Insecticide Resistance Status of Malaria Vectors in a Malarious Area, Southeast of Iran http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... Original Article Insecticide Resistance Status of Malaria Vectors in a Malarious Area, Southeast of Iran Jalil Nejati 1,2; Seyed Hassan Moosa-Kazemi2; Mohammad Ali Oshaghi2; Abdollah Badzohre2; Masoumeh Pirmohammadi2; Zahra Saeidi2; Nazanin Naseri- Karimi2; Seyedeh Zahra Parkhideh2; *Hassan Vatandoost2,3 1 Health Promotion Research Center, Zahedan University of Medical Sciences, Zahedan, Iran 2 Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 3 Department of Environmental Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran University of Medical Sciences, Tehran, Iran *Corresponding author: Prof Hassan Vatandoost, E-mail: hvatandoost1@yahoo.com, vatando@tums.ac.ir (Received 23 Jun 2020; accepted 30 Mar 2021) Copyright © 2021 The Authors. Published by Tehran University of Medical Sciences.Copyright © 2021 The Authors. Published by Tehran University of Medical Sciences. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/ by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited.by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. Abstract Background: Malaria continues to be the main vector-borne disease in Iran. The endemic foci of malaria are in Sistan and Baluchistan Province, the borderline of Iran and Pakistan. By the year 2020 the program of the country is malaria elimination. The main vector control is using insecti- cide as Indoor Residual Spraying. The aim of the study was to evaluate the susceptibility of main malaria vectors to different insecticides recommended by WHO. Methods: All the insecticides papers supported by WHO and evaluation of insecticide resis- tance of Anopheles stephensi, Anopheles culicifacies, Anopheles superpictus to different chemi- cal groups of imagicides including DDT 4%, malathion 5%, propoxur 01.%, lambdacyhalothrin 0.05%, deltamethrin 0.025% and permethrin 0.75% were followed by the WHO guideline. Results: Results of the susceptibility test against different insecticides revealed that An. stephensi and An. culicifacies are resistant to DDT and susceptible to other insecticides. An. superpictus is susceptible to all groups of pesticides. Conclusion: Knowledge on insecticide resistance in target species is a basic requirement to guide insecticide use in malaria control programmes in local and global scales. Keywords: Anopheles stephensi; Anopheles culicifacies; Anopheles superpictus; Resistant; Pesticides Introduction Malaria is the main vector borne diseases worldwide. According to the recent record of the World Health Organization, a total of 228 million cases have been reported in 2018 mainly in the African region (1). According to the report of the Ministry of Health of Iran, less than 89 locally- transmitted cases have been report ed in 2017. The aim of country is to eliminate the disease by 2025 (2). The campaign against malaria vectors started with organochlorines (DDT, dieldrin and BHC) during the 1960’s, followed by organophosphates (malathion and pirimiphos-methyl) for 2 decades from 1966 and continued with the carbamate, propoxur during 1977–1990, and then with pyrethroids including lambdacyhalothrin and Deltame thrin. Temephos, Reldan and pirimiphos-methyl was used for larviciding. The last checklist of Iranian mosquitoes 279 http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... shows 31 Anopheles species including sibling, biological forms and genotypes, 17 out of them are re ported as malaria vector transmission. These vectors are considered as sibling, genotype and type forms. Anopheles stephensi, An. cu licifacies, An. fluviatilis, An. dthali are the main vector species of south-eastern foci, while An. sacharovi and An. maculipennis are included in malaria transmission in northwest focus. Anopheles superpictus has wide distri bution in all malaria foci of the country (Fig. 1). Anopheles stephensi is reported from the Indi an subcontinent It is also distributed across the Middle East and South Asia region, exist ing in countries such as: Afghanistan, Bah rain, Bangladesh, China, Egypt, India, Iran, Iraq, Oman, Pakistan, Saudi Arabia, and Thai land (3, 4). It is also reported from Djibouti and Ethiopia (5, 6). Anopheles culicifacies reported from Afghanistan, Bahrain, Cambo dia, China, Eritrea, Ethiopia, India, Iran, Iraq, Laos, Myanmar (Burma), Nepal, Oman, Paki stan, Sri Lanka, Thailand, Vietnam, Yemen. It has five sibling species as A, B, C, D, and E. Anopheles superpictus is a main malaria vec tor in Palearctic region, Middle Eastern coun tries, northern Africa, India, Afghanistan, Pa kistan, central and southern Europe, and Russia (7). Insecticide resistance is the selection of a heritable trait in an insect population that re sults in an insect-control product no longer performing as intended. Establishing the base line of insecticide resistance and conducting a comprehensive situation analysis is the start- ing point for tracking resistance. This will re quire collecting available background data and, if necessary, conducting additional tests on vector susceptibility and on resistance mechanisms. Interpretation of the data must take into account the resistance situation in neighbouring countries as well as previous experience elsewhere with the same type of resistance mechanisms. Countries should de- sign a monitoring plan that includes data on vector distribution and relevant vector attrib- utes for transmission and control. Investiga- tion on susceptibility/resistance to currently used insecticides, and on the quality of vector control interventions. Experience suggests that if nothing is done, resistance will stabilize in the vector population and reversal will be difficult or even impossible, so that, some of the most effective insecticides will no longer be usable. Materials and Methods Study area The study was carried out in Sarbaz City, Sistan and Baluchistan Province, borderline of Iran and Pakistan (Fig. 2). Mosquito collection Mosquitoes were collected in the breeding places by a dipper equipment. The larvea were ternsferred to the insectary to become adults. Mosquito identification All the adutls females were identified using valuable key identification (8). Insecticide papers resource All the insecticides papers were supported by WHO. Insecticide susceptibility tests Aduls suceptibiity tests were carried out accordig to the WHO guideline. Susceptible when mortality is 98% or higher, possible re sistant when mortality is between 97 and 90%, and resistant when the mortality is lower than 90%. An excel sheet was created for in secticide resistance based on the applied in secticide at diagnostic dosage recommended by WHO. Statistical analysis The mortality quantities of 50% and 90% of imagicides (LT50 and LT90) and the level of confidence of 95%, the equation of the regres sion line were estimated using a regression probit analysis as described by Finney (1971) (9). When the mortality of the control group is less than 5%, then the data of biometric tests have not been corrected, but if the mortality of the control group is between 5% and 20%, they have to https://en.wikipedia.org/wiki/Afghanistan https://en.wikipedia.org/wiki/Bahrain https://en.wikipedia.org/wiki/Bangladesh https://en.wikipedia.org/wiki/China https://en.wikipedia.org/wiki/Egypt https://en.wikipedia.org/wiki/India https://en.wikipedia.org/wiki/Iran https://en.wikipedia.org/wiki/Iraq https://en.wikipedia.org/wiki/Oman https://en.wikipedia.org/wiki/Pakistan https://en.wikipedia.org/wiki/Saudi_Arabia https://en.wikipedia.org/wiki/Thailand https://en.wikipedia.org/wiki/Djibouti 280 http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... be corrected. The percentage mortality was calculated using Abbot’s for mula (1925) (10). Results Results of exposure of An. stephensi to different logarimic time of pesticides is shown in Table 1. Probit regression line is shown in Fig. 3. The results of the susceptibility test at diagnosctic dose are shown in Fig. 4. The order of LT50 value is DDT> Propoxur>Malathion >Bendiocarb>deltamethrin. Mortality at dignostic dose considering mortality less than 90% revealed that An. stephensi is resistant to DDT and suscpetible to other insecticides. Results of exposure of An. Table 1. Parameters of probit regression lines of Anopheles stephensi exposed to different insecticides Y=A+BX P χ2 (df) LT90 LT50 B±SE A Insecticide Y=-10.2229+2.9472X >0.05 5.747 (2) 8008.1993 2942.2500 2.94 ±0.309 -10.22 DDT Y=-9.5860+3.1479X >0.05 1.174 (2) 2833.6861 1109.7414 3.1 ±0.287 -9.58 Malathion Y=-11.3137+3.6761X <0.05 2.307 (2) 2668.2999 1195.6603 3.67 ±0.324 -11.31 Propoxur Y=-10.8544+3.6683X <0.05 0.634 (2) 2033.9448 909.8464 3.66 ±0.313 -10.85 Deltamethrin Y=-13.8762+4.6409X <0.05 0.401 (2) 1845.5122 977.1575 4.6 ±0.410 -13.87 Bendiocarb A= (interceptor), B±SE (Slope± standard error), LT50 (lethal time cause 50% mortality according to seconds), LT90 (lethal time cause 90% mortality according to seconds) Table 1. Parameters of probit regression lines of Anopheles stephensi exposed to different insecticides Table 2. Parameters of probit regression lines of Anopheles culicifacies exposed to different insecticides Y=A+BX P χ2 (df) LT90 LT50 B±SE A Insecticide Y=-13.4202+4.2917X >0.05 0.902 (2) 2664.5821 1339.7000 4.3 ±0.362 -13.42 DDT Y=-11.0527+3.6346X >0.05 0.002 (2) 2475.2129 1099.0019 3.6 ±0.325 -11.05 Malathion Y=-12.1599+3.8937X >0.05 1.419 (2) 2832.0720 1327.2653 3.9 ±0.336 -12.15 Propoxur Y=-11.8132+3.9346X >0.05 1.912 (2) 2128.8572 1005.5845 3.9 ±0.333 -11.81 Deltamethrin Y=-12.1914+4.0442X >0.05 1.635 (2) 2145.1592 1034.0933 4.0 ±0.358 -12.19 Bendiocarb Table 2. Parameters of probit regression lines of Anopheles culicifacies exposed to different insecticides Fig. 1. Spatial distribution of malaria vectors in Iran Fig. 1. Spatial distribution of malaria vectors in Iran 281 http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... culicifacies to different logarimic time of pesticides are shown in Table 2. Probit regression line is shown in Fig. 5. The results of susceptibility test at diagnosctic dose are shown in Fig. 6. The order of LT50 value is DDT> Propoxur>Malathion >Bendiocarb>deltamethrin. Mortality at dignostic dose considering mortality less than 90% revealed that An. culicifacies is suscpetible to all insecticides. Results of Table 3. Parameters of probit regression lines of Anopheles superpictus exposed to different insecticides Y=A+BX P χ2 (df) LT90 LT50 B±SE A Insecticide Y=-11.8709+3.3259 X <0.05 7.837 (2) 9007.5451 3709.0662 3.3±0.874 -11.87 DDT Y=-10.5072+3.4735X >0.05 3.980 (2) 2476.6908 1059.0387 3.4±0.444 -10.50 Malathion Y=-13.3080+4.2832X >0.05 3.360 (2) 2548.2910 1279.4752 4.2±0.489 -13.30 Propoxur Y=-11.8821+4.0435X >0.05 2.307 (2) 1801.2125 868.1769 4.0±0.371 -11.88 Deltamethrin Y=-11.5871+3.9542X >0.05 4.225 (2) 1796.5675 851.7902 3.9±0.380 -11.58 Lambdacyhalothrin Y=-12.4960+3.9622X <0.05 8.819 (2) 3000.9704 1424.9688 3.9±0.726 -12.49 Permethrin Table 3. Parameters of probit regression lines of Anopheles superpictus exposed to different insecticides Fig. 2. Map of study area, Sistan and Baluchistan Province, Iran Fig. 2. Map of study area, Sistan and Baluchistan Province, Iran Fig. 3. Probit regression line of Anopheles stephensi exposed to different insecticides Fig. 3. Probit regression line of Anopheles stephensi exposed to different insecticides 282 http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... exposure of An. superpictus to different logarimic time of pesticides are shown in Table 3. The results of susceptibility test at diagnosctic dose are shown in Fig. 7. The order of LT50 value is DDT> Propoxur >Malathion> Permetrhin> Deltamethrin> lamabdacyhalothrin. Mortality at dignostic dose considering mortality less than 90% revealed that An. superpictus is resistsnt to DDT and suscpetible to all insecticides. Fig. 4. Resistance of Anopheles stephensi to different insecticides at diagnostic doses Fig. 4. Resistance of Anopheles stephensi to different insecticides at diagnostic doses Fig. 5. Probit regression line of Anopheles culicifacies exposed to different insecticides Fig. 5. Probit regression line of Anopheles culicifacies exposed to different insecticides 283 http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... Discussion Results of susceptibility tests against dif- ferent WHO recommended insecticides, in cluding DDT, Malathion, Propoxur, Bendio carb, Del tamethrin, Lambdacyhalothrin and Per methrin against An. stephensi, An. culicifa cies and An. superpictus revealed that only An. superpictus is susceptible to all insecticides. However, An. stephensi and An. culicifacies showed re sistant to DDT. There are several reports on resistant status of malaria vectors including An. stephensi (11- 17). Anopheles ste phensi showed resistance to lambdacyhalo thrin, del tamethrin, permethrin, and bendio carb in Bandar Abbas County, southern Iran (17). Anopheles stephensi samples were re sistant bendiocarb, Fig. 6. Resistance of Anopheles culicifacies to different insecticides at diagnostic doses Fig. 6. Resistance of Anopheles culicifacies to different insecticides at diagnostic doses Fig. 7. Resistance of Anopheles superpictus to different insecticides at diagnostic dose Fig. 7. Resistance of Anopheles superpictus to different insecticides at diagnostic dose 284 http://jad.tums.ac.ir Published Online: Sep 30, 2021 J Arthropod-Borne Dis, Sep 2021, 15(3): 278–286 J Nejati et al.: Insecticide Resistance... propoxur, deltamethrin, per me thrin, DDT, malathion and pirimiphos-me thyl in Somali region (18). Resistant to DDT, mal athion, bendiocarb, permethrin and del tame thrin was reported in An. stephensi and An. culicifacies from Afghanistan. Resistant to only deltamethrin and bendiocarb was observed in An. superpictus (19). There are also report of resistant to pyrethroids in Afghanistan (20). Anopheles superpictus populations were con firmed resistant to DDT, malathion and propoxur and susceptible to pyrethroid insec ticides in different parts of Turkey (21). Anopheles cu licifacies was resistant to orga nochlorine in secticides and tolerant to carba mates insecti cides and susceptible to other insecticides (22). Insecticide resistance in An. culicifacies was reported (23-24). In order to suggest pyre thrpids for malaria vector control addition studies is necessary to find the mechanisms of resistant to DDT and cross-resistant to pyre throids. According to the re sults of Gorouhi et al. (2018) (25), metabolic mechanisms play a crucial role in the development of DDT and cyfluthrin resistance in An. stephensi. Global results showed a wide variety of susceptibil- ity/resistance status of malaria vectors to these chemicals according to the loca- tion, historical context of pesticide used, ge netic background of vectors, age and ab- dominal conditions of adults, use of pesti- cides for agricultural pest control may play important role in the sus ceptibility status of these species to different insecticides (26- 32). Conclusion The results of this study are providing a guideline for the country to manage their vector control activities against insecticide resistance of malaria vectors and provide novel ap proaches. Acknowledgments This research is financially supported by the Ministry of Health and Medical Education National Institute for Medical Research Devel opment. The au thors declare that they have no competing in terests. References 1. World Health Organization (2019) The E-2020 initiative of 21 malaria-eliminating countries: progress report. p. 16. 2. 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Pathog Glob Health. 111(6):289-296. 32. Soltani A, Vatandoost H, Oshaghi MA, Enaya- ti AA, Raeisi A, Eshraghian MR, Soltan- Dallal MM, Hanafi-Bojd AA, Abai MR, Rafi F (2013) Baseline susceptibility of different geographical strains of Anopheles stephensi (Diptera: Cu- licidae) to Temephos in malarious areas of Iran. J Arthropod Borne Dis. 7(1):56-65. https://pubmed.ncbi.nlm.nih.gov/28745553/?from_term=oshaghi%2Banopheles&from_pos=9 https://pubmed.ncbi.nlm.nih.gov/?term=Soltani%2BA&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Vatandoost%2BH&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Enayati%2BAA&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Enayati%2BAA&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Raeisi%2BA&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Eshraghian%2BMR&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Soltan-Dallal%2BMM&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Soltan-Dallal%2BMM&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Hanafi-Bojd%2BAA&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Abai%2BMR&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/?term=Rafi%2BF&cauthor_id=23785695 https://pubmed.ncbi.nlm.nih.gov/23785695/?from_term=oshaghi%2Banopheles&from_page=3&from_pos=4 https://pubmed.ncbi.nlm.nih.gov/23785695/?from_term=oshaghi%2Banopheles&from_page=3&from_pos=4 https://pubmed.ncbi.nlm.nih.gov/23785695/?from_term=oshaghi%2Banopheles&from_page=3&from_pos=4 https://pubmed.ncbi.nlm.nih.gov/23785695/?from_term=oshaghi%2Banopheles&from_page=3&from_pos=4 https://pubmed.ncbi.nlm.nih.gov/23785695/?from_term=oshaghi%2Banopheles&from_page=3&from_pos=4 https://pubmed.ncbi.nlm.nih.gov/23785695/?from_term=oshaghi%2Banopheles&from_page=3&from_pos=4 Insecticide Resistance Status of Malaria Vectors in a Malarious Area, Southeast of Iran Abstract Keywords Introduction Materials and Methods Study area Mosquito identifications Insecticide papers resource Insecticide susceptibility tests Statistical analysis Discussion Conclusion Acknowledgments References