Short Communication. C. D. Chen, 1,5 A. C. Chin, 1 K. W. Lau, 1 V. L. Low, 2 H. L. Lee, 3 P. K. Y. Lee, 4 A. A. Azidah, 1 and M.

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1 Short Communication Journal of Medical Entomology, XX(X), 2018, 1 5 doi: /jme/tjy130 Short Communication Bioefficacy Evaluation of Commercial Mosquito Coils Containing Metofluthrin, d-allethrin, d-trans Allethrin, and Prallethrin Against Aedes albopictus (Diptera: Culicidae) in Malaysia C. D. Chen, 1,5 A. C. Chin, 1 K. W. Lau, 1 V. L. Low, 2 H. L. Lee, 3 P. K. Y. Lee, 4 A. A. Azidah, 1 and M. Sofian-Azirun 1 1 Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia, 2 Tropical Infectious Diseases Research and Education Centre (TIDREC), University of Malaya, Kuala Lumpur, Malaysia, 3 Medical Entomology Unit, Institute for Medical Research, Jalan Pahang, Kuala Lumpur, Malaysia, 4 Office of Safety and Health, University of Malaya, Kuala Lumpur, Malaysia, and 5 Corresponding author, chen_ctbr@um.edu.my Subject Editor: Thomas Scott Received 15 December 2017; Editorial decision 13 July 2018 Abstract The bioefficacy of commercial mosquito coils containing four different active ingredients, namely metofluthrin, d-allethrin, d-trans allethrin, and prallethrin against Aedes albopictus (Skuse) (Diptera: Culicidae) from 10 states in Malaysia, was evaluated using the glass chamber method. In this study, Ae. albopictus exhibited various knockdown rates (50% knockdown time, KT 50 ), ranging from 2.50 to 5.00 min, 2.50 to 7.00 min, 3.00 to 8.00 min, and 5.00 to min for metofluthrin, d-trans allethrin, d-allethrin, and prallethrin, respectively. Overall, all strains of Ae. albopictus were most susceptible to metofluthrin, with mortality rates >80%. On the other hand, mortality rates ranging from 5.0 to 100% were observed from all populations exposed to d-trans allethrin, d-allethrin, and prallethrin. In addition, significant correlations between KT 50 of metofluthrin and d-allethrin (r = 0.758, P = 0.011), metofluthrin and prallethrin (r = 0.676, P = 0.032), d-allethrin and d-trans allethrin (r = 0.832, P = 0.003), d-allethrin and prallethrin (r = 0.921, ), and d-trans allethrin with prallethrin (r = 0.941, ) were detected, suggesting some levels of cross-resistance within the pyrethroid insecticides. This study demonstrated that metofluthrin can induce high insecticidal activity in Ae. albopictus in Malaysia, followed by d-trans allethrin, d-allethrin, and prallethrin. Key words: Aedes albopictus, mosquito coil, pyrethroid, Malaysia Aedes albopictus (Diptera: Culicidae), also known as the Asian tiger mosquito, is indigenous to the rain forest of Southeast Asia. It has spread to other regions of the world in the early 20th century including Africa, Europe, and the Americas (Gratz 2004, Paupy et al. 2009). Aedes albopictus is an exophilic species that feeds on animal blood and dwells outdoors. However, Ae. albopictus has been closely associated with humans in terms of shared habitat because of the overlapping of urban and rural regions (Jirakanjanakit et al. 2007). As a result, Ae. albopictus has been incriminated as the vector of various human diseases such as dengue, chikungunya, and Zika. The annual reported dengue cases were notably high with million cases from dengue endemic regions, especially in tropical countries (WHO 2012). Mosquito coils are the most widely used personal protection product to repel mosquitoes (Yap et al. 2003). To ensure the efficacy of mosquito coils in repelling mosquitoes, several coil efficacy studies have been conducted on both laboratory and field strains of Aedes aegypti and Culex quinquefasciatus in Malaysia (Yap and Chung 1987; Yap et al. 1990, 1996; El-garj et al. 2015; Chin et al. 2017). Although Avicor et al. (2014) have reported the enzyme expression in a laboratory strain of Ae. albopictus upon exposure to several coils, there is still a lack of information on the efficacy status of mosquito coils against Malaysian Ae. albopictus. Hence, the present study aimed to evaluate the bioefficacy of commercial coils containing metofluthrin, d-allethrin, d-trans allethrin, and prallethrin against field populations of Ae. albopictus, for the first time in Malaysia. Materials and Methods Field strains of Ae. albopictus were collected using oviposition traps (ovitraps) from 10 states in Malaysia (Table 1). The collection and The Author(s) Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please journals.permissions@oup.com. 1

2 2 colonization of Ae. albopictus were performed as described in Lee (1992) and Chin et al. (2017), respectively. A laboratory reference strain of Ae. albopictus from Institute for Medical Research (IMR), Kuala Lumpur, which has been colonized under insecticide-free condition for 64 generations was included for comparison. Four commercial coils with different active ingredients, metofluthrin 0.01% w/w, d-allethrin 0.20% w/w, d-trans allethrin 0.15% w/w, and prallethrin 0.04% w/w, all available in Malaysian markets were used for mosquito coil bioassays. The bioassays were conducted following the standardized protocol by Standards and Industrial Research Institute of Malaysia (SIRIM 1986). Briefly, a portion of commercial mosquito coil weighing 0.50 g was prepared, and fixed using a coil stand, with both ends ignited inside the chamber. In total, twenty 2- to 5-dold sugar-fed adult females were released into the chamber. The number of knocked-down mosquitoes was recorded for 20 min at 30-s interval. Those that were unable to fly or no longer maintain a normal posture were considered as knockdown. After 20 min exposure, all mosquitoes were transferred to clean cages for observation of 24-h posttreatment mortality. Sugar solution was provided in clean cages. The tests were run in triplicate for each active ingredient and location. Control experiments were performed by placing the adult females into the chamber without exposure to any coils for 20 min. The mortality rates were recorded after 24 h (Chin et al. 2017). Mosquito coil bioassay data in the range of 5 95% knockdown were subjected to Kaplan Meier survival function using computer software SPSS (version 21) to obtain 50% knockdown time (KT 50 ). The resistance ratios (RRs) of field collected Ae. albopictus were calculated by dividing the KT 50 of the field strain by KT 50 of the reference strain. RR values <5, 5 10, and >10 are indicative low, medium, and high resistance, respectively (Mazzarri and Georghiou 1995). Spearman rank-order correlation analysis between a pair of knockdown rates was used to determine Table 1. Aedes albopictus collection sites in Malaysia Malaysia Region State District Study site Geographical coordination Landscape Peninsular Northern Penang Gelugor Taman Pekaka N, E Perak Menglembu Taman Bukit Merah N, E Central Federal Territory Kuala Lumpur Taman Sri Endah N, E Selangor Ampang Taman Muda N, E Southern Johor Batu Pahat Taman Setia Jaya N, E Melaka Bukit Baru Taman Bahagia N, E Negeri Sembilan Titi Taman Desa N, E East Coast Pahang Gambang Kampung Sungai N, Belat E East Malaysia East Sabah Kota Kinabalu Taman Selesa N, E West Sarawak Kuching Tabuan Desa N, E Table 2. time (KT 50 ) and RR of Malaysian Aedes albopictus adults against metofluthrin (0.01%), d-allethrin (0.20%), d-trans allethrin (0.15%), and prallethrin (0.04%) Active ingredients Metofluthrin (0.01%) d-allethrin (0.20%) d-trans allethrin (0.15%) Prallethrin (0.04%) Location KT 50 (min) (95% CL) RR Reference 2.50 ( ) ( ) ( ) ( ) - Penang 4.00 ( ) ( ) ( ) ( ) 1.33 Perak 3.00 ( ) ( ) ( ) ( ) 1.11 Selangor 3.00 ( ) ( ) ( ) ( ) 1.56 Kuala Lumpur 5.00 ( ) ( ) ( ) ( ) 1.89 Negeri Sembilan 3.00 ( ) ( ) ( ) ( ) 0.67 Melaka 5.00 ( ) ( ) ( ) ( ) 1.56 Johor 4.00 ( ) ( ) ( ) ( ) 0.89 Pahang 2.50 ( ) ( ) ( ) ( ) 0.78 Sabah 3.00 ( ) ( ) ( ) ( ) 0.56 Sarawak 3.00 ( ) ( ) ( ) ( ) 0.89 Total mean (±SE) 3.55 ± ± ± ± CL = confidence limit.

3 3 Table 3. Percentages of knockdown and mortality of Malaysian Aedes albopictus adults against metofluthrin (0.01%), d-allethrin (0.20%), d-trans allethrin (0.15%), and prallethrin (0.04%) Location Metofluthrin (0.01%) d-allethrin (0.20%) d-trans allethrin (0.15%) Prallethrin (0.04%) Reference ± ± ± ± ± ± ± ± Penang ± ± 0.00 S ± ± R ± ± R ± ± 3.89 R Perak ± ± 0.00 S ± ± 3.33 M ± ± 2.89 M ± ± R Selangor ± ± 0.00 S ± ± M ± ± R ± ± R 7.50 Kuala ± ± 4.41 M ± ± 3.33 R ± ± R ± ± 1.67 R Lumpur Negeri Sembilan ± ± 0.00 S ± ± 1.67 M ± ± 3.33 M ± ± 5.77 R Melaka ± ± 4.41 M ± ± 4.41 R ± ± 2.89 R ± ± 2.50 R Johor ± ± 1.67 M ± ± R ± ± R ± ± R Pahang ± ± 0.00 S ± ± 0.00 M ± ± 0.00 S ± ± 0.00 R Sabah ± ± 1.67 S ± ± 2.87 M ± ± 1.67 S ± ± 2.50 R Sarawak ± ± 1.67 S ± ± 1.67 R ± ± 3.33 R ± ± 2.89 R P = F = df = 9,24 x 2 = P = F = df = 9,24 x 2 = F = x 2 = P = F = x 2 = F = x 2 = P = F = df = 9,22 x 2 = F = df = 9,22 x 2 = R = resistant (mortality <80%), S = susceptible (mortality >98%), and M = moderate resistance (mortality 80 98%) as determined by WHO (2009).

4 4 the presence of cross-resistance (Bisset et al. 1997). The mortality rate at 24-h posttreatment was used to assess the susceptibility status of the mosquitoes, where % indicates susceptible, 80 97% indicates possible development of resistance, and <80% indicates resistance (WHO 2009). Results and Discussion The knockdown rate and RR of Malaysian Ae. albopictus against metofluthrin, d-allethrin, d-trans allethrin, and prallethrin are presented in Table 2. Across all study sites, Ae. albopictus exhibited rapid knockdown toward metofluthrin, with KT 50 and RR values ranging from 2.50 to 5.00 min and 1.00 to 2.00, respectively. The mean knockdown time for the active ingredients against Ae. albopictus in decreasing order was prallethrin > d-allethrin > d-trans allethrin > metofluthrin. All tested Ae. albopictus displayed RR values <5, suggesting the populations were susceptible or had low resistance against the coils. This might be because Ae. albopictus prefers vegetation, and feeds and rests outdoors, thus the chances to be contacted with household insecticides are lower (Chen et al. 2005, Ponlawat et al. 2005). Aedes albopictus from the national capital of Malaysia, Kuala Lumpur, showed significantly higher (P < 0.05) knockdown time (KT 50 ) against metofluthrin, d-trans allethrin, and prallethrin compared to other regions. Originally, Ae. albopictus is an exophilic species dominating the suburban and rural zones because of its preferred habitats. However, due to rapid urbanization, both urban and rural areas have overlapped. It is now common to observe Ae. albopictus inhabiting urban zones such as Kuala Lumpur (Jirakanjanakit et al. 2007, Saleeza et al. 2011, Rozilawati et al. 2015). Hence, Ae. albopictus is likely to be exposed to insecticides especially in dengue endemic regions where insecticides have been applied extensively, such as space spraying and the uses of household insecticides. Additionally, pyrethroids are widely used as active ingredients for mosquito control in Malaysia (Lee et al. 2003) and were introduced in fogging activities in 1996 (Nazni et al. 1998). Furthermore, dengue cases are endemic and frequently reported in Kuala Lumpur (Low et al. 2013a). Hence, resulting in selection pressure toward Ae. albopictus in Kuala Lumpur. The percentages of knockdown and mortality of Malaysian Ae. albopictus against mosquito coils are shown in Table 3. In total, 70.00, 80.00, and 30.00% of Ae. albopictus populations were completely knocked down after exposures to d-allethrin, d-trans allethrin, and prallethrin, respectively. Full knockdown was observed for all Ae. albopictus strains against metofluthrin and exhibited mortality rates of >80% at 24-h posttreatment, of which 50% of the populations had complete mortality (100%). The populations tested were least susceptible to prallethrin with mortality rates ranging from 5.00 to 77.50%. Interestingly, most of the populations exhibited higher mortality rates than that of the reference strain, suggesting the wild strains were in fact more susceptible to certain active ingredients, compared to the reference strain which has been colonized in the laboratory for 64 generations. In agreement with its knockdown property, pyrethroid only exerts knockdown effect, as reflected in the percentages of knockdown in this study. The killing action may be just an additional effect which is usually inconsistent based on the extent of exposure of mosquitoes to the pyrethroid. The complexities of the underlying mechanisms toward pyrethroids in both reference and wild strains deserve additional research efforts. The effectiveness of metofluthrin against Aedes and Culex mosquitoes has been discussed in earlier studies (Argueta et al. 2004, Kawada et al. 2005, Rapley et al. 2009, Chin et al. 2017). Metofluthrin can induce rapid knockdown and high mortality rates in mosquitoes because of its high vapor pressure, which is 25 times greater than d-allethrin. Metofluthrin is also more stable compared with d-allethrin and prallethrin under field conditions, and it works in both heated and nonheated formulations (Ujihara et al. 2004, 2008; Sugano and Ishiwatari 2011). Spearman rank-order correlation displayed significant correlations between KT 50 of metofluthrin and d-allethrin (r = 0.758, P = 0.011), metofluthrin and prallethrin (r = 0.676, P = 0.032), d-allethrin and d-trans allethrin (r = 0.832, P = 0.003), d-allethrin and prallethrin (r = 0.921, ), and d-trans allethrin with prallethrin (r = 0.941, ) in Ae. albopictus, suggesting some levels of cross-resistance within the pyrethroid insecticides, possibly because of the similar mode of action or target sites. In addition, Ae. albopictus is also likely to be exposed to agrochemicals applied on vegetations and agricultural sites which was believed to result in cross-resistance (Ponlawat et al. 2005, Khan et al. 2011). The use of organochloride insecticide can be traced back to 1967 when DDT was used for malaria control but was stopped in Malaysia in 1998, and replaced by permethrin and deltamethrin (Low et al. 2013b). Both pyrethroid and organochlorine insecticides share the same mode of action which targets the voltage-gated sodium channel of insects (Hemingway and Ranson 2000), may take a role in contributing cross-resistance. In summary, metofluthrin coil offers some degree of protection and can induce rapid knockdown and high mortality (>80%) against Ae. albopictus across all studied populations. In comparison with other tested active ingredients, metofluthrin has shown promising insecticidal activity against Ae. albopictus. 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