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Indoor Spraying with Chlorfenapyr (A Pyrrole Insecticide)

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Indoor Spraying with Chlorfenapyr (A Pyrrole Insecticide) Ngufor et al. Malar J (2020) 19:249 https://doi.org/10.1186/s12936-020-03325-2 Malaria Journal RESEARCH Open Access Indoor spraying with chlorfenapyr (a pyrrole insecticide) provides residual control of pyrethroid-resistant malaria vectors in southern Benin Corine Ngufor1,2,3* , Augustin Fongnikin2,3, Neil Hobbs1,2, Martial Gbegbo2,3, Laurette Kiki2,3, Abibath Odjo2,3, Martin Akogbeto2,3 and Mark Rowland1,3 Abstract Background: New classes of insecticides with novel modes of action, which can provide efective and prolonged control of insecticide-resistant malaria vector populations, are urgently needed for indoor residual spraying. Such insecticides can be included in a rotation plan to manage and prevent further development of resistance in mosquito vectors of malaria. Chlorfenapyr, a novel pyrrole insecticide with a unique mode of action, is being developed as a long-lasting IRS formulation. Methods: The efcacy of several formulations of chlorfenapyr alone and as mixtures with alpha-cypermethrin were evaluated in an experimental hut trial against wild pyrethroid-resistant Anopheles gambiae sensu lato in Cové, Benin, in an attempt to identify the most efective and long-lasting formulations for IRS. The trial lasted 12 months. A com- parison was made with alpha-cypermethrin and bendiocarb formulations. CDC bottle bioassays were performed to investigate cross-resistance to chlorfenapyr in the local vector population. Results: Mortality rates in World Health Organization (WHO) cylinder bioassays were < 5% with pyrethroids due to high levels of pyrethroid resistance, but > 95% with bendiocarb thus confrming susceptibility to carbamates in the vector population. CDC bottle bioassays showed no cross-resistance between pyrethroids and chlorfenapyr. Overall mortality of free-fying mosquitoes entering the experimental huts over the 12-month trial was 4% with alpha-cyper- methrin and 12% with bendiocarb. The chlorfenapyr solo-formulations induced signifcantly higher levels of mortality (38–46%) compared to the bendiocarb (12% P < 0.001) and to the mixture formulations (18–22%, P < 0.05). The origi- nal Sylando 240SC formulation of chlorfenapyr was more efcacious than all other novel chlorfenapyr formulations tested. Bendiocarb induced > 80% mortality in the frst month, but this declined sharply to < 20% by the third month while the mortality rates achieved with the chlorfenapyr formulations (38–46%) were persistent lasting 7–10 months. The mixtures induced signifcantly lower percentage mortality than chlorfenapyr-solo formulations. Wall cone bioas- says only showed mortality rates that were consistent with chlorfenapyr IRS treated huts when the exposure time was increased to 2 h. Conclusion: Indoor residual spraying with chlorfenapyr (Sylando® 240SC) provides moderate but prolonged control of pyrethroid-resistant malaria vectors compared to pyrethroid and bendiocarb IRS. Wall cone bioassays on *Correspondence: [email protected] 1 London School of Hygiene and Tropical Medicine (LSHTM), London, UK Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ngufor et al. Malar J (2020) 19:249 Page 2 of 11 chlorfenapyr-treated walls required longer exposure times of 2 h than the customary 30 min indicating that WHO guidelines on residual cone bioassays need to be more insecticide-specifc. Keywords: Experimental huts, Chlorfenapyr, Mixtures, Indoor residual spraying, Alpha-cypermethrin, Bendiocarb, Sylando, CDC Bottle bioassays, Anopheles, Cové Background active ingredient (clothianidin) and thus share the same Indoor residual spraying (IRS) is a key vector control mode of action; a more diversifed portfolio of IRS insec- intervention for preventing or controlling malaria in ticides is required. many malaria-endemic countries [1]. When applied cor- Chlorfenapyr, a pyrrole insecticide has shown poten- rectly, IRS can rapidly reduce vector populations and tial to control pyrethroid-resistant Anopheles gambiae. It interrupt transmission. Te use of IRS has increased con- works by targeting the oxidative pathways in the insect’s siderably over the past two decades [2] contributing sig- mitochondria disrupting ATP production and thus pre- nifcantly to the remarkable reductions in malaria burden senting a novel mode of action for IRS which difers observed in endemic countries over this period. from other public health insecticides [16–18]. Tere are Te efectiveness of IRS for vector control depends on currently no records of cross-resistance to chlorfenapyr the residual activity of the insecticide on treated home and existing IRS insecticides [18]. While experimental walls and the continued susceptibility of local vectors to hut trials with one formulation of chlorfenapyr for IRS the insecticides being deployed. Until very recently, this (Sylando® 240SC) have reported comparable mortality intervention relied on a small number of insecticides rates against wild free-fying pyrethroid-resistant malaria from four classes of chemistry (pyrethroids, organo- mosquitoes to some conventional IRS products [17], phosphates, carbamates and the organochlorine DDT). reformulation of insecticides can the increase residual Most of the insecticides also showed low residual activ- activity of many classes of IRS insecticides such as pyre- ity (2–5 months) on wall substrates, thus requiring mul- throids [19] and organophosphates [7] and improve bio- tiple rounds of IRS application for efective control [3]. availability and efcacy on treated wall substrates. Unfortunately, malaria vectors have developed resist- In this study, the bioefcacy of a series of new formula- ance to all four classes of compounds [4, 5]. Resistance to tions of chlorfenapyr and mixtures of chlorfenapyr with pyrethroids and DDT is now widespread and increasing alpha-cypermethrin for IRS against wild, free-fying pyre- in intensity the more they are used, making these com- throid-resistant An. gambiae sensu lato (s.l.) was assessed pounds less efective as time goes on [5]. Tis resulted in experimental huts. To provide a more comprehensive in increased use of carbamates and organophosphates in understanding of the bioefcacy and residual activity of recent years [2, 6] driven by the development of a long- chlorfenapyr, the trial was conducted for 12 months and lasting formulation of pirimiphos-methyl (Actellic® comparison was made with IRS with alpha-cypermethrin 300CS) [7]. However, carbamate and organophosphate and bendiocarb. resistance is also increasing in malaria vectors especially in West Africa [4, 5, 8, 9]. Methods Te development of new IRS insecticides which can Study site and experimental huts provide improved and prolonged control of insecticide- Te study was performed at the CREC/LSHTM experi- resistant vector populations is critical for maintaining the mental hut site in Cové, southern Benin (7°14′ N 2°18′ efectiveness of this intervention. Two new IRS insecti- E). Te station is situated at the centre of a large rice- cide products belonging to the neonicotinoid class have growing zone which provides extensive mosquito breed- very recently been approved by the World Health Organ- ing sites throughout the year. Te rainy season extends ization (WHO) [10]. As a strategy for managing insecti- from March to October and the dry season from Novem- cide resistance in local vector populations, vector control ber to February. Te trial ran for 12 months from Sep- programmes are encouraged to implement a rotational tember 2016 to September 2017 in 9 experimental huts schedule of IRS insecticides of diferent modes of action of the West African design [20]. Te huts are built on to reduce selection pressure on the vector [11]. While concrete plinths surrounded by water-flled moats to pre- the newly prequalifed IRS insecticides show potential to vent the entry of scavenging ants and are equipped with improve the control of insecticide-resistant vector popu- veranda traps to capture exiting mosquitoes. Te walls lations [12–15], an efective rotational strategy which will are made of brick plastered with cement on the inside, prevent the development of further resistance cannot with a corrugated steel roof, a ceiling of palm thatch and rely on these compounds alone as they contain the same four window slits (1-cm gap) on the walls through which Ngufor et al. Malar J (2020) 19:249 Page 3 of 11 mosquitoes enter. Te vector species consists of Anoph- unknown pre-weighed amounts of the technical grade of eles coluzzii and
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