View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by edoc Suter et al. Parasites & Vectors (2017) 10:431 DOI 10.1186/s13071-017-2364-5 RESEARCH Open Access Insecticide susceptibility of Aedes albopictus and Ae. aegypti from Brazil and the Swiss-Italian border region Tobias Suter1,2,3, Mônica Maria Crespo4, Mariana Francelino de Oliveira4, Thaynan Sama Alves de Oliveira4, Maria Alice Varjal de Melo-Santos4, Cláudia Maria Fontes de Oliveira4, Constância Flávia Junqueira Ayres4, Rosângela Maria Rodrigues Barbosa4, Ana Paula Araújo4, Lêda Narcisa Regis4, Eleonora Flacio5, Lukas Engeler5, Pie Müller1,2* and Maria Helena Neves Lobo Silva-Filha4 Abstract Background: Aedes aegypti and Ae. albopictus are two highly invasive mosquito species, both vectors of several viruses, including dengue, chikungunya and Zika. While Ae. aegypti is the primary vector in the tropics and sub-tropics, Ae. albopictus is increasingly under the public health watch as it has been implicated in arbovirus-transmission in more temperate regions, including continental Europe. Vector control using insecticides is the pillar of most control programmes; hence development of insecticide resistance is of great concern. As part of a Brazilian-Swiss Joint Research Programme we set out to assess whether there are any signs of existing or incipient insecticide resistance primarily against the larvicide Bacillus thuringiensis svar. israelensis (Bti), but also against currently applied and potentially alternative insecticides in our areas, Recife (Brazil) and the Swiss-Italian border region. Methods: Following World Health Organization guidelines, dose-response curves for a range of insecticides were established for both colonized and field caught Ae. aegypti and Ae. albopictus. The larvicides included Bti,twoof its toxins, Cry11Aa and Cry4Ba, Lysinibacillus sphaericus, Vectomax CG®, a formulated combination of Bti and L. sphaericus, and diflubenzuron. In addition to the larvicides, the Swiss-Italian Ae. albopictus populations were also tested against five adulticides (bendiocarb, dichlorodiphenyltrichloroethane, malathion, permethrin and λ-cyhalothrin). Results: Showing a similar dose-response, all mosquito populations were fully susceptible to the larvicides tested and, in particular, to Bti which is currently used both in Brazil and Switzerland. In addition, there were no signs of incipient resistance against Bti as larvae were equally susceptible to the individual toxins, Cry11Aa and Cry4Ba. The field-caught Swiss-Italian populations were susceptible to the adulticides tested but DDT mortality rates showed signs of reduced susceptibility. Conclusions: The insecticides currently used for mosquito control in Switzerland and Brazil are still effective against the target populations. The present study provides an important reference as relatively few insecticide susceptibility surveys have been carried out with Ae. albopictus. Keywords: Vector control, Insecticide resistance, Biolarvicides, Insect growth regulator * Correspondence: [email protected] 1Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Socinstrasse 57, PO Box, 4002 Basel, Switzerland 2University of Basel, Petersplatz 1, 4003 Basel, Switzerland Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Suter et al. Parasites & Vectors (2017) 10:431 Page 2 of 11 Background As a reaction to the dengue epidemics in Brazil, a na- Dengue (DENV), chikungunya (CHIKV) and Zika virus tional programme with the aim to eliminate Ae. aegypti (ZIKV) are mosquito-borne viruses of medical import- (Programa para Erradicação do Aedes aegypti)was ance in most tropical regions but also emerging in more launched in 1996, and in 2002 it became the National temperate regions including continental Europe. Dengue Programme for Dengue Control (Programa Nacional de fever is the most prevalent mosquito-borne disease Controle de Dengue). The main goal of the programme worldwide with an estimated 390 million cases per year is to fight dengue through integrated vector control strat- [1]. In the Americas, most dengue cases have been re- egies, including the use of larvicides [18]. Until 2008 the ported from Brazil, which has been affected by several main larvicide used in the programme was the organo- epidemics since the 1990s [2]. In 2016, around 1.5 phosphate temephos. Due to increasing resistance ob- million cases were reported from all states of the coun- served in several Ae. aegypti populations [19–21] try [3]. In Brazil Aedes aegypti is the major vector of temephos was replaced by the biological larvicide Bacil- dengue and all four DENV serotypes are co-circulating lus thuringiensis svar. israelensis (Bti) in some munici- in the country [4]. In 2014, the first autochthonous chi- palities in 2002. Then, in 2009, it was replaced by the kungunya cases have been detected in Brazil and in 2016 insect growth regulators (i.e. chitin synthesis inhibitors), a total of 271,824 confirmed cases have been reported diflubenzuron and novaluron [19, 22] and finally, be- from several states, including Pernambuco [3]. In 2015, tween 2014 and 2015, by pyriproxyfen, a juvenile hor- autochthonous cases of ZIKV were also reported from mone analogue [23]. Already in 2001, the health Brazil for the first time [5] and 125,319 cases were con- secretary of the city of Recife had decided to use Bti as firmed in 2016 [3]. All the above cases have been linked the sole larvicide to fight Ae. aegypti. Bti equally targets to Ae. aegypti, a highly competent vector of arboviruses. Ae. albopictus larvae that share the same breeding sites In continental Europe, the most prominent example is with Ae. aegypti in many urban areas [24, 25] and, there- the chikungunya outbreak in Ravenna, Italy in 2007 with fore, monitoring of Bti susceptibility to both Aedes spe- over 200 confirmed cases and one death. The outbreak cies is needed. was linked to a transmission by the invasive mosquito Ae. In Switzerland, Ae. albopictus was found for the first albopictus and a single viraemic person that returned with time in the Canton of Ticino in the southernmost tip of chikungunya from India [6]. CHIKV is a mosquito-borne the country in 2003 [13]; its surveillance has since been alphavirus indigenous to African countries, the Indian continuously expanded [26]. Today, the monitoring sys- subcontinent and Southeast Asia where it causes endemic tem consists of more than 1000 ovitraps that are ana- and epidemic fever outbreaks [7]. The outbreak in Italy lysed bi-weekly and the trapping data are used to demonstrates the vector capacity of the local Ae. albopic- coordinate targeted applications of insecticides [26]. In tus population to transmit CHIKV. Following this out- addition, public information campaigns are carried out break, additional cases of autochthonous chikungunya in order to reduce breeding sites on private grounds. On were recorded in mainland France [8] as well as dengue public grounds, where larval breeding sites may not be cases in both Croatia and France (e.g. [9–11]). These out- removed (e.g. water drains), the authorities mainly apply breaks show that continental Europe is vulnerable to the Bti and diflubenzuron for larval control. In addition, transmission of “tropical” arboviruses, particularly in re- focal spraying of permethrin to target adult mosquitoes gions where Ae. albopictus and Ae. aegypti are present. is implemented if there is a risk of autochthonous trans- Ae. aegypti and Ae. albopictus are the main vectors of mission due to imported fever cases. Despite these ef- DENV and CHIKV worldwide. Both mosquito species forts, Ae. albopictus has expanded its range in the have recently shown a large geographical expansion. Ae. Canton of Ticino over the last years [12, 26], requiring albopictus, known as the Asian tiger mosquito is among careful monitoring of the current insecticides’ efficacy. the 100 of the world’s most invasive alien species [11] Bti formulations are widely used and shown to be ef- and is currently present in many regions in the Ameri- fective in controlling mosquitoes [27–29]. The toxicity cas, Africa, Australia and Europe, where its presence of Bti against mosquito larvae is linked to crystals, pro- has been reported in several European countries, in- duced during bacterial sporulation, that contain mainly cluding Switzerland [12–14]. In Brazil, Ae. albopictus four protoxins Cry11Aa, Cry4Aa, Cry4Ba and Cyt1Aa was recorded for the first time in 1986 and has since [30]. When ingested by mosquito larvae the crystals are spread throughout the country [15]. The rapid world- dissolved in the alkaline milieu of the midgut and the re- wide expansion of Ae. albopictus is attributed to its leased protoxins are then activated into toxins by gut eggs that resist desiccation and may undergo diapause, proteases. The toxins bind to the receptors on the mid- an adaptation