Incremental impact upon malaria transmission of supplementing pyrethroid-impregnated long-lasting insecticidal nets with indoor residual spraying using pyrethroids or the organophosphate, pirimiphos methyl

Background Long-lasting, insecticidal nets (LLINs) and indoor residual spraying (IRS) are the most widely accepted and applied malaria vector control methods. However, evidence that incremental impact is achieved when they are combined remains limited and inconsistent. Methods Fourteen population clusters of approximately 1000 residents each in Zambia’s Luangwa and Nyimba districts, which had high pre-existing usage rates (81.7 %) of pyrethroid-impregnated LLINs were quasi-randomly assigned to receive IRS with either of two pyrethroids, namely deltamethrin [Wetable granules (WG)] and lambdacyhalothrin [capsule suspension (CS)], with an emulsifiable concentrate (EC) or CS formulation of the organophosphate pirimiphos methyl (PM), or with no supplementary vector control measure. Diagnostic positivity of patients tested for malaria by community health workers in these clusters was surveyed longitudinally over pre- and post-treatment periods spanning 29 months, over which the treatments were allocated and re-allocated in advance of three sequential rainy seasons. Results Supplementation of LLINs with PM CS offered the greatest initial level of protection against malaria in the first 3 months of application (incremental protective efficacy (IPE) [95 % confidence interval (CI)] = 0.63 [CI 0.57, 0.69], P < 0.001), followed by lambdacyhalothrin (IPE [95 % CI] = 0.31 [0.10, 0.47], P = 0.006) and PM EC (IPE, 0.23 [CI 0.15, 0.31], P < 0.001) and then by deltamethrin (IPE [95 % CI] = 0.19 [−0.01, 0.35], P = 0.064). Neither pyrethroid formulation provided protection beyond 3 months after spraying, but the protection provided by both PM formulations persisted undiminished for longer periods: 6 months for CS and 12 months for EC. The CS formulation of PM provided greater protection than the combined pyrethroid IRS formulations throughout its effective life IPE [95 % CI] = 0.79 [0.75, 0.83] over 6 months. The EC formulation of PM provided incremental protection for the first 3 months (IPE [95 % CI] = 0.23 [0.15, 0.31]) that was approximately equivalent to the two pyrethroid formulations (lambdacyhalothrin, IPE [95 % CI] = 0.31 [0.10, 0.47] and deltamethrin, IPE [95 % CI] = 0.19 [−0.01, 0.35]) but the additional protection provided by the former, apparently lasted an entire year. Conclusion Where universal coverage targets for LLIN utilization has been achieved, supplementing LLINs with IRS using pyrethroids may reduce malaria transmission below levels achieved by LLIN use alone, even in settings where pyrethroid resistance occurs in the vector population. However, far greater reduction of transmission can be achieved under such conditions by supplementing LLINs with IRS using non-pyrethroid insecticide classes, such as organophosphates, so this is a viable approach to mitigating and managing pyrethroid resistance

A cost-effective, community-based, mosquito-trapping scheme that captures spatial and temporal heterogeneities of malaria transmission in rural Zambia

Background Monitoring mosquito population dynamics is essential to guide selection and evaluation of malaria vector control interventions but is typically implemented by mobile, centrally-managed teams who can only visit a limited number of locations frequently enough to capture longitudinal trends. Community-based (CB) mosquito trapping schemes for parallel, continuous monitoring of multiple locations are therefore required that are practical, affordable, effective, and reliable. Methods A CB surveillance scheme, with a monthly sampling and reporting cycle for capturing malaria vectors, using Centers for Disease Control and Prevention light traps (LT) and Ifakara Tent Traps (ITT), were conducted by trained community health workers (CHW) in 14 clusters of households immediately surrounding health facilities in rural south-east Zambia. At the end of the study, a controlled quality assurance (QA) survey was conducted by a centrally supervised expert team using human landing catch (HLC), LT and ITT to evaluate accuracy of the CB trapping data. Active surveillance of malaria parasite infection rates amongst humans was conducted by CHWs in the same clusters to determine the epidemiological relevance of these CB entomological surveys. Results CB-LT and CB-ITT exhibited relative sampling efficiencies of 50 and 7%, respectively, compared with QA surveys using the same traps. However, cost per sampling night was lowest for CB-LT ($13.6), followed closely by CB-ITT ($18.0), both of which were far less expensive than any QA survey (HLC: $138, LT:$289, ITT: $269). 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), all of which were far more cost-effective than QA-LT ($141) and QA-ITT ($168). 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). Conclusions CB trapping schemes appear to be far more affordable, epidemiologically relevant and cost-effective than centrally supervised trapping schemes and may well be applicable to enhance intervention trials and even enable routine programmatic monitoring of vector population dynamics on unprecedented national scales

Evaluation of alternative mosquito sampling methods for malaria vectors in Lowland South - East Zambia.

Sampling malaria vectors and measuring their biting density is of paramount importance for entomological surveys of malaria transmission. Human landing catch (HLC) has been traditionally regarded as a gold standard method for surveying human exposure to mosquito bites. However, due to the risk of human participant exposure to mosquito-borne parasites and viruses, a variety of alternative, exposure-free trapping methods were compared in lowland, south-east Zambia. Centres for Disease Control and Prevention miniature light trap (CDC-LT), Ifakara Tent Trap model C (ITT-C), resting boxes (RB) and window exit traps (WET) were all compared with HLC using a 3 × 3 Latin Squares design replicated in 4 blocks of 3 houses with long lasting insecticidal nets, half of which were also sprayed with a residual deltamethrin formulation, which was repeated for 10 rounds of 3 nights of rotation each during both the dry and wet seasons. The mean catches of HLC indoor, HLC outdoor, CDC-LT, ITT-C, 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. Indoor CDC-LT was more efficient in sampling An. quadriannulatus and An. funestus than HLC indoor (Relative rate [95% Confidence Interval] = 1.873 [1.653, 2.122] and 1.532 [1.441, 1.628], respectively, P < 0.001 for both). ITT-C was the only other alternative which had comparable sensitivity (RR = 0.821 [0.765, 0.881], P < 0.001), relative to HLC indoor other than CDC-LT for sampling An. funestus. While the two most sensitive exposure-free techniques primarily capture host-seeking mosquitoes, both have substantial disadvantages for routine community-based surveillance applications: the CDC-LT requires regular recharging of batteries while the bulkiness of ITT-C makes it difficult to move between sampling locations. RB placed indoors or outdoors and WET had consistently poor sensitivity so it may be useful to evaluate additional alternative methods, such as pyrethrum spray catches and back packer aspirators, for catching resting mosquitoes

Research agenda for preventing mosquito-transmitted diseases through improving the built environment in sub-Saharan Africa

Mosquito-transmitted diseases are a major threat to health in sub-Saharan Africa, but could be reduced through modifications to the built environment. Here we report findings from a major workshop held to identify the research gaps in this area, namely: (1) evidence of the health benefits to changes to the built environment, (2) understanding how mosquitoes enter buildings, (3) novel methods for reducing mosquito-house entry, (4) sustainable approaches for reducing mosquito habitats, (5) case studies of micro-financing for healthy homes and (6) methods for increasing scale-up. Multidisciplinary research is essential to build out mosquito-transmitted diseases, and not build them in

Proportional decline of Anopheles quadriannulatus and increased contribution of An. arabiensis to the An. gambiae complex following introduction of indoor residual spraying with pirimiphos-methyl: an observational, retrospective secondary analysis of pre-existing data from southeast Zambia

Background: Across most of sub-Saharan Africa, malaria is transmitted by mosquitoes from the Anopheles gambiae complex, comprising seven morphologically indistinguishable but behaviourally-diverse sibling species with ecologically-distinct environmental niches. Anopheles gambiae and An. arabiensis are the mostly widely distributed major malaria vectors within the complex, while An. quadriannulatus is sparsely distributed. Methods: Indoor residual spraying (IRS) with the organophosphate pirimiphos-methyl (PM) was conducted four times between 2011 and 2017 in the Luangwa Valley, south-east Zambia. Anopheles mosquitoes were repeatedly collected indoors by several experiments with various objectives conducted in this study area from 2010 onwards. Indoor mosquito collection methods included human landing catches, Centres for Disease Control and Prevention miniature light traps and back pack aspirators. Anopheles gambiae complex mosquitoes were morphologically identified to species level using taxonomic keys, and to molecular level by polymerase chain reaction. These multistudy data were collated so that time trends in the species composition of this complex could be assessed. Results: The proportion of indoor An. gambiae complex accounted for by An. quadriannulatus declined from 95.1% to 69.7% following two application PM-IRS rounds with an emulsifiable concentrate formulation from 2011 to 2013, while insecticidal net utilisation remained consistently high throughout that period. This trend continued after two further rounds of PM-IRS with a longer-lasting capsule suspension formulation in 2015 and 2016/2017, following which An. quadriannulatus accounted for only 4.5% of the complex. During the same time interval there was a correspondingly steady rise in the proportional contribution of An. arabiensis to the complex, from 3.9 to 95.1%, while the contribution of nominate An. gambiae remained stable at ≤ 0.9%. Conclusion: It seems likely that An. arabiensis is not only more behaviourally resilient against IRS than An. gambiae, but also than An. quadriannulatus populations exhibiting indoor-feeding, human-feeding and nocturnal behaviours that are unusual for this species. Routine, programmatic entomological monitoring of dynamic vector population guilds will be critical to guide effective selection and deployment of vector control interventions, including supplementary measures to tackle persisting vectors of residual malaria transmission like An. arabiensis. Keywords: Anopheles, Mosquito, Vector control, Indoor feeding, Outdoor feeding, Residual transmission, Monitoring, Surveillanc

Wash-resistance of pirimiphos-methyl insecticide treatments of window screens and eave baffles for killing indoor-feeding malaria vector mosquitoes: an experimental hut trial, South East of Zambia.

The effectiveness of long-lasting insecticidal-treated nets (LLINs) and indoor residual spraying (IRS) for malaria control is threatened by resistance to commonly used pyrethroid insecticides. Rotations, mosaics, combinations, or mixtures of insecticides from different complementary classes are recommended by the World Health Organization (WHO) for mitigating against resistance, but many of the alternatives to pyrethroids are prohibitively expensive to apply in large national IRS campaigns. Recent evaluations of window screens and eave baffles (WSEBs) treated with pirimiphos-methyl (PM), to selectively target insecticides inside houses, demonstrated malaria vector mortality rates equivalent or superior to IRS. However, the durability of efficacy when co-applied with polyacrylate-binding agents (BA) remains to be established. This study evaluated whether WSEBs, co-treated with PM and BA have comparable wash resistance to LLINs and might therefore remain insecticidal for years rather than months. WHO-recommended wire ball assays of insecticidal efficacy were applied to polyester netting treated with or without BA plus 1 or 2 g/sq m PM. They were then tested for insecticidal efficacy using fully susceptible insectary-reared Anopheles gambiae mosquitoes, following 0, 5, 10, 15, then 20 washes as per WHO-recommended protocols for accelerated ageing of LLINs. This was followed by a small-scale field trial in experimental huts to measure malaria vector mortality achieved by polyester netting WSEBs treated with BA and 2 g/sq m PM after 0, 10 and then 20 standardized washes, alongside recently applied IRS using PM. Co-treatment with BA and either dosage of PM remained insecticidal over 20 washes in the laboratory. In experimental huts, WSEBs treated with PM plus BA consistently killed similar proportions of Anopheles arabiensis mosquitoes to PM-IRS (both consistently ≥ 94%), even after 20 washes. Co-treating WSEBs with both PM and BA results in wash-resistant insecticidal activity comparable with LLINs. Insecticide treatments for WSEBs may potentially last for years rather than months, therefore, reducing insecticide consumption by an order of magnitude relative to IRS. However, durability of WSEBs will still have to be assessed in real houses under representative field conditions of exposure to wear and tear, sunlight and rain

Control of Malaria Vector Mosquitoes by Insecticide-Treated Combinations of Window Screens and Eave Baffles

We assessed window screens and eave baffles (WSEBs), which enable mosquitoes to enter but not exit houses, as an alternative to indoor residual spraying (IRS) for malaria vector control. WSEBs treated with water, the pyrethroid lambda-cyhalothrin, or the organophosphate pirimiphos-methyl, with and without a binding agent for increasing insecticide persistence on netting, were compared with IRS in experimental huts. Compared with IRS containing the same insecticide, WSEBs killed similar proportions of Anopheles funestus mosquitoes that were resistant to pyrethroids, carbamates and organochlorines and greater proportions of pyrethroid-resistant, early exiting An. arabiensis mosquitoes. WSEBs with pirimiphos-methyl killed greater proportions of both vectors than lambda-cyhalothrin or lambda-cyhalothrin plus pirimiphos-methyl and were equally efficacious when combined with binding agent. WSEBs required far less insecticide than IRS, and binding agents might enhance durability. WSEBs might enable affordable deployment of insecticide combinations to mitigate against physiologic insecticide resistance and improve control of behaviorally resistant, early exiting vectors

MOESM1 of Wash-resistance of pirimiphos-methyl insecticide treatments of window screens and eave baffles for killing indoor-feeding malaria vector mosquitoes: an experimental hut trial, South East of Zambia

Additional file 1. Data collection forms for the experimental hut study, South East of Zambia