The efficacy of insecticide-treated window screens and eaves against Anopheles mosquitoes: a scoping review

Female mosquitoes serve as vectors for a host of illnesses, including malaria, spread by the Plasmodium parasite. Despite monumental strides to reduce this disease burden through tools such as bed nets, the rate of these gains is slowing. Ongoing disruptions related to the COVID-19 pandemic may also negatively impact gains. The following scoping review was conducted to examine novel means of reversing this trend by exploring the efficacy of insecticide-treated window screens or eaves to reduce Anopheles mosquito bites, mosquito house entry, and density. Two reviewers independently searched PubMed, Scopus, and ProQuest databases on 10 July, 2020 for peer-reviewed studies using insecticide-treated screens or eaves in malaria-endemic countries. These articles were published in English between the years 2000–2020. Upon collection, the reports were stratified into categories of biting incidence and protective efficacy, mosquito entry and density, and mosquito mortality. Thirteen out of 2180 articles were included in the final review. Eaves treated with beta-cyfluthrin, transfluthrin or bendiocarb insecticides were found to produce vast drops in blood-feeding, biting or mosquito prevalence. Transfluthrin-treated eaves were reported to have greater efficacy at reducing mosquito biting: Rates dropped by 100% both indoors and outdoors under eave ribbon treatments of 0.2% transfluthrin (95% CI 0.00–0.00; p < 0.001). Additionally, co-treating window screens and eaves with polyacrylate-binding agents and with pirimiphos-methyl has been shown to retain insecticidal potency after several washes, with a mosquito mortality rate of 94% after 20 washes (95% CI 0.74–0.98; p < 0.001). The results from this scoping review suggest that there is value in implementing treated eave tubes or window screens. More data are needed to study the longevity of screens and household attitudes toward these interventions.

treatment opportunities, food security, and housing quality [3].
With improved housing comes a reduced risk of contracting malaria due to lowered exposure to mosquitoes [2,4,5]. A 2001-2017 cross-sectional analysis using data from 33 African countries found that improved housing lowered the risk of child mortality from malaria by 12-18% [4]. Openings in walls and other points of entry, once closed, can bar vectors from biting indoors during their active hours. Tools such as insecticide-treated window screens and eaves are designed to do just that, along with the added community effect of reducing mosquito populations due to the insecticide treatment. However, these devices are not as widely prioritized in the fight against malaria compared to bed net programmes or indoor residual spraying [6]. More concrete research displaying the benefits of window screens and eaves is required [6]. Added research will help to motivate all critical stakeholders, such as policymakers, to invest in said tools. Addressing housing quality could help to alleviate other issues of poverty by identifying household needs and concerns.
The following review addresses the call for more research by synthesizing and summarizing current scientific knowledge of housing interventions to inform policy. More specifically, this scoping review provides a detailed account of the literature, assessing whether chemical insecticide-treated window screens and eaves are capable of reducing malaria incidence, prevalence, and mosquito biting densities within malaria-endemic countries.

Search strategy
On 10 July, 2020, the research team performed a literature search exploring PubMed, Scopus, and Pro-Quest databases using the terms found in Table 1. These search terms were selected through collaboration with a research librarian and incorporated medical subject headings and keywords. Both categories pertained to malaria-endemic regions, insecticides or pyrethroids, window screens, and eaves. To address outcomes, search terms on epidemiology, mosquito bites, disease prevalence, and incidence were also included.

Inclusion and exclusion criteria
The research team incorporated guidelines from the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) study selection process [7]. The inclusion criteria comprised: (1) data reported from malaria-endemic countries in the WHO regions of sub-Saharan Africa, Southeast Asia, the Eastern Mediterranean, the Western Pacific, and South America; (2) studies reported in English; (3) interventions investigating Anopheles mosquitoes using insecticide-treated netting for window screens and eaves; (4) studies that used empirical methods, meaning the collection and analysis of data using the scientific method; and (5) studies that were published in the years 2000-2020. Articles that investigated bed nets or curtains alone were excluded from the study.

Data extraction
Data were collected in RefWorks Legacy, and each article was independently assessed by two reviewers (BIA and KV). Data from each study were qualitatively synthesized into categories of biting incidence and protective efficacy, mosquito entry and density, mosquito mortality, and household member attitudes toward each intervention. The Critical Appraisal Skills Programme Checklist (CASP) for case-control studies was used to evaluate the quality of these reports, where groups exposed to the insecticide were taken as cases and non-exposed groups were categorized as controls [8]. Randomized controlled trials (RCTs) were appraised with the CASP for RCT studies [9]. Reviewers discussed and resolved any discrepancies.

Characteristics of studies
Population demographics of all articles varied widely, particularly in the Anopheles species that researchers studied (Table 3). Three interventions utilized RCT study designs and the remaining 10 used case-control releaserecapture, wild mosquito recruitment, and/or experimental hut studies (Table 3). Studies using experimental huts first reconstructed West African-style homes. These homes were modified to include multiple eave tubes at eave level. Other reports identified as village studies, as they incorporated housing units already present in a community. To collect mosquitoes, the overnight releaserecapture method or the recruitment of wild mosquitoes was used. With the release-recapture method, laboratory-reared mosquitoes were released into the experimental enclosure and later captured to record their position and status. The recruitment of wild mosquitoes, conversely, involved the capture of mosquitoes that were not raised in a controlled setting.
Most studies (n = 10) reported on treated eave inserts, while three studies investigated both window screens and eaves. All data were collected in African countries: four studies took place in Tanzania, whereas three articles were aggregated in Côte d'Ivoire and three in Kenya. All other studies produced results from Mozambique, Bénin, and Zambia.
All reports (n = 13) indicated that their studies included human volunteers. Of the 13 articles, eight involved adult participants, one involved children, and four did not identify participant ages. Five studies comprised all male volunteers and the eight remaining studies did not provide information on the gender of their volunteers. Insect samples ranged from 90 to 11,362 released or collected mosquitoes. Twelve studies re-evaluated the intervention at least twice, while one design did not clearly state whether treatment replication took place (Table 2).

Biting incidence and protective efficacy
Five of the 13 studies indicated the intervention effects on mosquito-biting incidence and protective efficacy ( Table 4). Three of these reports utilized transfluthrin insecticide against mosquito vectors, of which one study found that eave ribbons treated with insecticide concentrations of 0.2% led to 100% reductions in indoor and outdoor biting with zero average nightly mosquito catches (95% CI 0.00-0.00; p < 0.001) [10]. In this report, volunteers assigned to houses with eaves covered in 10 times less transfluthrin (0.02%) still experienced 77.2% protection indoors with three average nightly catches (95% CI 0.32-5.18; p < 0.001) and 56.2% protection outdoors with 46 average nightly catches (95% CI 23.5-68.6; p < 0.001).
Mmbando et al. indicated that eaves treated with transfluthrin afforded 96% indoor and 84% outdoor protection against Anopheles arabiensis [10]. Drastically lower, though, were the treatment results on Anopheles funestus, as volunteers experienced only 42% protection indoors and 40% outdoor protection [10]. As a form of community defence, one study reported that if 80% of households installed transfluthrin-eaves, an entire community would experience a state of herd immunity [8].
Mwanga et al. [11] found that eave ribbons treated with transfluthrin protected participants who slept under a net at 83% efficacy indoors and 62% outdoors. Conversely, volunteers who did not sleep under a net experienced 57% protection indoors and 48% outdoors against An. arabiensis mosquitoes [11]. Volunteers who slept under nets and with treated eaves had constant levels of protection, whereas those who did not sleep under a net experienced increased levels of protection when eave ribbons were added to the mix [11].

Mosquito entry and density
Seven studies reported the intervention outcomes on mosquito entry and indoor density (Table 4). In Barreaux et al. 's [12] report, inserts treated with 10% betacyfluthrin and placed in eave tubes using the In2Care tool resulted in 0-0.4% of mosquitoes entering houses with closed windows. This method is known as the Lethal House Lure. The control hut had around 50-80% of mosquitoes entering the structure when eaves were untreated [12].

Mosquito mortality
In addition to outcomes related to mosquito entry behaviour, seven of the included studies generated reports based on mosquito mortality (Table 4). These #3. Were all participants who entered the study accounted for at its conclusion?
#4. Were the participants 'blind' to the intervention they were given? Were the investigators 'blind' to the intervention they were giving to participants? Were the interventions utilized the In2Care insert (n = 2), transfluthrin (n = 2), beta-cyfluthrin (n = 1), bendiocarb (n = 1), and pirimiphos-methyl (PM) insecticides (n = 1). Barreaux et al. [12] found that the In2Care tool differentially killed 25% more mosquitoes per day compared to the control hut in which 2-4% daily deaths occurred. In another report, 11 insecticides were tested for their toxicity, wherein beta-cyfluthrin remained the most durable and potent of them all [16]. Beta-cyfluthrin was observed to maintain 100% mortality rates up to one month of use [16]. This team found that the insecticide killed 55% of mosquitoes that came into contact with treated eaves (an average of 44% of released mosquitoes) by the following morning; then, after 24 h of exposure, 64% of mosquitoes died, although not at a significant difference (p > 0.05). Within the untreated control hut, less than 5% of mosquitoes died that came into contact with untreated eaves [16].
Along with beta-cyfluthrin eaves, two interventions focused on mosquito mortality from transfluthrintreated eaves. Eaves covered with transfluthrin were reported to result in high mortality rates. In one report, around 99.5% of all mosquitoes died upon exposure to houses protected by treated eaves [10]. Moreover, Mwanga et al. [11] found that, after exposing caged mosquitoes to treated eave ribbons, all mosquitoes reportedly died.
Chinula et al. [17] investigated the wash resistance of window screens and eave baffles (WSEBs) treated with pirimiphos-methyl (PM) insecticide and polyacrylatebinding agents (BA). Exposed mosquitoes died at rates equal to that of LLIN and continued to die at 94% after 20 washes (95% CI 0.74-0.98; p < 0.001) [17]. When BA was removed, all mosquitoes died after zero washes; however, after 10 washes, less than 10% of all mosquitoes died [17]. Likewise, when the PM insecticide was removed, less than 5% of mosquitoes died after 0, 5, 10, and 20 washes whether or not BA was present [17].

Participant needs and attitudes
Only two articles discussed volunteer attitudes toward treated eaves or window screens (Table 4). Mmbando et al. [18] reported that participants had overall positive outlooks toward prototype windows because of their ventilation and attraction. A positive regard for these devices was demonstrated over 10 weeks by the doubling of male residents from four to eight in houses newly installed with prototype windows. Eventually, new inhabitants displayed housing comfort, redecorating 10 out of the 20 housing units with new curtains and floors [18]. Relative to bed nets, which can generally accommodate two people, eave ribbons treated with transfluthrin could accommodate four residents [10].

Discussion
The evidence reviewed suggests that eave tubes infused with specific insecticides can reduce vector-biting incidence rates, mosquito entry rates and mosquito prevalence (Tables 3-4). Based on the studies reviewed here, insecticide-treated eaves coated with beta-cyfluthrin or transfluthrin can reduce vector biting by noteworthy amounts: A 64% drop in An. gambiae s.l. blood-feeding when treated with 10% beta-cyfluthrin; and a 100% drop in indoor and outdoor biting when treated with 0.2% transfluthrin [10,19]. Transfluthrin appears to be one of the more effective insecticides on eave tubes for reducing mosquito biting, as at a concentration of 0.02% biting protection rates were 77.2% indoors and 56.2% outdoors [10]. Worth noting, however, is that transfluthrin-eaves appear to offer minimal to no protection against An. funestus mosquitoes [10]. Public health practitioners should therefore base the type of insecticide they treat eaves with on the most prevalent species of mosquito in a community.
Households fitted with beta-cyfluthrin-treated eaves might also be protected against mosquito entry. Of all the tests included with this insecticide, the one that followed the Lethal House Lure approach was the most successful. Using this system where beta-cyfluthrin-coated eaves were installed in houses, only 0-0.4% of mosquitoes entered these structures [12]. Local governments people assessing/analysing outcome/s 'blinded'? #5. Were the study groups similar at the start of the randomised controlled trial? #6. Apart from the experimental intervention, did each study group receive the same level of care (that is, were they treated equally)?
#7. Were the effects of intervention reported comprehensively?
#8. Was the precision of the estimate of the intervention or treatment effect reported?
#9. Do the benefits of the experimental intervention outweigh the harms and costs?
#10. Can the results be applied to your local population/in your context? #11. Would the experimental intervention provide greater value to the people in your care than any of the existing interventions?
The black shaded areas for these articles indicate the absence of an additional critical appraisal question in malaria-endemic areas could consider implementing similar designs in their communities. Alternatively, applying bendiocarb to eaves resulted in a 79% drop in mosquito entry rates and could be used as a substitute for beta-cyfluthrin [13]. Alone, bendiocarb-eaves performed as well as LLIN coupled with untreated eaves, suggesting that together this intervention and LLIN may bolster preventative efforts [14]. Insecticide-treated eaves may also increase mosquito mortality. Transfluthrin was found to kill around 99.5% of mosquitoes in one report [10], while beta-cyfluthrin treatments killed 100% of mosquitoes for at least one month in another [16]. As impressive as most of these figures are, few studies investigated the long-term use of their interventions. This is concerning because durability is an important factor in cost-benefit analyses, raising logistical questions about replacing tools that have lost their effectiveness. The compounds in an insecticide are of varying levels of photosensitivity, meaning that exposure to sunlight initiates chemical breakdown [23]. For window screens coated with insecticide, the risk of sunlight exposure is high, eventually reducing insecticidal strength over time. Eaves, on the other hand, are situated in an enclosed space and experience less sunlight exposure. Thus, the insecticidal strength of treated eaves may last longer than on window screens.
Available evidence suggests that both window screens and eaves should be co-treated with BA to retain insecticidal potency after washes [16]. The data comes specifically from research done with PM insecticide and may not translate as accurately to other insecticides. Only two of the 13 included articles discussed participant attitudes toward any of these interventions, and both of these articles were from the same research team [10,18]. The international community needs more data on community preferences for these tools in order that they are maintained when installed.

Study strengths and limitations
The strengths of this review include its specificity and current analysis of treated eaves and window screens against Anopheles mosquitoes. Moreover, it provides comparisons between insecticides, detailing their effectiveness and, in many cases, against what species of mosquito. This information is critical for public health researchers or programmers aiming to install said devices in affected communities, as it will help them to tailor their interventions. In addition, the research team conducted this review during a time when malaria progression expressed stagnation, thereby enhancing this review's timeliness by providing supplementary solutions [24]. The results of this study are consistent with other published reports that indicated reductions in mosquito density and biting due to eave closures or tube installations [25,26].
Although specificity could be regarded as a strength, it may also be a limitation. Studies or corresponding results that tested netting without insecticide treatments, tested insecticidal resistance, or tested entomopathogenic fungi alone did not appear in this review. Similarly, many articles may have been overlooked due to the assessment of three databases. Only two reviewers, moreover, screened each paper for eligibility, which opens up this analysis to potential biases. The majority of studies were of a semi-field or entomological nature, and may not have similar results in real-life settings. Finally, none of the included articles explicitly discussed blinding of the investigators during their experiments [10][11][12][13][14][15][16][17][18][19][20][21][22].

Conclusions
The implementation of insecticide-treated window screens and eaves could serve as useful tools to reduce mosquito biting incidence, mosquito entry, and increase mosquito mortality (Table 4). This rapid scoping review ties into the essential public health service of developing policy, as the review is a call to action for stakeholders, such as WHO, to encourage window screen and eave installations, as well as local public health agencies to support these efforts [27]. Specific insecticides that public health practitioners can consider include transfluthrin, beta-cyfluthrin, bendiocarb, and deltamethrin, although the method and community one works with should reflect that of the associated study design. Future research should more deeply study the sole impact of treated window screen installations, interventions for An. funestus and An. arabiensis, and household attitudes toward these devices.