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The Efficacy of a Chitin Synthesis Inhibitor Against Field Populations of Organophosphate-Resistant Aedes Aegypti in Brazil

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The Efficacy of a Chitin Synthesis Inhibitor Against Field Populations of Organophosphate-Resistant Aedes Aegypti in Brazil Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 107(3): 387-395, May 2012 387 The efficacy of a chitin synthesis inhibitor against field populations of organophosphate-resistant Aedes aegypti in Brazil Nathalia Giglio Fontoura1,2, Diogo Fernandes Bellinato1,2, Denise Valle1,2, José Bento Pereira Lima1,2/+ 1Laboratório de Fisiologia e Controle de Artrópodes Vetores, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ, Brasil 2Laboratório de Entomologia, Instituto de Biologia do Exército, Rio de Janeiro, RJ, Brasil The mosquito Aedes aegypti is the main focus of dengue control campaigns. Because of widespread resistance against conventional chemical insecticides, chitin synthesis inhibitors (CSIs) are considered control alternatives. We evaluated the resistance status of four Brazilian Ae. aegypti populations to both the organophosphate temephos and the pyrethroid deltamethrin, which are used in Brazil to control larvae and adults, respectively. All vector populations exhibited high levels of temephos resistance and varying rates of alterations in their susceptibility to pyrethroids. The effect of the CSI novaluron on these populations was also investigated. Novaluron was effective against all populations under laboratory conditions. Field-simulated assays with partial water replacement were conducted to evaluate novaluron persistence. Bioassays were continued until an adult emergence inhibition of at least 70% was attained. We found a residual effect of eight weeks under indoor conditions and novaluron persisted for five-six weeks in assays conducted in an external area. Our data show that novaluron is effective against the Ae. aegypti populations tested, regardless of their resistance to conventional chemical insecticides. Key words: Aedes aegypti - chitin synthesis inhibitors - temephos - deltamethrin - novaluron - cross-resistance Among the arboviruses transmitted by mosquitoes The biological insecticide Bacillus thuringiensis se- throughout the world, dengue is presently the most rel- rovar israelensis (Bti) has been employed against Ae. evant; it is endemic to all of the continents, except Eu- aegypti in various municipalities of Brazil. However, rope (Nogueira et al. 2001, Forattini 2002, Claro et al. the reduced field persistence of commercially available 2004). Brazil has an alarming dengue incidence with Bti formulations is an obstacle; under tropical condi- several outbreaks all over the country and an increasing tions, the maximal residual effect observed lasted four incidence of severe cases. Therefore, major public health weeks (Lima et al. 2005). campaigns target this disease (Teixeira et al. 1999, Câ- In contrast to the classical chemical insecticides and mara et al. 2007, MS/SVS 2009). biolarvicides, IGRs are not directly toxic, but act selec- Specific drugs and an effective vaccine against den- tively on the development, metamorphosis or reproduction gue virus are not yet available (Durbin & Whitehead of the target insect species (Hoffmann & Lorenz 1998, 2010). Consequently, the only way to control the dengue Martins & Silva 2004). Among IGRs, the chitin synthesis epidemiological network is to target the virus’ vector, inhibitors (CSIs) act by interfering with the synthesis or Aedes aegypti (Medronho 2006, Braga & Valle 2007). deposition of chitin on the exoskeleton or other chitinised Although the elimination of potential Aedes breeding internal structures, such as the peritrophic matrix (Mer- sites is increasingly considered a crucial component of zendorf & Zimoch 2003, Merzendorf 2005). dengue control, the utilisation of chemical insecticides Novaluron is a CSI that is already utilised in agricul- is still a common measure. Until very recently, the most ture. It is highly effective against Coleoptera, Homoptera commonly used insecticides against Aedes in Brazil and Lepidoptera larvae of several crop pests (Mulla et al. were the organophosphate temephos and the pyrethroid 2003). It can act through ingestion, as verified in the larvae deltamethrin, which are used to control the larval and of the moth species Spodoptera littoralis and Helicoverpa adult populations, respectively (Braga & Valle 2007). armigera, or through contact, as reported with the flies The continuous use of chemical insecticides can Bemisia tabaci and Trialeurodes vaporariorum (Ishaaya lead to the dissemination of resistance and the conse- et al. 1996, 1998). Novaluron is also efficient against Ae. quent failure of the control efforts. Therefore, alternative aegypti larvae, as reported by Mulla et al. (2003) and methods of controlling disease-transmitting vectors are Arredondo-Jiménez and Valdez-Delgado (2006). Because urgently needed. Two examples are entomopathogenic novaluron is recommended by the World Health Organi- bacteria and insect growth regulators (IGRs). zation for use in drinking water, it represents a potential tool in the control of the dengue vector (WHO 2007). We quantified the effect of novaluron against Rock- efeller, a reference Ae. aegypti strain susceptible to in- Financial support: CNPq, FIOCRUZ, SVS-MS, FaperJ secticides. These data enabled later comparisons with + Corresponding author: [email protected] results obtained in the laboratory with wild Ae. aegypti Received 9 June 2011 populations that exhibit varying resistance levels to Accepted 29 November 2011 temephos and deltamethrin, the two most frequently online | memorias.ioc.fiocruz.br 388 Efficacy of novaluron against Ae. aegypti • Nathalia Giglio Fontoura et al. used chemical insecticides in Brazil. The persistence Laboratory bioassays - Temephos quantitative bio- of novaluron under field-simulated conditions was also assays were performed according to Braga et al. (2004), evaluated to assess its potential contribution to resis- following procedures recommended by WHO (1981). A tance management strategies for controlling the dengue complete test consisted of at least 10 insecticide doses, vector in Brazil. with four replicates per dose and 20 larvae per replicate. MATERIALS And METHODS Four tests were performed on each population on differ- ent days. Mortality rates were recorded 24 h after expo- Mosquitoes - Four populations of mosquitoes from sure to the insecticide. Lethal concentrations (LCs) and three regions of Brazil were evaluated: Henrique Jorge, resistance ratios (RRs) were calculated by probit analy- a district of Fortaleza, at the state of Ceará, Aracaju, at sis (Raymond 1985) and by comparison with Rockefeller the state of Sergipe, Cuiabá, at the state of Mato Grosso, LC values, respectively. According to criteria adopted in in the Central West, and Uberaba, state of Minas Gerais, Brazil in 2006, a temephos RR above 3.0 represents the in the Southeast (Fig. 1). With the exception of Fortaleza, cut-off level for triggering resistance management strat- the samples were obtained between August-December egies (Montella et al. 2007). of 2005 by collecting eggs with ovitraps installed to Novaluron emergence inhibition (EI) quantitative cover the whole municipalities, according to Braga et assays were adapted from Martins et al. (2008). Brief- al. (2000) and Lima et al. (2003). Fortaleza eggs were ly, L3 larvae were exposed to eight concentrations of collected with ovitraps in the district of Henrique Jorge, novaluron in transparent plastic cups containing 150 mL a location chosen because of its high infestation rates. of solution. Ten larvae per replicate and eight replicates In this case, 40 ovitraps were installed between March- per concentration were used. Four control replicates con- October of 2006 (Paixão 2007). sisted of larvae exposed to the higher acetone volume Generations F1 through F4 were used for the bioas- used in the experimental conditions (120 µL). A small says listed in Table I. The Rockefeller strain, an insecti- amount of cat food (Friskies®, Purina, Camaquã/RS, cide-susceptible reference strain, was used as a control Brazil) was added on the first day. The plastic cups were for each test (Hartberg & Craig-Jr 1970). Mosquito rear- covered with a nylon mesh in order to avoid adult escape. ing and experimentation were performed at 26 ± 1ºC and Larvae were kept in contact with the CSI until death or relative humidity 70 ± 10%. adult emergence. Mortality at each stage was assessed daily and the success of adult emergence was confirmed Insecticides - The CSI novaluron (Rimon 100 EC) by counting the number of pupae exuvia (Mulla 1974, and technical grade temephos (Fersol 90%) were gen- Mulla et al. 2003). At least three assays were performed erously provided by Agricur and the Brazilian Health for each population, each on different days. Ministry, respectively. Technical grade deltamethrin Qualitative assays with adults were performed us- (99.1%) was purchased from Bayer. ing deltamethrin-impregnated bottles, essentially as de- scribed by da-Cunha et al. (2005), that was adapted from Brogdon and McAllister (1998). Each assay consisted of three bottles impregnated with the insecticide (5 µg/ bottle) and one control bottle impregnated only with ac- etone that was used as the solvent. Each bottle received 20 non-blood fed adult females that were one-three days old. Knockdown was registered at 15 min intervals for up to 2 h. Mosquitoes were then transferred to recov- ery cages free of insecticide and mortality was regis- tered again 24 h later. Each population was submitted to four complete assays on different days. Interpretation of these qualitative assays was performed according to the Davidson and Zahar (1973) criteria modified by
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