J Arthropod-Borne Dis, December 2019, 13(4): 407–415 T Hazratian et al.: Baseline Susceptibility of … 407 http://jad.tums.ac.ir Published Online: December 31, 2019 Original Article Baseline Susceptibility of Culiseta longiareolata (Diptera: Culicidae) to Different Imagicides, in Eastern Azerbaijan, Iran Teimour Hazratian1; Azim Paksa1; Mohammad Mahdi Sedaghat2; Hassan Vatandoost2,3; Seyed Hassan Moosa-Kazemi2; Alireza Sanei-Dehkordi4,5; Yaser Salim-Abadi6; Masoumeh Pirmohammadi2; Saideh Yousefi2; Masoumeh Amin2; *Mohammad Ali Oshaghi2 1Departmemt of Parasitology, Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 3Department of Environmental Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, 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 Health Services and Health Promotion, School of Health, Rafsanjan University of Medical Sciences, Rafsanjan, Iran (Received 25 Oct 2019; accepted 30 Dec 2019) Abstract Background: Culiseta longiareolata is an important vector for many human diseases such as brucellosis, avian influen- za and West Nile encephalitis. It is likely an intermediate host of avian Plasmodium that can transmit Malta fever. The aim of this study was to determine the susceptibility level of Cs. longiareolata to different classes of imagicides which are recommended by World Health Organization . Methods: Larval stages of the Cs. longiareolata were collected from their natural habitats in Marand County at East Azerbaijan Province, northwestern of Iran in 2017. Adult susceptibility test were carried out with using impregnated papers to insecticides including DDT 4%, Cyfluthrin 0.15%, Deltamethrin 0.05%, Propoxur 0.1% and Fenitrothion 1% by standard test kits. Results: Results showed that Cs. longiareolata adult is more susceptible to pyrethroid and carbamate insecticides. Among tested insecticides, Cyfluthrin was the most toxic against Cs. longiareolata with LT50 value of 11.53 minutes and Fenitrothion had the least toxic effect (LT50: 63.39 min). Conclusions: This study provided a guideline for monitoring and evaluation of insecticide susceptibility tests against Cs. longiareolata mosquitoes for further decision making. Keywords: Baseline susceptibility; Culiseta longiareolata; Insecticides Introduction Mosquitoes transmit many important human diseases such as malaria, filariasis, several types of encephalitis, many arboviral diseases and al- so cause serious nuisance and irritation (1-5). West Nile virus has been detected in 62 mos- quito species, including genera of Aedes, Anoph- eles, Culiseta and Culex in the United State of America (6-9). About 3500 species of mosqui- toes reported worldwide, and approximately 64 of those can be found in Iran (10-17). Culiseta longiareolata is a vector for brucellosis, avian influenza and West Nile encephalitis. These mosquitoes are likely an intermediate host of avian Plasmodium and can transmit Malta fe- ver (18, 19). The mosquito Cs. longiareolata is a common and abundant species in many countries of Europe, Africa and also Asia, such as Iran, Albania, Azores, Botswana, Bulgaria, Canary islands, Croatia, Cyprus, Djibouti, Egypt, southern England, Ethiopia, France, Greece, *Corresponding author: Dr Mohammad Ali Oshaghi, E-mail: moshaghi@sina.tums.ac.ir http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 407–415 T Hazratian et al.: Baseline Susceptibility of … 408 http://jad.tums.ac.ir Published Online: December 31, 2019 Hungary, India, Iraq, Italy, Jordan, Lebanon, Lesotho, Madeira, Mauritania, Morocco, Na- mibia, Pakistan, Portugal, Romania, Russia, Slovakia, Somalia, South Africa, Spain, Sudan, Switzerland, Syria, Tajikistan, Tunisia, Tur- key, Ukraine and Yemen (1). Eggs and larvae of Cs. Longiareolata is found mostly in tires, so it can be spread across the world through tire trading (20). Culiseta longiareolata is found common in human habitations. The lar- vae are rarely found in natural waters that are found mostly in temporary pools, rock pools, artificial containers, wooden and metal barrels and tanks built of concrete, which are rich in decaying organic materials (18). Early growth stages larvae of Cs. longiareolata are more found in shallow areas of pools, whereas late growth stages are found deeper areas of the pools (21). Chemical insecticides such as organophos- phates, organochlorine, carbamate, and pyre- throid are principal weapon against both adult and larval stages of mosquitoes vectors (22- 24). Increasing and inappropriate use of syn- thetic insecticides in mosquito control in par- allel to pest control agriculture is one of the main causes of increased tolerance and resistance in different species of mosquitoes across the world (25-27). According to reports in recent years, the level of tolerance and resistance of some mosquitoes and other arthropods has increased in some parts of the world which is a major barrier to the success of vector control programs (28-34). In our knowledge, there was no com- prehensive study on monitoring the suscepti- bility level of Cs. longiareolata to various in- secticides in the world. The aim of this study was to evaluate the susceptibility of Cs. longi- areolata to five common insecticides recom- mended by World Health Organization. Materials and Methods Study area This study was carried out in Marand Coun- ty in East Azerbaijan Province, northwestern of Iran. The county located at latitude 38°42'N, lon- gitude 45°76'E and altitude 1342 Meter (Fig. 1). Bioassay procedure In this experimental study larval stage of Cs. longiareolata were collected from larval habi- tats, then all specimens were transferred to in- sectary of Department of Medical Entomology and Vector Control with 27±1 °C temperature, 12:12 light and dark period and 60±5% of rel- ative humidity. Adult susceptibility test of mos- quitoes were carried out using standard im- pregnated papers insecticides such as DDT 4%, Cyfluthrin 0.15%, Deltamethrin 0.05%, Propoxur 0.1% and Fenitrothion 1%. Accord- ing to the standard procedures recommended by the World Health Organization (WHO). In brief, twenty-five unfed female mosquitoes were exposed to insecticide-impregnated papers at dif- ferent exposure interval times, moreover for each different exposure time 4 replicates of mos- quitos were used and 2 replicates of 25 adult mosquitoes were considered as controls with untreated papers. Probit analysis was conducted on mortality data collected after 24 hours exposure to dif- ferent times of insecticides using Finney’s sta- tistical method to determine the lethal time caus- ing for 50% and 90% mortality (LT50 and LT90) values and their 95% confidence limit of up- per and lower confidence levels (35-37). The percentage mortality was calculated and cor- rections for mortality when necessary were done by Abbot’s formula (38). According to the WHO criteria, the susceptibility level of the mosque- itoes was considered in three classes as suscep- tible, tolerant and resistant. The mortality be- tween 98–100% was considered as suscepti- ble, less than 90% demonstrated resistance and between 90–97% was determined as resistance candidate (36, 39, 40). Results Table 1 and 2 show the probit regression line parameters for females of Cs. longiareolata to http://jad.tums.ac.ir/ https://www.google.com/search?q=organochlorine&spell=1&sa=X&ved=0ahUKEwjvi7GamrnaAhVS3qQKHfWID4AQBQghKAA https://www.google.com/search?q=carbamate&spell=1&sa=X&ved=0ahUKEwibwPm9mrnaAhXSCuwKHZTOCEYQBQghKAA https://www.google.com/search?q=pyrethroid&spell=1&sa=X&ved=0ahUKEwiF7PfPmrnaAhUQMewKHVCdBIMQBQghKAA https://www.google.com/search?q=pyrethroid&spell=1&sa=X&ved=0ahUKEwiF7PfPmrnaAhUQMewKHVCdBIMQBQghKAA J Arthropod-Borne Dis, December 2019, 13(4): 407–415 T Hazratian et al.: Baseline Susceptibility of … 409 http://jad.tums.ac.ir Published Online: December 31, 2019 different insecticides. In addition, Probit re- gression lines of insecticides against adult of Cs. longiareolata were drown which showed a linear relationship between mortality and time (Fig. 2). The LT50 values were 52.38, 28.79, 11.53, 63.39 and 28.05min after treatment with DDT 4%, deltamethrin 0.05%, cyfluthrin 0.15%, fenitrothion 1% and propoxur 0.1%, respec- tively (Fig. 3). The highest toxicity against Cs. longiareolata was found on cyfluthrin (LT50: 11.53 and LT90: 43.37min) while the lowest toxicity was observed for fenitrothion 1% (LT50: 63.39 and LT90: 183.26min) (Table 1). Table 1. The Parameters of probit regression line of five insecticides on Culisita longiareolata in Marand County at East Azerbaijan Province, northwestern of Iran, 2017 Insecticide Name A B±SE LT50 , (LCL-UCL) 95% C.I. LT90, (LCL-UCL) 95% C.I. X2 (df) P value Cyfluthrin -2.37 2.23±0.27 9.18 32.05 4.36 (3) > 0.05 11.53 43.37 14.27 68.03 DDT -4.41 2.57±0.32 43.35 125.78 5.8 (3) > 0.05 52.38 165.47 63.02 250.91 Deltamethrin -3.67 2.53±0.30 23.72 70.17 6.46 (3) > 0.05 28.79 92.24 34.8 138.22 Fenitrothion -5.01 2.78±0.34 53.26 140.51 2.39 (3) > 0.05 63.39 183.26 75.85 274.31 Propoxur -5.85 4.04±0.46 24.19 48.64 2.81 (3) > 0.05 28.05 58.2 32.36 74.68 A= y-intercept, B= the slope of the line, SE= Standard error LT50, 95% CI= Lethal Time causing 50% mortality and its 95% confidence interval LT90, 95% CI= Lethal Time causing 90% mortality and its 95% confidence interval LCL: Lower Confidence Limit, UCL: Upper Confidence Limit X2= Heterogeneity about the regression line df= degree of freedom, p= Represent heterogeneity in the population of tested Table 2. Susceptibility level of Culisita longiareolata exposed to different groups of insecticides at diagnostic dose in Marand County at East Azerbaijan Province, northwestern of Iran, 2017 Insecticides MR±EB* Resistance status** Cyfluthrin 95±0.25 RC DDT 42.5±0.25 R Deltamethrin 70±0.41 R Fenitrothion 37.5±0.48 R Propoxur 87.5±0.48 R *Mortality Rate±Error Bar **RC: Resistance Candidate ***R: Resistance http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 407–415 T Hazratian et al.: Baseline Susceptibility of … 410 http://jad.tums.ac.ir Published Online: December 31, 2019 Fig. 1. Map showing Iran, highlighting the location of East Azerbaijan Province and Marand County Fig. 2. Regression lines of Culiseta longiareolata exposed to different group of insecticides in Marand County at East Azerbaijan Province, northwestern of Iran, 2017 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 407–415 T Hazratian et al.: Baseline Susceptibility of … 411 http://jad.tums.ac.ir Published Online: December 31, 2019 Fig. 3. Lethal time causing 50% mortality of Culiseta longiareolata exposed to different group of insecticides in Ma- rand County at East Azerbaijan Province, northwestern of Iran, 2017 Discussion The excessive use of synthetic pesticides in agriculture plays an important role in the de- velopment of insecticide resistance in arthropods (41, 42). Resistance in medically important ar- thropods is developing and this is a major prob- lem in their control (43). Considering the current WHO criteria for in- secticide resistance evaluation, Cs. longiareolata is resistant to Fenitrothion, DDT, deltamethrin, propoxur and candidate of resistance to cyfluth- rin. Some studies showed that Cs. longiaerolata is resistance to DDT, propoxur, lambda-cyhalot- rin and tolerant to malathion and deltamethrin more over LT50 value found as 131.94, 5.21, 17.60, 5.19 and 29.12min for DDT, deltame- thrin, lambda-cyhalothrin, malathion and propoxur respectively (43). LT90 value of Cs. longiaerolata for DDT, deltamethrin, lambda- cyhalothrin, malathion and propoxur calculat- ed as 588.13, 29.24, 229.26, 26.69 and 371.76 minutes respectively(41). Our results based on probit regression line showed that adult of Cs. longiareolata is more suseceptible to pyrethroid and carbamate insecticides. LT50 value of this species for DDT, cyfluthrin, deltamethrin, fenitrothion and propoxur calculated as 52.28, 11.53, 28.79, 63.39 and 28.05 minutes respec- tively. LT90 value found as 165.47, 43.37, 92.27, 183.26 and 58.2 minutes for DDT, cyfluthrin, deltamethrin, fenitrothion and propoxur respec- tively. Previous studies reported that Cs. Longiare- olata larvae was susceptible to Bacillus sphaer- icus and B. thuringiensis (44). Some reports showed that the LC50 and LC90 values of No- valuron (Insect Growth Regular) against Cs. longiareolata were reported as 0.51–0.91μg/l and 2.32–4.30μg/l, respectively (45). In many regions of Iran, results of suscep- tibility test on Cx. pipiens, Cx. quinquefascia- tus, Anopheles stephensi, and Cs. longiareola- ta showed that high resistant to different clas- ses of insecticides, such as DDT, deltamethrin, lambda-cyhalo-thrin, propoxur and cyfluthrin and this finding is similar to our results for Cs. longiareolata (29-31, 41, 46, 47). http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 407–415 T Hazratian et al.: Baseline Susceptibility of … 412 http://jad.tums.ac.ir Published Online: December 31, 2019 The lack of data on mosquito susceptibility to insecticides is a limiting factor for the suc- cess of control programs. Therefore, this find- ing can be useful in future vector control pro- grams and investigations in order to prevent the development of resistance to insecticides. Due to the emergence of resistance in mos- quitoes to different classes of insecticides, the use of biological agents can be an effective method to control mosquitoes (42). However, the use of botanical insecticide, which have no adverse effects on the environment and humans, can be appropriate and an alternative control method for insecticide in vector control pro- grams (48-55). Conclusion This study confirms the resistance of the Cs. longiareolata to fenitrothion, DDT, deltamethrin, propoxur and candidate of resistance to cyfluth- rin. When we observed the high resistance level of Cs. longiareolata increases to the insecticides in the study area, therefore, in order to avoid increasing resistance to insecticides, appropri- ate and effective strategies should be used such as: use of regular monitoring of current insec- ticides resistance, interventions in combination, rotations of insecticides, mixtures insecticides and plant insecticides. 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