J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 453 http://jad.tums.ac.ir Published Online: December 30, 2017 Original Article Baseline Susceptibility of Filarial Vector Culex quinquefasciatus (Diptera: Culicidae) to Five Insecticides with Different Modes of Action in Southeast of Iran Yaser Salim-Abadi 1,2, Mohammad Asadpour 1, Iraj Sharifi 3, Alireza Sanei-Dehkordi 4,5, Mohammad Amin Gorouhi 6, Azim Paksa 7, Zohre Tayyebi 8, *Abbas Aghaei-Afshar 3 1Department of Health Services and Health Promotion, School of Health, Rafsanjan University of Medical Sciences, Rafsanjan, Iran 2Pistachio Safety Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran 3Leishmaniasis Research Center, Kerman University of Medical Sciences, Kerman, Iran 4Department of Medical Entomology and Vector Control, Faculty of Health, Hormozgan University of Medical Sciences, Bandar Abbas, Iran 5Infectious and Tropical Diseases Research Center, Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran 6Department of Medical Entomology and Vector Control, School of Health, Kerman University of Medi- cal Sciences, Kerman, Iran 7Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 8Student Research Committee, Rafsanjan University of Medical Sciences, Rafsanjan, Iran (Received 11 May 2017; accepted 19 Sep 2017) Abstract Background: Culex quinquefasciatus (Diptera: Culicidae) is an important vector for many human diseases. The aim of this study was to evaluate the susceptibility level of larval and adult stages of Cu. quinquefasciatus to different groups of WHO recommended insecticides for vector control. Methods: Larval stages of the Culex mosquitoes were collected from their natural habitats in Rafsanjan County at Kerman Province, southeast of Iran in 2016. Insecticide susceptibility status of adult female Cx. quinquefasciatus against DDT (4%), deltamethrin (0.05%), malathion 5%, and bendiocarb (0.1%) were determined using WHO stand- ard insecticide susceptibility test. Additional test was carried out to determine the susceptibility status of larvae of Cx. quinquefasciatus to temephos. Bioassay data were analyzed by Probit program. Results: Cx. quinquefasciatus adults showed resistance to all four groups of the tested insecticides according to the WHO criteria for resistance evaluation. The lethal concentrations for 50% mortality (LC50) and 90% mortality (LC90) of temephos against Cx. quinquefasciatus larvae were 0.18mg/l and 0.78mg/l, respectively. This finding also con- firms resistance to temephos based on the WHO recommended instructions for resistance evaluation. Conclusion: Resistance to all groups of the tested insecticides should be considered for future vector control investi- gations in the study area. Keywords: Susceptibility status, Resistance, Insecticide, Culex quinquefasciatus, Iran Introduction The southern house mosquito, Culex quin- quefasciatus (Diptera: Culicidae) is an im- portant vector for many human diseases. This species plays a crucial role in the transmis- sion of some important pathogen such as Wu- chereria bancrofti, Dirofilaria immitis, Plasmo- dium relictum, Sindbis virus, West Nile virus, Equine encephalitis, St Louis, Oropouche and Rift Valley fever which are today among the major public health problems worldwide (1–8). Wastewater and sewage system are im- portant breeding places for Culex mosquitoes. *Corresponding author: Dr Abbas Aghaei-Afshar, E-mail: afshara2@yahoo.com J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 454 http://jad.tums.ac.ir Published Online: December 30, 2017 Constant exposure of Cx. quinquefasciatus to the high organic content of wastewater in- cluding detergents, different groups of insec- ticides, industrial pollutants, and oil compounds can lead to the development of resistance in mosquito larvae against insecticides and lar- vicides (9–11). In recent years, increasing level of resistance to various groups of insec- ticides has been a major barrier to the suc- cess of vector control programs. Many stud- ies have reported high level of resistance in Cx. quinquefasciatus to many groups of in- secticides (12–14). Culex quinquefasciatus is an important member of Cx. pipiens com- plex wildly distributed worldwide (2, 5, 15). In Iran, the resistance status of Cx. pipiens complex against different groups of insecti- cides was indicated the development of re- sistance in the members of this species, in- cluding Cx. quinquefasciatus, during the past quarter-century: development of resistance to most of the organochlorine insecticides includ- ing DDT (Dichloro diphenyl trichloroethane) (6, 11, 16–20). Resistance to pyrethroid insec- ticides such as lambda-cyhalothrin, deltame- thrin, and cyfluthrin (6, 16, 17, 19). Resistance to the carbamate insecticides propoxur and ben- diocarb (11, 16, 17) and relative resistance to malathion organophosphates insecticides (11, 16). Moreover, resistance of the larvae of Cx. pipiens complex to temephos has recently been reported for the first time in Iran (9). There was no study on monitoring the susceptibility level of Cx. quinquefasciatus to insecticides in Rafsanjan County at Kerman Province, southeastern Iran. We aimed to de- termine the susceptibility status of Cx. quin- quefasciatus against insecticides in this area. Materials and Methods Study area This study was carried out in Rafsanjan County at Kerman Province, southeastern Iran. The county located at latitude 30°30'N and longitude 55°40'E, with a population of 300000 in 2015 (Fig. 1). Bioassay procedure Larvae of Cx. quinquefasciatus were col- lected from larval habitats in Rafsanjan Coun- ty in 2016, and all sample were transferred to laboratory and reared at 27 °C and 65±5% relative humidity using a 12h light/ 12h dark photoperiod. Bioassay tests were carried out using WHO test kits on adult mosquitoes (21). The following diagnostic concentrations of insecticides were tested: DDT 4%, lambda- cyhalothrin 0.05%, malathion 5%, and ben- diocarb 0.1%. Tests were carried out on3 to 5-day-old unfed females. Batches of 25 fe- males were exposed to insecticide-impregnated papers at different exposure times. Two rep- licates of 25 adult mosquitoes (3 to 5-day-old unfed females) were considered as controls with untreated papers for each different exposure time. The lethal time for 50% mortality and 90% mortality (LT50 and LT90) among the mos- quitoes was calculated using log-probit soft- ware according to Finney’s formula (22, 23). Larvicide susceptibility tests were carried out on late 3rd to early 4th stage larvae to determine larval susceptibility to temephos using WHO standard kit (1.25, 6.25, 31.25 and 156.25 mg/l concentrations), according to WHO instruc- tions (22, 23). Each test consisted of four rep- licates with 25 larvae each in glass beakers containing 250ml of distilled water and the specified insecticide concentration. Two rep- licates of 25 untreated larvae were maintained as controls. After 24h exposure period, lar- val mortality was calculated the lethal con- centrations for 50% mortality and 90% mor- tality (LC50 and LC90) were calculated by probit analysis (24). In both adult and larval susceptibility testing, mortality rate in the test samples was corrected using Abbott formula (25), when the mortality rate of control was between 5% and 20%. Results The mortality rate (MR) in adult Cx. quin- quefasciatus mosquitoes exposed to four dif- ferent groups of insecticide-impregnated pa- J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 455 http://jad.tums.ac.ir Published Online: December 30, 2017 pers are shown in Table 1 and 2. Lambda- cyhalothrin with LT50= 25 minute and LT90= 74min and DDT with LT50= 139min and LT90= 227min had the lowest and highest LT50 and LT90 values, respectively (Table 1). Culex quinquefasciatus is resistant to mal- athion and bendiocarb and candidate of re- sistance to lambda-cyhalothrin and DDT based on the criteria for insecticide resistance de- scribed by WHO (Table 2). The mortality rate in the mosquitoes at one-hour exposure to the insecticides calculated after 24h recovery pe- riod has been summarized in Table 2. Mala- thion had a mortality rate of 80% (MR= 80%), bendiocarb 88%, lambda-cyhalothrin and DDT 90% each, the mortality rate of DDT was cal- culated after 4h exposure time instead of 1h (Table 2). The regression line of different concentration is shown in Fig. 2. The mortality rate of each concentration of temephos is shown in Table 3. The mor- tality rate of temephos ranged from 3% to 100%. Moreover, using Finney’s method, we calculated LC50 and LC90 for Cx. quinque- fasciatus that were 0.18 and 0.78 ppm, re- spectively (Table 4). The regression line of the different concentrations of temephos is shown in Fig. 3. Table 1. Probit regression line parameters of Culex quinquefasciatus exposed to different groups of insecticides in Rafsanjan City, southeastern Iran, 2016 Insecticides A B ± SE LT50, 95% C.I. (Min) LT90, 95% C.I. (Min) X2 (df) p value Lambda- cyhalothrin 0.05% -3.80 2.72 ± 0.27 22 58 5.84(2) >0.05 25 74 29 102 Malathion 5% -3.89 2.55 ± 0.28 29 80 5.7 (2) >0.05 33 106 39 159 Bendiocarb 0.1% -3.90 2.72 ± 0.28 23 63 5.49 (2) >0.05 27 79 31 112 DDT 4% - 13.01 6.06 ± 0.55 129 204 3.04 (2) >0.05 139 227 172 260 A= y-intercept, B= the slope of the line, SE= standard error, CI= confidence interval, x2= heterogeneity about the regression line, df= degree of freedom, P> 0.05= represents no heterogeneity in the population of tested mosquitos. Table 2. Susceptibility level of Culex quinquefasciatus exposed to different groups of insecticides in Rafsanjan County, southeastern Iran, 2016 Insecticides MR ± EB* Resistance status** Lambda-cyhalothrin 0.05% 90 ± 2 RC Malathion 5% 80 ± 3 R Bendiocarb 0.1% 88 ± 3 R DDT 4%*** 90±2 RC *Mortality rate± errorbar **RC Resistance Candidate ***After 4 h exposure period J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 456 http://jad.tums.ac.ir Published Online: December 30, 2017 Fig. 1. The geographical location of Rafsanjan County in Kerman Province, Iran Fig. 2. Regression lines of Culex quinquefasciatus exposed to different group of insecticides in Rafsanjan City, Southeastern Iran, 2016 J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 457 http://jad.tums.ac.ir Published Online: December 30, 2017 Table 3. Mortality rate in Culex quinquefasciatus larvae at WHO standard concentrations of Temephos in Rafsan- jan County, Southeastern Iran, 2016 Concentration (ppm) Replicates No. of tested larvae No. of mortality Mortality rate (%) Observed mor- tality probit Expected mor- tality probit 0.005 4 100 3 3 3.119 1.762 0.025 4 100 6 6 3.445 3.199 0.125 4 100 10 10 3.718 4.636 0.625 4 100 100 100 7.576 6.073 Control 2 50 0 0 - - Table 4. Probit regression line parameters of Temephos against Culex quinquefasciatus larvae in Rafsanjan County, Southeastern Iran, 2016 A B LC50, 95% CI (ppm) LC90, 95% CI (ppm) X2 (df) P-value 1.49 2.05 0.18 0.78 190.76(2) <0.05 Fig. 3. Mortality Regression lines of different concentrations of Temephos against Culex quinquefasciatus in Raf- sanjan City, Southeastern Iran, 2016 Discussion The present study provides evidence of resistance to four different classes of insecti- cides according to the current WHO criteria for insecticide resistance evaluation. The mortality rate was interpreted as fol- lows: higher than 98% was considered as sus- ceptible, less than 90% indicated resistance, and from 90% to 97% was defined as re- sistance candidate. For the resistance candi- date category (90–97% mortality rate), addi- tional investigation is needed for the confir- mation of resistance (21). Although both lambda-cyhalothrin and DDT have mortality rate of 90% each which classifies them as J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 458 http://jad.tums.ac.ir Published Online: December 30, 2017 potential candidate for resistance according to the WHO criteria. This finding can be useful in future vector control programs and investigations in order to prevent the development of resistance to both insecticides. Previous studies have also reported Cx. pipiens resistance to different classes of in- secticides in different geographical regions of Iran, resistance to DDT, lambda-cyhalo- thrin, deltamethrin and cyfluthrin in Tehran, capital of Iran (6, 11, 20). Resistance to DDT in the North of Iran (18), resistance to DDT, lambda-cyhalothrin and propoxur in a diro- filariasis foci in the Northwest of Iran (18), resistance to DDT, propoxur, cyfluthrin and lambda-cyhalothrin and tolerance to deltame- thrin in a malaria endemic area in the South- eastern part of Iran (17), and resistance to del- tamethrin and DDT in the Northwestern part of Iran (19). The use of pesticides in agricultural sec- tor can lead to the development of resistance to insecticides in medically important vectors including Cx. quinquefasciatus (13, 26–28). There is a growing concern over the de- velopment of multiple insecticide resistance mechanisms in medically important arthro- pods that is a major problem in vector con- trol (15, 29–31). Over the last fifty years, resistance to insecticides has been a growing concern. Resistance of mosquitoes to DDT was first reported in 1949 (32, 33). Howev- er, resistance to organophosphorus insecti- cides in Cx. quinquefasciatus was first re- ported in 1961 (34), and to date, there have been several reports on resistance to various classes of insecticides in Cx. quinquefasciatus. This species is now quite resistant to some insecticides such as DDT and Malathion such that it does not exhibit mortality at one-hour exposure and 24h recovery period (35). In the present study, in addition to adult susceptibility test, susceptibility of the larvae of Cx. quinquefasciatus to Temephos was eval- uated according to WHO standard method. We observed mortality rate ranged between 3% and 100%. In another study, laboratory evaluation of the susceptibility of Anopheles stephensi larvae collected from Kazeroun, south of Iran and Cx. pipiens larvae collect- ed from Tehran, capital of Iran to temephos insecticides was carried out. LC50 values of both species were the same that is similar to our findings. Mosquito larvae in all the three geographical regions mentioned above have become resistant to temephos (9). In other countries were reported resistance of adult and larval stages of Cx. quinquefasciatus to different groups of insecticides and larvicides. In a study conducted in Morocco, bioassay re- sults showed that Cx. pipiens is resistant to temephos that is consistent with our results (36). In Kuala Lumpur (Malaysia), Cx. quin- quefasciatus larvae were found to be highly resistant to Malathion that was similar to the adults (35). In Central Tunisia, resistance to temephos in Cx. quinquefasciatus larvae have been reported (37) Moreover, resistance of Cx. quinquefasciatus larvae to malathion, per- methrin, and resmethrin has been reported in Florida (USA) (38). The use of pesticides in agriculture could play a role in the development of resistance to insecticides as well as larvicides in Cx. quinquefasciatus in Rafsanjan County (9, 11). Owing to the emergence of Cx. quinque- fasciatus resistance to different classes of insecticides and larvicides, using some bio- logical control agents such as Bacillus thu- ringiensis (a Gram-positive, soil-dwelling bacterium) and Gambusia affinis (larvivorous fish) can provide an efficient control strate- gy (39–41). Moreover, use of natural prod- ucts derived from some plants such as Buni- um persicum and Zhumeria majdae that have no adverse effects on the environment and humans can be suitable and alternative con- trol approach for larvae as well as adult Cx. quinquefasciatus mosquitos (42–46). https://en.wikipedia.org/wiki/Gram-positive https://en.wikipedia.org/wiki/Bacterium J Arthropod-Borne Dis, December 2017, 11(4): 453–462 Y Salim-Abadi et al.: Baseline Susceptibility of … 459 http://jad.tums.ac.ir Published Online: December 30, 2017 Conclusion Resistance to all tested insecticides was found. The high resistance status observed in the study area may be due to irregular use of pesticides in agriculture led to the constant exposure of the mosquito species to organic chemicals and subsequent development of re- sistance to insecticides and larvicides in Cx. quinquefasciatus. 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