Title:
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Community-based monitoring of vector control interventions impact upon mosquito population dynamics in rural Zambia
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Over the last decade, the malaria burden has reduced drastically across many parts of sub-Saharan Africa. This is mainly due to effective implementation of integrated malaria control programmes that include large scale application of vector control in the form of long-lasting insecticidal nest (LLINs) and indoor residual spraying (IRS), both of which target the most efficient human-seeking malaria vector species. However, in spite of these efforts, malaria has yet to be eliminated from most of Africa. However, recent increases in the physiological resistance of vector populations, especially to the pyrethroids that remain the only active ingredients currently used on nets threaten these achievements. Furthermore, various forms of behavioural resilience and resistance exhibited by some vector species to LLIN and IRS delivery formats for insecticides respectively limit and undermine these valuable impacts upon malaria transmission. To monitor the impact that LLINs and IRS have on vector population dynamics and malaria transmission, more effective, practical and affordable entomological surveillance systems are required. Currently, surveillance of mosquito populations are conducted by the centralized specialist teams with limited personnel, resources and geographic outreach. None of these existing systems can adequately monitor vector population dynamics longitudinally across the vastness of entire countries. The overall goal of the study was to demonstrate how a community-based surveillance system can be applied to longitudinally monitor vector population dynamics and assess the impact that LLINs and IRS have on malaria transmission in rural Zambia. To achieve this overall goal, the following specific objectives were addressed: (1) To evaluate the efficacy of exposure-free mosquito trapping methods for measuring malaria vector density, as alternatives to human landing catch; (2) To assess the cost-effectiveness using a community-based (CB) mosquito trapping scheme for monitoring vector population dynamics; (3) To determine the extent to which a community-based mosquito trapping scheme captures trends in epidemiological indicators of malaria infection risk; (4) To determine the impact of indoor residual spraying with different classes of insecticides on malaria infection burden and vector abundances in an area of high coverage with insecticide treated nets using a community-based platform. To address objective 1, a 3 x 3 Latin square method was used to evaluate the sensitivity of the Center for Disease and Control and Prevention miniature light traps (LT), the Ifakara tent trap (ITT), window exit traps (WET) and the resting boxes (RB) using the golden standard human land catch (HLC) as the reference method. The mean catches of HLC indoor, HLC outdoor, CDC-LT, ITT, WET, RB indoor and RB outdoor, were 1.687, 1.004, 3.267, 0.088, 0.004, 0.000 and 0.008 for Anopheles quadriannulatus Theobald respectively, and 7.287, 6.784, 10.958, 5.875, 0.296, 0.158 and 0.458, for An. funestus Giles, respectively. The LT (Relative rate (RR) [95% Confidence Interval] = 1.532 [1.441, 1.628] P < 0.001) and ITT (RR = 0.821 [0.765, 0.881], P < 0.001), were the only exposure-free alternatives which had comparable sensitivities relative to HLC indoor for sampling An. funestus. To address objectives 2 and 3, the two most sensitive of these exposure-free trapping methods, the LT and ITT, were applied through a CB longitudinal entomological surveillance system implemented by local community health workers (CHW) trained in basic entomology. This surveillance platform was conducted using a monthly sampling cycle for over 2 years in 14 population clusters distributed across two rural districts covering over 4,000km2 of south-east Zambia. Parallel active surveillance of malaria parasite infection rates amongst humans was also conducted by CHWs in the same population clusters to determine the epidemiological relevance of these CB entomological surveys. Prior to the end of the study, a controlled quality assurance (QA) survey was conducted by a centrally supervised expert team using HLC, LT and ITT to evaluate accuracy of the CB trapping data. While the relative sampling efficiencies of both CB surveys were less than their QA counterparts, the costs of implementing per sampling night were far less expensive than any QA survey. The cost per specimen of Anopheles funestus captured was lowest for CB-LT ($5.3), followed by potentially hazardous QA-HLC ($10.5) and then CB-ITT ($28.0). Time-trends of malaria diagnostic positivity (DP) followed those of An. funestus density with a one-month lag and the wide range of mean DP across clusters was closely associated with mean densities of An. funestus caught by CB-LT (P<0.001). To address objective 4, the same 14 cluster populations, with pre-existing high coverage of pyrethroid-impregnated long-lasting insecticidal nets (LLINs), were quasi-randomly assigned to receive IRS with either of two pyrethroid formulations, namely Deltamethrin (Wettable granules (WG)) (DM-WG) and Lambdacyhalothrin (Capsule suspension (CS)) (LC-CS), or with an emulsifiable concentrate (EC) or CS formulation of the organophosphate pirimiphosmethyl (PM), or with no supplementary vector control measure. DP conducted is described in objective 2. Over the first 3 months, the PM-CS IRS supplement offered the greatest level of protection against malaria followed by LC-SC and then by DM-WG. Neither pyrethroid formulation provided protection beyond 3 months after spraying, but both PM CS and EC formulations persisted for 6 months and 12 months respectively. The CS formulation of PM provided greater protection than the combined pyrethroid IRS formulations throughout its effective life (Incremental protective efficacy (IPE) [95%CI] = 0.79 [0.75, 0.83]) over 6 months. The EC formulation of PM provided incremental protection for the first three months (IPE [95%CI] = 0.23 [0.15, 0.31]) that was approximately equivalent to the two pyrethroid formulations (LC-CS, IPE [95%CI] = 0.31 [0.10, 0.47] and DM-WG, IPE [95%CI] = 0.19 [-0.01, 0.35]) but the additional protection provided by the former, apparently lasted an entire year. There were no obvious differences in the densities of An. funestus during the first three months post-spraying for both pyrethroid formulations (DM-WG (IPE[95%CI]=0.01[-0.56,0.37],P=0.103) and LC-CS (IPE[95%CI]=-0.03[-0.88,0.44],P=0.195) and PM-EC (IPE[95%CI]=-0.04[-0.30,0.17], P=0.103). However, where PM-CS was applied, mosquito densities were dramatically reduced during the same period (IPE [95%CI] =0.93[0.87, 0.97], P<0.001). Between the fourth and the sixth month after spraying with DM-WG, there was an apparent, but presumably spurious, three-fold increase in An. funestus densities while LC-CS, PM-EC and PM-CS achieved 5, 3 and 71-fold reductions, respectively. However, from the seventh to twelfth months after spraying, DM-WG and PM-EC had no obvious effect on the An. funestus densities while insufficient data was available to examine the incremental impact of LC-CS or PM-CS. When applied at this pilot scale, this CB mosquito-trapping scheme provided entomological evidence that complements epidemiological monitoring data to demonstrate how supplementing LLINs with IRS can reduce malaria transmission beyond levels achieved with LLINs alone in this setting where physiological resistance to pyrethroids occurs, especially when a non-pyrethroid organophosphate insecticide is used. Overall, it appears that CB trapping schemes are affordable, cost-effective, and epidemiologically relevant. It also appears, based on the evidence from this pilot scale evaluation, that they may be applicable to routine programmatic monitoring of vector population dynamics on unprecedented national scales.
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