecticidal residual sprays, fencing, vapour emanators or space sprays to barrier areas along their fringes

Fine scale mapping of malaria infection clusters by using routinely collected health 1 facility data in urban Dar es Salaam, Tanzania

This study investigated whether passively collected routine health facility data can be used for mapping spatial heterogeneities in malaria transmission at the level of local government housing cluster administrative units in Dar es Salaam, Tanzania. From June 2012 to Jan 2013, residential locations of patients tested for malaria at a public health facility were traced based on their local leaders’ names and geo-referencing the point locations of these leaders’ houses. Geographic information systems (GIS) were used to visualise the spatial distribution of malaria infection rates. Spatial scan statistics were deployed to detect spatial clustering of high infection rates. Among 2,407 patients tested for malaria, 46.6% (1,121) could be traced to their 411 different residential housing clusters. One small spatially aggregated cluster of neighbourhoods with high prevalence was identified. While the home residence housing cluster leader was unambiguously identified for 73.8% (240/325) of malaria-positive patients, only 42.3% (881/2,082) of those with negative test results were successfully traced. It was concluded that recording simple points of reference during routine health facility visits can be used for mapping malaria infection burden on very fine geographic scales, potentially offering a feasible approach to rational geographic targeting of malaria control interventions. However, in order to tap the full potential of this approach, it would be necessary to optimise patient tracing success and eliminate biases by blinding personnel to test results

Effectiveness of the innovative 1,7-malaria reactive community-based testing and response (1, 7-mRCTR) approach on malaria burden reduction in Southeastern Tanzania

In 2015, a China-UK-Tanzania tripartite pilot project was implemented in southeastern Tanzania to explore a new model for reducing malaria burden and possibly scaling-out the approach into other malaria-endemic countries. The 1,7-malaria Reactive Community-based Testing and Response (1,7-mRCTR) which is a locally-tailored approach for reporting febrile malaria cases in endemic villages was developed to stop transmission and Plasmodium life-cycle. The (1,7-mRCTR) utilizes existing health facility data and locally trained community health workers to conduct community-level testing and treatment.; The pilot project was implemented from September 2015 to June 2018 in Rufiji District, southern Tanzania. The study took place in four wards, two with low incidence and two with a higher incidence. One ward of each type was selected for each of the control and intervention arms. The control wards implemented the existing Ministry of Health programmes. The 1,7-mRCTR activities implemented in the intervention arm included community testing and treatment of malaria infection. Malaria case-to-suspect ratios at health facilities (HF) were aggregated by villages, weekly to identify the village with the highest ratio. Community-based mobile test stations (cMTS) were used for conducting mass testing and treatment. Baseline (pre) and endline (post) household surveys were done in the control and intervention wards to assess the change in malaria prevalence measured by the interaction term of 'time' (post vs pre) and arm in a logistic model. A secondary analysis also studied the malaria incidence reported at the HFs during the intervention.; Overall the 85 rounds of 1,7-mRCTR conducted in the intervention wards significantly reduced the odds of malaria infection by 66% (adjusted OR 0.34, 95% CI 0.26,0.44, p < 0001) beyond the effect of the standard programmes. Malaria prevalence in the intervention wards declined by 81% (from 26% (95% CI 23.7, 7.8), at baseline to 4.9% (95% CI 4.0, 5.9) at endline). In villages receiving the 1,7-mRCTR, the short-term case ratio decreased by over 15.7% (95% CI - 33, 6) compared to baseline.; The 1,7-mRCTR approach significantly reduced the malaria burden in the areas of high transmission in rural southern Tanzania. This locally tailored approach could accelerate malaria control and elimination efforts. The results provide the impetus for further evaluation of the effectiveness and scaling up of this approach in other high malaria burden countries in Africa, including Tanzania

The epidemiology of residual Plasmodium falciparum malaria transmission and infection burden in an African city with high coverage of multiple vector control measures.

BACKGROUND In the Tanzanian city of Dar es Salaam, high coverage of long-lasting insecticidal nets (LLINs), larvicide application (LA) and mosquito-proofed housing, was complemented with improved access to artemisinin-based combination therapy and rapid diagnostic tests by the end of 2012. METHODS Three rounds of city-wide, cluster-sampled cross-sectional surveys of malaria parasite infection status, spanning 2010 to 2012, were complemented by two series of high-resolution, longitudinal surveys of vector density. RESULTS Larvicide application using a granule formulation of Bacillus thuringiensis var. israelensis (Bti) had no effect upon either vector density (P = 0.820) or infection prevalence (P = 0.325) when managed by a private-sector contractor. Infection prevalence rebounded back to 13.8 % in 2010, compared with <2 % at the end of a previous Bti LA evaluation in 2008. Following transition to management by the Ministry of Health and Social Welfare (MoHSW), LA consistently reduced vector densities, first using the same Bti granule in early 2011 [odds ratio (OR) (95 % confidence interval (CI)) = 0.31 (0.14, 0.71), P = 0.0053] and then a pre-diluted aqueous suspension formulation from mid 2011 onwards [OR (95 % CI) = 0.15 (0.07, 0.30), P ≪ 0.000001]. While LA by MoHSW with the granule formulation was associated with reduced infection prevalence [OR (95 % CI) = 0.26 (0.12, 0.56), P = 0.00040], subsequent liquid suspension use, following a mass distribution to achieve universal coverage of LLINs that reduced vector density [OR (95 % CI) = 0.72 (0.51, 1.01), P = 0.057] and prevalence [OR (95 % CI) = 0.80 (0.69, 0.91), P = 0.0013], was not associated with further prevalence reduction (P = 0.836). Sleeping inside houses with complete window screens only reduced infection risk [OR (95 % CI) = 0.71 (0.62, 0.82), P = 0.0000036] if the evenings and mornings were also spent indoors. Furthermore, infection risk was only associated with local vector density [OR (95 % CI) = 6.99 (1.12, 43.7) at one vector mosquito per trap per night, P = 0.037] among the minority (14 %) of households lacking screening. Despite attenuation of malaria transmission and immunity, 88 % of infected residents experienced no recent fever, only 0.4 % of these afebrile cases had been treated for malaria, and prevalence remained high (9.9 %) at the end of the study. CONCLUSIONS While existing vector control interventions have dramatically attenuated malaria transmission in Dar es Salaam, further scale-up and additional measures to protect against mosquito bites outdoors are desirable. Accelerated elimination of chronic human infections persisting at high prevalence will require active, population-wide campaigns with curative drugs