Insecticide resistance in disease vectors from Mayotte: an opportunity for integrated vector management

Pocquet et al. Parasites & Vectors 2014, 7:299 http://www.parasitesandvectors.com/content/7/1/299 RESEARCH Open Access Insecticide resistance in disease vectors from Mayotte: an opportunity for integrated vector management Nicolas Pocquet1*, Frédéric Darriet1, Betty Zumbo2, Pascal Milesi3, Julien Thiria2,3,4, Vincent Bernard1, Céline Toty1,2, Pierrick Labbé3 and Fabrice Chandre1 Abstract Background: Mayotte, a small island in the Indian Ocean, has been affected for many years by vector-borne diseases. Malaria, Bancroftian filariasis, dengue, chikungunya and Rift Valley fever have circulated or still circulate on the island. They are all transmitted by Culicidae mosquitoes. To limit the impact of these diseases on human health, vector control has been implemented for more than 60 years on Mayotte. In this study, we assessed the resistance levels of four major vector species (Anopheles gambiae, Culex pipiens quinquefasciatus, Aedes aegypti and Aedes albopictus) to two types of insecticides: i) the locally currently-used insecticides (organophosphates, pyrethroids) and ii) alternative molecules that are promising for vector control and come from different insecticide families (bacterial toxins or insect growth regulators). When some resistance was found to one of these insecticides, we characterized the mechanisms involved. Methods: Larval and adult bioassays were used to evaluate the level of resistance. When resistance was found, we tested for the presence of metabolic resistance through detoxifying enzyme activity assays, or for target-site mutations through molecular identification of known resistance alleles. Results: Resistance to currently-used insecticides varied greatly between the four vector species. While no resistance to any insecticides was found in the two Aedes species, bioassays confirmed multiple resistance in Cx. p. quinquefasciatus (temephos: ~ 20 fold and deltamethrin: only 10% mortality after 24 hours). In An. gambiae, resistance was scarce: only a moderate resistance to temephos was found (~5 fold). This resistance appears to be due only to carboxyl-esterase overexpression and not to target modification. Finally, and comfortingly, none of the four species showed resistance to any of the new insecticides. Conclusions: The low resistance observed in Mayotte’s main disease vectors is particularly interesting, because it leaves a range of tools useable by vector control services. Together with the relative isolation of the island (thus limited immigration of mosquitoes), it provides us with a unique place to implement an integrated vector management plan, including all the good practices learned from previous experiences. Keywords: Insecticide resistance, Mosquito control, Resistance management, Integrated vector management * Correspondence: 1 Institut de Recherche pour le Développement, Unité Mixte de Recherche MIVEGEC (IRD 224-CNRS 5290-UM1-UM2), 911, avenue Agropolis, BP 64501 34394 Montpellier cedex 5, France Full list of author information is available at the end of the article © 2014 Pocquet et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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. Pocquet et al. Parasites & Vectors 2014, 7:299 http://www.parasitesandvectors.com/content/7/1/299 Background Mayotte is a French island located in the Indian Ocean, in the Comoros archipelago. For many years, this island has been heavily affected by vector-borne diseases. Historically, the two diseases that mainly plagued the island were Bancroftian filariasis, mostly transmitted by Culex pipiens quinquefasciatus [1-4], and malaria, transmitted by several anopheline species, including Anopheles gambiae s.s. [5,6]. Today, malaria is still present in Mayotte, although the number of cases has significantly decreased during the last two years [7]. Moreover, while the disease was considered eliminated from the island, some cases of Bancroftian filariasis were recently recorded [8]. In addition to these endemic diseases, a major dengue fever outbreak in 1943 [9] and a chikungunya outbreak in 2005 and 2006 have also affected Mayotte [10]. Both are due to arboviruses transmitted by Aedes species. However, while dengue was principally transmitted by Aedes aegypti, chikungunya main vector was Ae. albopictus [11]. This last species, observed for the first time on the island in 2001 [12], has since almost completely replaced Ae. aegypti [13], and certainly played the main role in the recently recorded cases of dengue and chikungunya [14]. Finally, new arboviruses recently started to circulate on the island, including the Rift Valley Fever virus [15]. To limit the impact of these diseases on people from Mayotte, many vector control programs have been implemented since the early 50s [16]. Most of the efforts were intended to control Cx. p. quinquefasciatus and An. gambiae populations, to prevent filariasis and malaria. They relied almost entirely on the use of chemical insecticides (from the organochlorines (OC), organophosphates (OP) and pyrethroids (PYR) families), through extensive applications on larval breeding sites, indoor residual spraying treatments (IRS) [3,5,9,16-18] and, more recently, long-lasting insecticide treated nets (LLIN). These vector control campaigns have had good results and greatly limited the impact of lymphatic filariasis and malaria in Mayotte [4,6]. Today however, several constraints could impede vector control. The first constraint is administrative, with a significant reduction of the number of insecticides available for vector control due to new Europeana regulations [19]. All pesticide molecules had indeed to be re-examined in 2007 for marketing authorization, through a costly application filed by the producers; some unprofitable yet efficient molecules were not supported. There are also technical difficulties, due to the increasing role of Ae. albopictus as a major vector of arboviruses in Mayotte. Due to their preferences for confined larval breeding sites (natural, like tree holes, or artificial, like used tires) and their eggs resistant to desiccation [20,21], Ae. albopictus is particularly difficult to reach through conventional sprays of Page 2 of 12 insecticides. The third type of constraints is ecological: Mayotte is a small island with a specific ecosystem encompassing many endemic species, and as such must be protected from anthropic pollutions. The effects of insecticide treatments on non-target fauna and their potential accumulation in the food chain need to be taken into account and limited. Finally, the last and most important cha (...truncated)