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

Lidar reveals activity anomaly of malaria vectors during pan-African eclipse

Yearly, a quarter billion people are infected and a half a million killed by the mosquito-borne disease malaria. Lack of real-time observational tools for continuously assessing the unperturbed mosquito flight activity in situ limits progress toward improved vector control. We deployed a high-resolution entomological lidar to monitor a half-kilometer static transect adjacent to a Tanzanian village. We evaluated one-third million insect observations during five nights, four days, and one annular solar eclipse. We demonstrate in situ lidar classification of several insect families and their sexes based on their modulation signatures. We were able to compare the fine-scale spatiotemporal activity patterns of malaria vectors during ordinary days and an eclipse to disentangle phototactic activity patterns from the circadian mechanism. We observed an increased insect activity during the eclipse attributable to mosquitoes. These unprecedented findings demonstrate how lidar-based monitoring of distinct mosquito activities could advance our understanding of vector ecology

Household factors associated with access to insecticide-treated nets and house modification in Bagamoyo and Ulanga districts, Tanzania.

BACKGROUND: Insecticide-treated nets (ITNs) and house modifications are proven vector control tools, yet in most regions, full coverage has not been achieved. This study investigates household factors associated with access to ITNs and house modification in Tanzania. METHODS: Baseline cross-sectional survey data from previous studies on spatial repellants and indoor residual spray evaluation was analysed from 6757 households in Bagamoyo (60 km north of Dar es Salaam) and 1241 households in Ulanga (a remote rural area in southeast Tanzania), respectively. Regression models were used to estimate the associations between the outcomes: population access to ITNs, access to ITN per sleeping spaces, window screens and closed eaves, and the covariates household size, age, gender, pregnancy, education, house size, house modification (window screens and closed eaves) and wealth. RESULTS: Population access to ITNs (households with one ITN per two people that stayed in the house the previous night of the survey) was 69% (n = 4663) and access to ITNs per sleeping spaces (households with enough ITNs to cover all sleeping spaces used the previous night of the survey) was 45% (n = 3010) in Bagamoyo, 3 years after the last mass campaign. These findings are both lower than the least 80% coverage target of the Tanzania National Malaria Strategic Plan (Tanzania NMSP). In Ulanga, population access to ITNs was 92% (n = 1143) and ITNs per sleeping spaces was 88% (n = 1093), 1 year after the last Universal Coverage Campaign (UCC). Increased household size was significantly associated with lower access to ITNs even shortly after UCC. House modification was common in both areas but influenced by wealth. In Bagamoyo, screened windows were more common than closed eaves (65% vs 13%), whereas in Ulanga more houses had closed eaves than window screens (55% vs 12%). CONCLUSION: Population access to ITNs was substantially lower than the targets of the Tanzania NMSP after 3 years and lower among larger households after 1 year following ITN campaign. House modification was common in both areas, associated with wealth. Improved access to ITNs and window screens through subsidies and Behaviour Change Communication (BCC) strategies, especially among large and poor households and those headed by people with a low level of education, could maximize the uptake of a combination of these two interventions

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

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

Spatially aggregated clusters and scattered smaller loci of elevated malaria vector density and human infection prevalence in urban Dar es Salaam, Tanzania

Background Malaria transmission, primarily mediated by Anopheles gambiae, persists in Dar es Salaam (DSM) despite high coverage with bed nets, mosquito-proofed housing and larviciding. New or improved vector control strategies are required to eliminate malaria from DSM, but these will only succeed if they are delivered to the minority of locations where residual transmission actually persists. Hotspots of spatially clustered locations with elevated malaria infection prevalence or vector densities were, therefore, mapped across the city in an attempt to provide a basis for targeting supplementary interventions. Methods Two phases of a city-wide population-weighted random sample of cross-sectional household surveys of malaria infections were complemented by two matching phases of geographically overlapping, high-resolution, longitudinal vector density surveys; spanning 2010–2013. Spatial autocorrelations were explored using Moran’s I and hotspots were detected using flexible spatial scan statistics. Results Seven hotspots of spatially clustered elevated vector density and eight of malaria infection prevalence were detected over both phases. Only a third of vectors were collected in hotspots in phase 1 (30 %) and phase 2 (33 %). Malaria prevalence hotspots accounted for only half of malaria infections detected in phase 1 (55 %) and phase 2 (47 %). Three quarters (76 % in phase 1 and 74 % in phase 2) of survey locations with detectable vector populations were outside of hotspots. Similarly, more than half of locations with higher infection prevalence (>10 %) occurred outside of hotspots (51 % in phase 1 and 54 % in phase 2). Vector proliferation hazard (exposure to An. gambiae) and malaria infection risk were only very loosely associated with each other (Odds ratio (OR) [95 % Confidence Interval (CI)] = 1.56 [0.89, 1.78], P = 0.52)). Conclusion Many small, scattered loci of local malaria transmission were haphazardly scattered across the city, so interventions targeting only currently identifiable spatially aggregated hotspots will have limited impact. Routine, spatially comprehensive, longitudinal entomological and parasitological surveillance systems, with sufficient sensitivity and spatial resolution to detect these scattered loci, are required to eliminate transmission from this typical African city. Intervention packages targeted to both loci and hotspots of transmission will need to suppress local vector proliferation, treat infected residents and provide vulnerable residents with supplementary protective measures against exposure

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

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

Pathways and associated costs of care in patients with confirmed and presumptive tuberculosis in Tanzania : a cross-sectional study

To assess pathways and associated costs of seeking care from the onset of symptoms to diagnosis in patients with confirmed and presumptive tuberculosis (TB).; Cross-sectional study.; District hospital in Dar es Salaam, Tanzania.; Bacteriologically confirmed TB and presumptive TB patients.; We calculated distance in metres and visualised pathways to healthcare up to five visits for the current episode of sickness. Costs were described by medians and IQRs, with comparisons by gender and poverty status.; Of 100 confirmed and 100 presumptive TB patients, 44% of confirmed patients sought care first at pharmacies after the onset of symptoms, and 42% of presumptive patients did so at hospitals. The median visits made by confirmed patients was 2 (range 1-5) and 2 (range 1-3) by presumptive patients. Patients spent a median of 31% of their monthly household income on health expenditures for all visits. The median total direct costs were higher in confirmed compared with presumptive patients (USD 27.4 [IQR 18.7-48.4] vs USD 19.8 [IQR 13.8-34.0], p=0.02), as were the indirect costs (USD 66.9 [IQR 35.5-150.0] vs USD 46.8 [IQR 20.1-115.3], p&lt;0.001). The indirect costs were higher in men compared with women (USD 64.6 [IQR 31.8-159.1] vs USD 55.6 [IQR 25.1-141.1], p&lt;0.001). The median total distance from patients' household to healthcare facilities for patients with confirmed and presumptive TB was 2338 m (IQR 1373-4122) and 2009 m (IQR 986-2976) respectively.; Patients with confirmed TB have complex pathways and higher costs of care compared with patients with presumptive TB, but the costs of the latter are also substantial. Improving access to healthcare and ensuring integration of different healthcare providers including private, public health practitioners and patients themselves could help in reducing the complex pathways during healthcare seeking and optimal healthcare utilisation