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Chemical control and insecticide resistance status of sand fly vectors worldwide

['Sofia Balaska', 'Institute Of Molecular Biology', 'Biotechnology', 'Foundation For Research', 'Technology Hellas', 'Heraklion', 'Department Of Biology', 'University Of Crete', 'Emmanouil Alexandros Fotakis', 'Department Of Crop Science']

Date: 2021-08

Chemical control of sand flies.

Indoor residual and space spray applications

IRS comprises the backbone of chemical control interventions in high-burden areas [13]. IRS involves coating of the inner walls and other surfaces of households and animal shelters with a residual insecticide, primarily targeting endophilic and endophagic vector species (Table 1). The intervention’s operational success relies on multifarious parameters, including commitment to the technical guidelines by properly trained spraying personnel, effective ground program supervision, the type of wall surface treated/sprayed, the quality and residual activity of the active ingredients/formulations used, the climatic conditions, and the entomological/epidemiological features of the intervention area (e.g., levels of indoor versus outdoor transmission) [14,15].

Dichlorodiphenyltrichloroethane (DDT)-based IRS, often integrated within malaria elimination programs, was the mainstay of sand fly control since 1944 and for several decades to follow [8], largely contributing to leishmaniasis transmission suppression in this period in countries such as India, Nepal, Iran, Syria, Italy, Greece, and Peru [10,11,16]. However, the introduction of restrictive measures against several organochlorines (OCs) in the 1970s, due to their high toxicity risk (for human and animal health) and environmental persistence, in conjunction with reports on DDT resistance in sand fly vector populations in disease-endemic regions (e.g., India) [11], imposed a shift toward the use of safer insecticides. To date, pyrethroids are the primary insecticide class used in IRS applications around the globe [17]. Indicatively, interior wall spraying with lambda-cyhalothrin in villages of the Peruvian Andes [10] and deltamethrin in regions of the Indian subcontinent [14,18] resulted in a 70% or higher household-level reduction in the abundance of Lutzomyia spp. and Phlebotomus argentipes sand flies, respectively, for up to 6 months post-intervention. During a controlled trial in villages of Bangladesh, 2 rounds of alpha-cypermethrin spraying resulted in an average maximum of 75% P. argentipes population density reduction (14 months post-first round and 2 months post-second round) [19]. A markedly lower vector density was reported in pyrethroid-treated kala-azar–endemic districts in eastern Nepal (mean drop of 94.5% in the number of sand flies trapped per night/per house over a 5-month period post-intervention) [9]. Furthermore, alpha-cypermethrin spraying in areas of northern Morocco significantly limited CL cases from 9 to 0 per 1,000 inhabitants [15], yet no considerable effect was observed on the abundance of Phlebotomus sergenti, the main CL vector in the region.

Several field studies have reported suboptimal results upon IRS operations with the duration of insecticides’ residual efficacy being the critical point. For example, recent small-scale pyrethroid IRS trials targeting P. argentipes in high-risk areas of the Indian subcontinent failed to sustain a significant population reduction for more than 12 weeks [14,20]. Similar results were reported following lambda-cyhalothrin IRS applications against Lutzomyia vectors in Margarita Island, Venezuela [21,22].

Insecticide-treated durable wall lining (DWL) is an alternative type of indoor residual intervention, relying on the application of an insecticide-treated thin polyethene net covering partially or completely the inner wall surfaces [23] (Table 1). This new technology was created to improve the residual effect of insecticides commonly observed in IRS treatments and for the practicality of the application. Although we lack epidemiological data showing the method’s impact on leishmaniasis focal incidence, recent comparative analyses of different interventions (DWL, IRS, and slow-release insecticide tablet impregnation of bed nets) in southern Asian countries evaluated DWL as the most powerful tool for reducing the abundance of local P. argentipes populations [13,24]. Indicatively, Huda and colleagues [25] recorded a 63% to 73% decrease of the indoor female sand fly density in the DWL intervention clusters 1 month post-installation, while the material retained its insecticidal activity for at least 12 months. Overall, linings have been accepted in a number of traditional settings (particularly in isolated villages), where IRS logistics pose a significant challenge. However, the intervention’s high cost along with the deposition and handling of the large volume of insecticide-treated plastic surfaces following their use remain critical issues possibly having triggered the cessation of the manufacturing processes.

Indoor space spraying (ISS), targeting resting or flying individuals, has been performed against malaria mosquitoes especially as an emergence response, offering a one-off knockdown (KD) effect (often also exploited for monitoring purposes), followed by a short residual effect. Even though ISS adulticidal outcome on mosquito vectors has been assessed [26], there is currently no evidence available of its potential operational efficacy against sand fly vectors.

Insecticide-treated bed nets

ITNs and long-lasting ITNs (LLINs) comprise important intradomestic Leishmania transmission control tools through acting as a toxic physical barrier against blood-seeking sand flies [27], offering both personal- and community-level protection upon high net coverage/distribution (Table 1). Their field efficacy has been evidenced in countries of the Mediterranean basin, Latin America, and Africa [10]. In community-wide trials conducted in Sudan and countries of the Middle East, broad distribution of ITNs reduced the leishmaniasis burden by 59% to 98% for at least 1 year [28–30]. Specifically in Iran, epidemiological evidence revealed a close to elimination of CL incidence rate in high-risk regions of the country where pyrethroid-treated bed nets and curtains had been in use for 1- or 2-year trials [16,30–32]. A remarkable drop in the annual CL incidence (compared to control regions) was also reported upon ITNs deployment in 2 intervention areas in Sanliurfa, Turkey [33]. Mondal and colleagues [34] and Chowdhury and colleagues [35] reported a 66.5% and 46.8% VL incidence reduction in rural areas of Bangladesh after 1 and 3 years of ITNs application, respectively.

A small number of community-scale ITNs/LLINs trials, alongside the recorded reduction of leishmaniasis incidence, also report a reduction of the local vector populations’ abundancy [9,20,30,36]. Indicatively, Chowdhury and colleagues [19] observed a maximum drop of 78% in P. argentipes household density following village trials in Bangladesh. A similar effect (60% reduction) against the same vector species, lasting for at least 18 months, was observed by Mondal and colleagues [34], accompanying deltamethrin impregnation of the existing bed nets. In addition, trials conducted in the Indian subcontinent have shown a sand fly density drop persisting for 9 months in the ITN clusters [24].

The cotreatment of LLINs with insecticide synergists, such as piperonyl butoxide (PBO; a known inhibitor of P450 monoxygenases), appears a highly promising supplement for vector control in vector-borne disease (VBD) endemic areas of intense pyrethroid resistance. Gunay and colleagues [37], having assessed the protective efficacy of Olyset Plus LLIN (2% permethrin and 1% PBO) in a hyperendemic village in Cukurova region, Turkey, reported a 92% protection rate from Phlebotomus tobbi bites and a decrease of CL prevalence up to 4.78%, during the post-intervention year.

In some cases, village-wide distribution of LLINs in India and Nepal did not significantly impact the infection rates nor affected the transmission occurring in these regions’ ecological settings [38]. Operational issues, short residual efficacy, lack of community compliance, and/or possible IR/tolerance, including potential behavioral shifts in vector species’ feeding patterns, are likely to be responsible for such unsatisfactory results [13,20,38,39]. Indicatively, the KALANET project, a cluster randomized controlled trial of mass ITNs distribution implemented in India and Nepal, failed at remarkably diminishing vector’s survival and, thus, VL infection rates, due to P. argentipes exhibiting a more intensely zoophilic and exophagic behavior than previously observed in some endemic biotopes [39,40].

Other insecticide-treated materials (ITMs) for personal and community protection

In VBD high risk–prone regions, workers, the public, and the military commonly utilize clothing impregnated with insecticides [41] (Table 1). Permethrin is the preferred active ingredient (for treating clothing), due to its low health risk, combined with its insecticidal and repellent effect. Although the protective efficiency of insecticide-treated clothing is substantial against mosquitoes, we lack robust evidence concerning sand flies. The few available studies report a leishmaniasis protection rate varying from 0% to 79% [41].

In Jordan Valley, Iran, field trials with pyrethroid-impregnated vertical fine mesh nets serving as physical barriers against sand flies entering inhabited areas [42,43] reduced the abundance of sand flies trapped in the enclosed areas by over 60% compared to pre-fence net placement. These preliminary results suggest that this could be a valuable additive measure integrated in comprehensive chemical control campaigns.

Outdoor residual and space spray applications

Insecticide spraying on trees and vegetation around human dwellings, animal shelters, or in barrier zones targeting flying, breeding, or resting insects is not a widely applicable measure against Leishmania vectors, as it comes with important limitations due to inadequate habitat coverage and poor insecticide residual activity [10] (Table 1).

However, multiple trials of cold fogging or ULV space spray insecticide applications in countries of Latin America have demonstrated satisfying results in the reduction of sand fly population and leishmaniasis incidence within the intervention sites [10]. In a recent study carried out in western Kenya, malathion and synthetic pyrethroid + PBO formulations tested in ULV applications suppressed the local sand fly populations (mainly, Phlebotomus duboscqi) by at least 50%, immediately after spraying [44]. Encouraging results were also published by Chaskopoulou and colleagues [45], where Phlebotomus perfiliewi populations decreased by 66% in heavily infested animal facilities of Greece, 24 hours post-high rate ULV ground application of a deltamethrin-based formulation.

Attractive toxic sugar baits (ATSBs)

Composed of a sugar source, an attractant and an oral toxin/insecticide, attractive toxic sugar baits (ATSBs) are applied against indoor or outdoor insect vector populations, targeting their sugar-seeking behavior (Table 1). This method appears to act on both male and female insects during their adult life span, by killing them either directly or through dissemination [46]. ATSBs have been applied in small-scale field trials in multiple formats: (i) sprayed on vegetation; (ii) coating barrier fences around villages; and (iii) incorporated into bait stations, overall generating encouraging preliminary results. In zoonotic CL-endemic regions of the Middle East, specifically Iran and Israel, vegetation and barrier fencing ATSB applications including 1.0% w/w boric acid led to a close to 90% reduction of the Phlebotomus papatasi populations [47–49]. In addition, evaluation of the residual activity of ATSB-treated barrier fence nets in central Iran revealed their potency for at least 60 days post-installation, causing at that time point a mortality rate of 51% in the field-caught, cone bioassay–exposed P. papatasi sand flies [50]. Finally, Qualls and colleagues [46], following a 4-week period of ATSB vegetation spraying and bait station deployment in a Moroccan agricultural area, recorded an 83% decrease in P. papatasi and P. sergenti populations within the treated sites, with negligible impact on non-target insects.

Topical and spatial repellents

Natural or synthetic compounds with repellent activity are commonly applied against several insect vectors either at the household level or on skin/clothing for personal protection, hindering the vector–human interaction (Table 1). Spatial repellents appear in different formats, such as candles, coils, and sprays.

Laboratory pilot trials on the repellency effect of several chemical compounds, such as picaridin, SS220, N,N-diethyl-3-methylbenzamide (DEET), and ethyl-butylacetylaminoproprionate (IR3535), proved that they could serve as biting deterrents against different sand fly species (e.g., P. papatasi, P. duboscqi, Phlebotomus perniciosus). However, the repellency effect and duration seem to vary depending on the targeted species [51]. Active natural ingredients derived from plants, such as Ricinus communis, Solanum jasminoides, Capparis spinosa, and Geranium spp., have also been tested against sand fly laboratory colonies, displaying repellent and/or insecticidal properties [52], yet the potential effect of natural ingredients’ field application against local sand fly population abundance and/or protection from sand fly bites remains greatly understudied.

Applications targeting sand fly immature stages

The control of sand flies at their immature stages mainly relies on habitat modification and manipulation (within the EVM context). Sand flies breed in a wide variety of terrestrial sites that are not easily detectable nor well characterized, making the use of larvicides difficult (Table 1). However, an increasing effort to develop tools for easy identification of sand fly larval habitats [53] may greatly enhance the precision and efficacy of larviciding interventions.

Within the framework of larval chemical control, Gómez-Bravo and colleagues [54] evaluated the Dragon Max formulation (i.e., a combination of 2 active ingredients: permethrin + pyriproxyfen (insect growth regulator (IGR)) versus a permethrin (only) formulation, in field applications in Clorinda, Argentina. Chicken coops and surrounding vegetation were sprayed, covering potential phlebotomine breeding sites. The denoted drastic decrease in the abundance of Lutzomyia longipalpis exposed to Dragon Max lasted for 21 weeks and was not observed in areas exposed to permethrin-only treatments. In another study conducted in Bangladesh, no significant reduction was observed following chlorpyrifos (organophosphate (OP)) spraying in sand fly oviposition sites, i.e., shady, moisture, and rich in organic materials (e.g., cow dung) places, outside human dwellings, and cattle shades [19].

Other active ingredients of biological origin, such as formulations of Bacillus thuringiensis var. israelensis (Bti) and Bacillus sphaericus (Bsph) have been also tested against sandflies. Bti has been shown to cause significant mortality in both larval and adult stages, under laboratory conditions, whereas a similar effect was noticed upon Bsph field spraying on vegetation [10]. Application of the entomopathogenic fungi Metarhizium anisopliae in termite mounds used for resting/breeding sites led to 3- to 10-fold increase in mortalities of the sand fly vectors Phlebotomus martini and P. duboscqi, 9 weeks post-application in Rabai, Kenya, while a reduced adult sand fly longevity was also observed [55]. However, the operational efficiency of such interventions is yet to be evidenced.

Insecticide zooprophylaxis and animal protection

Systemic treatment of livestock (e.g., cattles) and/or other sand fly vertebrate reservoir hosts with orally administered insecticides displays promising potential in facilitating the control of outdoor blood-feeding adults and/or feces-feeding larvae (Table 1). To date, several laboratory studies have revealed reduced survival of Phlebotomus spp. larvae upon feeding on Mesocricetus auratus hamsters’ feces treated with IGR larvicides, such as diflubenzuron, novaluron, and juvenile hormone analogues [56]. Ivermectin, widely used against zoophilic and anthropophilic/anthropozoophilic insect vectors and the pathogens they transmit [57,58], has proved a powerful rodent feed through insecticide in Leishmania vector control laboratory trials [59]. Additionally, the significant activity of the systematic use of ivermectin-treated livestock against Anopheles mosquito vectors’ survival in field conditions may have a similar impact on sand fly populations [60]. Similarly, fipronil single dose–treated rodent (Meriones shawi, Rattus rattus, Bandicota bengalensis, etc.) and cattle (Bos taurus, Bos indicus) baits have been evaluated, under both laboratory and field conditions, against Phlebotomus spp. (i.e., P. argentipes, P. papatasi), causing an effect of almost total larvae/adult mortality (80% to 100%) lasting for 3 to 6 weeks [61–64]. Protection of dogs, the principal Leishmania infantum reservoir host, from sand fly bites is commonly mediated by slow-release insecticide IDCs that maintain an antifeeding and insect-killing activity for approximately 6 to 8 months (Table 1). So far, collars impregnated with deltamethrin and flumethrin/imidacloprid have been developed and validated both in laboratory and field studies [65]. Recently, Yimam and colleagues [66] systematically reviewed the effectiveness of IDCs. Mass use of IDCs has efficiently reduced the risk of canine leishmaniasis (canL) transmission by 46% to 86% during intervention trials in Italy, Iran, and Brazil. High collar coverage (approximately 90%) within the target area was shown to be essential to abate canL occurrence. However, this comes at a considerable economic cost and is not always feasible [66]. Interestingly, community-wide deployment of deltamethrin IDCs in Iran demonstrated an additional protective efficiency against infantile L. infantum infections [67].

Biocidal spot-on formulations such as lotions and sprays comprise complementary prophylactic measures mostly applied at an individual–animal level [68].

[END]

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