Review Article ABSTRACT INTRODUCTION

J Vector Borne Dis 54, June 2017, pp. 111130 eview Article Temporo-spatial distribution of insecticide-resistance in Indian malaria vectors in the last quarter-century: Need for regular resistance monitoring and management Kamaraju aghavendra 1, Poonam harma Velamuri 1, Vaishali Verma 1, Natarajan Elamathi 1, Tapan Kumar Barik 1-2, ajendra Mohan Bhatt 3-4 & Aditya Prasad Dash 1,5 1 ICM-National Institute of Malaria esearch, New Delhi; 2 Department of Zoology, Berhampur University, Berhampur; 3 National Institute of Malaria esearch, Field Unit, LTI Campus, aipur; 4 Jal agar Apartment, College oad, Nadiad; 5 Central University of Tamil Nadu, Thiruvarur, India ABTACT The Indian vector control programme similar to other programmes in the world is still reliant on chemical insecticides. Anopheles culicifacies is the major vector out of six primary malaria vectors in India and alone contributes about 2 /3 malaria cases annually; and per se its control is actually control of malaria in India. For effective management of vectors, current information on their susceptibility status to different insecticides is essential. In this review, an attempt was made to compile and present the available data on the susceptibility status of different malaria vector species in India from the last 2.5 decades. Literature search was conducted by different means mainly web and library search; susceptibility data was collated from 62 sources for the nine malaria vector species from 145 districts in 21 states and two union territories between 1991 and 2016. Interpretation of the susceptibility/resistance status was made on basis of the recent WHO criteria. Comprehensive analysis of the data indicated that An. culicifacies, a major vector species was resistant to at least one insecticide in 70% (101/145) of the districts. It was reported mostly resistant to DDT and malathion whereas, its resistant status against deltamethrin varied across the districts. The major threat for the malaria control programmes is multiple-insecticide-resistance in An. culicifacies which needs immediate attention for resistance management in order to sustain the gains achieved so far, as the programmes have targeted malaria elimination by 2030. Key words Anopheles culicifacies; India; insecticide-resistance; susceptible; malaria INTODUCTION Despite significant progress achieved in the fight against malaria, it is still a major public health problem across the globe. According to the latest estimates of WHO, there were 214 million new cases of malaria worldwide in 2015 (ange 149303 million) and 438,000 malaria deaths (ange 236,000635,000) 1. In India ~1.17 million cases and 384 deaths were reported in 2015 2. Absence of protective malaria vaccine, spread of parasite-resistance to antimalarial drugs and insecticideresistance in vectors have been the key issues for malaria control, and more so would be the determinants to achieve elimination of malaria by 2030. Due to continuous use of insecticides there is rapid development of resistance in malaria vectors worldwide. ince 2010, 60 of the 78 countries that monitor insecticide resistance have reported mosquito resistance to at least one insecticide used in nets and indoor spraying; of these, 49 reported resistance to two or more insecticide classes 1. In India malaria is transmitted by ten vector species, of these six are primary vectors, viz. An. culicifacies, An. fluviatilis, An. stephensi, An. dirus, An. minimus and An. sundaicus; and four are secondary vectors, namely An. annularis, An. philippinensis, An. jeyporiensis and An. varuna. The most dominant mosquito species responsible for the transmission of malaria parasites in India is An. culicifacies, the vector of malaria in the rural areas, contributing ~65% of new cases annually followed by An. fluviatilis contributing ~15% in the forested, foothills and plains 3. Other anophelines species, like An. minimus transmit malaria in foothills of the east and northeast, An. dirus (baimai) in forested areas of Northeastern states, An. sundaicus in Andaman and Nicobar Islands and An. stephensi is the vector in urban areas and in some desert ecotypes 4. Unabated use of insecticides in public health lead to widespread resistance in the vector mosquitoes. Hence, there has always been a need for regular monitoring of insecticide-resistance, and a database on resistance, for

112 J Vector Borne Dis 54, June 2017 implementing effective management strategies for vector control. The available data sets are sometimes not very useful to arrive at decision for reasons, mainly incomplete information on insecticide susceptibility status to different insecticides in use. For their appropriate application, vector susceptibility data needs to be generated using standard protocol, which should be relatively recent and easily accessible. However, due to various administrative and logistic reasons this aspect was neglected and the true status of insecticide-resistance in the malaria vectors in India could not be ascertained routinely. Meanwhile, WHO has embarked on total elimination of malaria by 2030 and efforts have been intensified. Many countries including India have launched malaria elimination programme while, few countries have already achieved it. ensing the importance of insecticide resistance for malaria control and its elimination, WHO has suggested a Global Plan for Insecticide esistance Management (GPIM) 5 that can be followed for resistance management at country level, which also provides technical advocacy. Until recently, there was no consolidation of historical and up-to-date information on insecticide-resistance in malaria vectors in India. This review is an effort to provide an updated report on the status of insecticide-resistance among the major malaria vectors in India based on the information available in last 25 yr drawn from various sources. The study also provides a rational trend on the development of insecticide-resistance in malaria vectors retrospectively, and might provide a better understanding on the dynamics of development of insecticide-resistance with respect to different malaria vector species in India. Insecticide resistance database A data base was collated through search of the published peer-reviewed literature including PubMed/Cochrane review and other online sources. The search was performed using key words from archives of publications and information from international and national sources in the field of Anopheles and insecticide research. Major keywords used for the search were Anopheles, insecticide, susceptible, resistance, names of states, etc. The journal search included Malaria Journal, Parasites and Vectors, Medical and Veterinary Entomology, Journal of Medical Entomology, Tropical Medicine and International Health, American Journal of Tropical Medicine and Hygiene, Transactions of the oyal ociety of Tropical Medicine and Hygiene, Journal of Vector Ecology, Journal of Vector Borne Diseases (formerly Indian Journal of Malariology), Journal of Communicable Diseases, Indian Journal of Medical esearch, Current cience, Journal of Biosciences, Parasitology esearch, outh East Asian Journal of Tropical Medicine and Public Health, Acta Tropica, etc. The search exercise was completed for all the administrative states of India and most of the information were retrieved from national journals. The database was augmented with other sources including published/ unpublished reports such as annual reports and institutional publications from the Indian Council of Medical esearch (ICM) institutes dealing with vector control, like the National Institute of Malaria esearch (formerly, Malaria esearch Centre), Vector Control esearch Centre, as well as other government research organizations. ince, the data contained information retrieved from published/unpublished reports, the onus of the correctness of the data rests with the individual/organization. The data were retrieved till May 9, 2016. Data were extracted into Microsoft Excel data sheets and compiled for analysis. The criteria fixed for susceptibility and resistance were : >98% mortality usceptible, >90 and < 98% mortality Possible resistance/verification required, and <90% mortality esistant 6 ; where mortality rates were reported in range format; the average of the highest and lowest values was used to assign susceptibility status. The locations could not be linked to the GP coordinates as most of the available data was retrospective and not pertaining to specific indications of the study. During data compilation, care was taken to overcome the issues related to quality of the data such as disparities in criteria for reporting resistance, nomenclature of places, period of collection vs reporting of the data, heterozygosity in the data, information in the sample size and dosages, etc. uch disparities are clearly mentioned as footnotes in the data tables of the manuscript. Assumptions were not made during data compilation and it may be assumed as quality assured. However, some of the generated data did not adhere to standard WHO protocol with respect to nonprescribed diagnostic dosages of insecticides or specified number of mosquitoes, etc. uch parameters influencing the study outcomes are mentioned under footnotes of the data table. All data were checked through double entry. Checks were also made for (i) pellings of locality; (ii) Information in the data fields; (iii) Homonyms among the localities; and (iv) ecent identification of the locations with respective administrative states that are bifurcated in the recent years (recently created districts). The information for the data sets included, name of state, name of district (with specified locality/village where available), period of mosquito collection, insecticide-wise percentage mortality, dosages tested (e.g. DDT 4%, malathion

aghavendra et al: Insecticide resistance in Indian malaria vectors 113 5%, deltamethrin 0.05%), number of mosquitoes exposed for test (n), susceptibility status [susceptible (), possible resistance (designated as V, verification required) and resistance ()] categorized as per the WHO guidelines 6. The temporo-spatial insecticide susceptibility data was compiled and mapped district-wise for each state of India. The insecticide susceptibility status for the three insecticides (DDT, malathion and deltamethrin) were depicted in the form of pie chart with three different colour codes: Green for, yellow for V and red for confirmed. Each anopheline species was represented by different colour code rim on the circumference of pie diagram. The year of collection was also mentioned in the respective pie diagram. Literature search yielded 62 reports on susceptibility data sets for nine different Anopheles spp namely An. culicifacies, An. stephensi, An. fluviatilis, An. annularis, An. dirus, An. minimus, An. nivipes, An. subpictus and An. sundaicus that are reported malaria vectors in India. ecently An. subpictus has been implicated to be a dominant vector in urban areas of Goa state. The compiled data, pertain to 145 districts from 21 states and two union territories reported during the years 1991 to 2016. Most of the reported data was for An. culicifacies owing to its wide distribution and intense generation of susceptibility data in the field. It is worthy to mention that An. culicifacies is a major vector of malaria in India and is alone responsible for annual transmission of about two-thirds of total malaria cases. For convenience of the data reporting, the geographical area of India was divided into six zones, namely North, outh, East, West, Central and Northeast Zones comprising 29 states and seven union territories as depicted in Table 1. Insecticide susceptibility in malaria vectors ingle resistance DDT: esistance to DDT in An. culicifacies (Table 2) was reported to be widespread in India except in ithala, Northwest Delhi (Fig. 1) in 1991, where it was reported in V category, while, it was reported susceptible to DDT in Dibrugarh and Nalbari districts of Assam (Fig. 2) in 1995. Anopheles stephensi (Table 3) was reported resistant to DDT in Northwest Delhi (Fig. 1); Pune, Maharashtra (Fig. 3); Bengaluru, and Tumkur in Karnataka (Fig. 4); Gautam Buddh Nagar, Uttar Pradesh (Fig. 1) and Barmer, Pali in ajasthan (Fig. 3). The species was reported susceptible to DDT in Dakshina Kannada (Fig. 4) and under V category in Jaisalmer, ajasthan (Fig. 3). The susceptibility status of An. fluviatilis (Table 4) against DDT was reported mostly from the states of Jharkhand and Odisha. Few data were also reported from some districts of Andhra Pradesh (Fig. 4), Chhattisgarh (Fig. 5), Himachal Pradesh (Fig. 1), Karnataka (Fig. 4), Maharashtra (Fig. 3),Tamil Nadu (Fig. 4); and Uttarakhand (Fig. 1). The species was reported susceptible to DDT in Visakhapatnam, Andhra Pradesh (Fig. 4) in the year 1999 and in districts Angul, Bolangiri, Gajapati, Ganjam, Kalahandi, Kandhamal, Kendujhar, Koraput, Malkangiri, Mayurbhanj, Nabarangpur, Nuapada, ayagada, ambalpur and undargarh of Odisha state (Fig. 6) Table 1. Zonal distribution of India with prevalent vector species in each zone. No. Zones tates (Districts surveyed/total no. of districts) Malaria vectors Primary 1. North Zone Jammu and Kashmir ( 0/22), Haryana (5/21), Himachal Pradesh (1/12), Punjab (1/22), Uttarakhand (2/13), Uttar Pradesh (5/75) and National Capital Territory of Delhi (1/11) 2. outh Zone Andhra Pradesh (4/13), Telangana (1/10), Karnataka (9/29), Kerala ( 0/14) and Tamil Nadu (3/32) and Car Nicobar Island (1/3) 3. East Zone Bihar ( 0/38), Jharkhand (8/24), Odisha (22/30), and West Bengal (5/20) 4. West Zone Goa (1/2), Gujarat (4/26), ajasthan (6/33) and Maharashtra (2/35) An. culicifacies, An. fluviatilis and An. stephensi An. culicifacies, An. fluviatilis, An. stephensi and An. sundaicus An. annularis, An. culicifacies, An. fluviatilis, An. minimus and An. stephensi An. annularis, An. culicifacies, An. fluviatilis, An. stephensi and An. subpictus 5. Central Zone Chhattisgarh (28/28), Madhya Pradesh (15/50) An. culicifacies and An. fluviatilis 6. Northeast Zone Arunachal Pradesh ( 0/20), Assam (16/33), Manipur ( 0/9), Meghalaya (2/11), Mizoram (0/8), Nagaland (0/11), ikkim (0/4) and Tripura (3/8) An. annularis, An. culicifacies, An. dirus and An minimus econdary An. subpictus An. nivipes (philippinensis) An. nivipes (philippinensis)

114 J Vector Borne Dis 54, June 2017. No. Table 2. Insecticide susceptibility status on Anopheles culicifacies in different states of India tate District (Location) Year Percentage mortality (n) and susceptibility status eference DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus 1. Andhra Pradesh East Godavari 2009 36.6 (60) 80 (60) 70 (60) 7 rikakulam 0 (21 a ) 44.4 (135) 77.7 (72) Visakhapatanam 6.6 (15 a ) 46.6 (15 a ) 73.6 (19 a ) Vizianagaram 0 (17 a ) 32.2 (62) 93.3 (15 a ) V Visakhapatanam (Allamput) 1999 40 b b b 8 2. Assam Chirang/Chirag 2009 25 (8 a ) 30 (7 a ) aghavendra Dhemaji, Lakhimpur 70 (40 a ) Dibrugarh (onitpur 1995 b 9 Gorubandh) Nalbari b 10 3. Chhattisgarh Baloda Bazar 2016 4.9 (101) 60.9 (105) 75.8 (112) Bhatt Bemetara 3 (100) 60.1 (103) 82.6 (104) Durg 4.5 (110) 72.9 (111) 70.5 (102) Janjgir-Champa 14.2 (105) 53 (83) 64.1 (106) Kabirdham/Kabeerdham 2.9 (102) 60 (100) 80.3 (102) (Formerly Kawardha) Bastar 2015 63.4 (112) 77.3 (110) Bijapur 1 (100) Bilaspur 67.5 (111) 65.7 (105) Dantewada 0 (70) 65 (20 a ) Dhamtari 73.5 (132) 61.2 (103) Gariyaband/Gariaband 67 (103) 45 (100) Kanker 63.9 (111) Kondagaon 54.3 (105) 79.9 (105) Korba 57.7 (109) Mahasamund 70.1 (104) 30 (100) Mungeli 81 (100) Narayanpur 81.8 (110) 56.9 (105) aigarh 4 (126) 75 (124) aipur 0 (100) 26.5 (102) ajnandgaon 35 (100) 62.6 (127) ukma 2.5 (80) 73.3 (60) Balod 2014 60 (60) Balrampur 5 (101) 88.8 (107) Kanker 82.7 (98) Koriya/Korea 10 (100) 72.9 (107 urajpur 7.3 (109) 87.9 (107) urguja 14 (100) 85.3 (102) Bilaspur, Korba, Korea 2009 33.7 (95) 42 (108) 80.5 (118) 11 Dantewada 9.8 (82) 55.3 (85) 98.7 (96) Dhamtari, aipur 4 (99) 73.5 (98) 78.6 (98) Jagdalpur 21 (100) 39.4 (100) 77 (100) Jashpur, aigarh 10 (60) 42.4 (66) 68 (75) Kanker 3.2 (186) 69.4 (216) 83.3 (190) Jagdalpur 2002 83.8 (40 a ) 90.4 (46 a ) V 12 Kanker 22.9 (40 a ) 74.1 (43 a ) 89.4 (45 a ) Mahasamund 25 (78) 87.9 (36 a ) 89.5 (40 a ) aigarh 13.8 (79) 59.3 (65) 92.5 (40 a ) V 4. Delhi Northwest Delhi (Mukundpur/Mukunpur) 1989 53.3 (15 a ) 100 (15 a ) 100 (15 a ) 13 1991 c contd...

aghavendra et al: Insecticide resistance in Indian malaria vectors 115. No. Table 2 (Contd.) tate District (Location) Year Percentage mortality (n) and susceptibility status eference DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus Northwest Delhi (ithala) 90 (10 a ) V 100 (10 a ) 100 (10 a ) 5. Gujarat urat 2006 20 (168) 57 (220) 99 (190) 14 urat 2005 40 (66) 68 (145) 98 (62) urat 2001 9 (192) 66 (322) urat 2001 6078 b 15 urat (Gangapore) 13.1 (74) 60.4 (106) urat (Kakrapara) 6.7 (60) 78.3 (106) urat (Limbi) 6.9 (58) 61.3 (109) urat (Nidwada) 69.2 (117) urat 1993 8.822 b 11.11 b 16 urat 1992 6 (100) 17 (60) 17 6. Haryana Gurgaon (Mewat) 1997 100 (45 a ) 18 onepat 100 (45 a ) Gurgaon (Prataphas) 1996 78 (50 a ) 19 Gurgaon (alamba) 73 (30 a ) 87.9 (133) 100 (30 a ) Gurgaon (Tekri) 45.9 (61) 79.3 (92) 100 (147) Gurgaon (irsa) 1994 b b 20 Karnal (Gharaunda) 85 (34 a ) Karnal (Kaiwala) 88 (35 a ) Punchkula (Pinjore) 75 (30 a ) Yamuna Nagar (Todarpur) 65 (26 a ) 7. Jharkhand Koderma 2010 37.8 (180) 98.3 (180) 100 (180) 21 (Divided East inghbhum 2009 23.7 (140) 95.1 (110) V 100 (120) 7 out of Gumla 26.3 (227) 96.9 (152) V 99.0 (191) Bihar in 2000) anchi 10.4 (320) 98.1 (170) 98.1 (210) West inghbhum 15.8 (180) 98 (170) 100 (160) Gumla 2007 38.4 (664) 95.4 (611) V 98.8 (566) 22 Hazaribagh 1992 37.5 e (60) 94.6e (60) V 23 8. Karnataka Tumkur 2005 97 (60) V 24 9. Madhya Anuppur 2012 33 (1520 a ) 100 (1520 a ) 25 Pradesh Chhindwara 54 (1520 a ) 80 (1520 a ) Dhindori/Dindori 26 (1520 a ) 100 (1520 a ) Katni 55 (1520 a ) 95 (1520 a ) V Mandla 50 (1520 a ) 100 (1520 a ) Narsinghpur/Narsingpur 30 (15-20 a ) 100 (1520 a ) atna 35 (1520 a ) 100 (1520 a ) eoni 50 (1520 a ) 95 (1520 a ) V Umaria 40 (1520 a ) 100 (1520 a ) Balaghat 2009 6.7 (120) 84 (150) 92 (150) V 26 Betul 12.4 (225) 72.4 (225) 83.1 (225) Chhindwara 9.2 (315) 74.9 (315) 85.9 (315) Dhindori/Dindori 12.8 (180) 80 (180) 71.6 (180) Guna 26.6 (300) 100 (300) 100 (270) Jhabua/Jhabula 6.6 (240) 65.4 (240) 87 (240) Mandla 13.3 (180) 78.3 (180) 76.6 (180) hahdol 8.8 (180) 77.8 (180) 93.8 (180) V idhi 7.5 (360) 78.8 (360) 94.1 (360) V 10. Maharashtra Gadchiroli (Murumgaon) 2010 23.2 (100) 96 (100) V 94 (100) V 27 Gadchiroli (Malanda, Maveli, Chavela) 2001 51 (45) 92.9 (33) V 100 (60) 28 contd...

116 J Vector Borne Dis 54, June 2017. No. Table 2 (Contd.) tate District (Location) Year Percentage mortality (n) and susceptibility status eference DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus 11. Odisha Kalahandi 2014 12.4 (105) 60.4 (111) 79.4 (131) 29 Koraput 15.3 (111) 66.7 (111) 76.8 (112) Malkangiri 12.6 (111) 76.2 (105) 84.0 (119) Nabarangpur/Nawaranghpur 11.4 (105 70.9 (110) 72.6 (113) ayagada 12.6 (135) 63.1 (130) 81.7 (131) Balangir/Bolangir 2010 12.3 (106) 80 (105) 94.2 (104) V 30 Gajapati 15.5 (103) 83.8 (105) 82.9 (105) Ganjam 14.7 (102) 70.3 (101) 95.2 (104) V Kalahandi 14.3 (105) 86.7 (105) 81.7 (104) Kandhamal 9.5 (105) 77.6 (109) 96.3 (109) V Koraput 13.5 (111) 76.6 (111) 98.4 (123) Malkangiri 15.2 (105) 75.5 (110) 86.2 (109) Nabarangpur/Nawaranghpur 13.8 (109) 63.5 (126) 96.5 (114) V Nuapada 15 (107) 67.3 (98) 100 (89) ayagada 16.7 (102) 77.6 (105) 89.8 (108) Angul 2009 9.7 (80) 100 (40 a ) 96.3 (30 a ) V 7 Bargarh/Baragarh 12.5 (300) 72.3 (280) 98.8 (340) Balangir/Bolangir 7.8 (502) 74.4 (511) 96.0 (494) V Cuttack 20 (100) 74 (90) 100 (90) Dhenkanal, ubarnapur/ 9.3 (30 a ) 100 (20 a ) 100 (20 a ) onepur Gajapati 12.6 (300) 70.3 (280) 98 (280) Ganjam 18.4 (30 a ) 85 (20 a ) 100 (30 a ) Jagatsinghpur 23 (100) 85.5 (80) 100 (90) Jharsuguda 12.6 (260) 40.0 (240) 96.7 (240) V Kalahandi 11.8 (76) 78.3 (120) 81.6 (120) Kendujhar/Keonjhar 11.1 (40 a ) 100 (30 a ) 100 (20 a ) Khordha/Khurda 20 (20 a ) 80 (20 a ) 100 (30 a ) Mayurbhanj, ambalpur 14.8 (30 a ) 100 (20 a ) 96.3 (27 a ) V Nuapada 3.3 (60) 93.8 (49 a ) V 88.1 (59 a ) Kandhamal (Phulbani) 6.4 (93) 59.1 (98) 93.7 (96) V ayagada 23.1 (272) 90.6 (278) V 89.2 (270) undargarh 25.9 (280) 70.7 (260) 95.1 (260) V undargarh 2008 b b 31 Gajapati (Guma) 2005 20 (15 a ) 100 (15 a ) Hazra Gajapati (Mohana) 26.6 (15 a ) 100 (15 a ) Mayurbhanj (Badampahar, 20 (15 a ) 100 (15 a ) angamatia) Nabarangpur (Nandahandi) 20 (15 a ) 100 (15 a ) Nabarangpur (Papadahandi) 26.6 (15 a ) 100 (15 a ) Nabarangpur (Tentulikhunti) 20 (15 a ) 100 (15 a ) ayagada (Bisamcuttack) 26.6 (15 a ) 100 (15 a ) ayagada (Muniguda) 13.3 (15 a ) 100 (15 a ) Balangir/Bolangir 2002 23.3 (60) 68.3 (60) 95 (60) V 32 Kalahandi 12 (60) 88.3 (60) 96.7 (60) V Kendujhar/Keonjhar 14 (50 a ) 100 (80) Mayurbhanj 62.5 (40 a ) 50 (40 a ) 100 (60) Nuapada 8.3 (60) 75 (60) 81.7 (60) Kandhamal (Phulbani) 20 (60) 100 (60) 100 (60) ayagada 15 (60) 100 (60) 100 (60) undargarh 12 (100) 100(100) 100 (100) Koraput 21.2 (33) 33 Malkangiri 21.1 (90) 35.3 (102) 100 (51) Malkangiri 1993 010 (925) 34 contd...

117 aghavendra et al: Insecticide resistance in Indian malaria vectors Table 2 (Contd.). tate No. 12. 13. 14. 15. District (Location) Year DDT (4%) b 30 (10a) 60.6 (94) 46.6 (60) 83.3 (180) ajasthan Jaisalmer 1999 Jaisalmer (Pokaran) 1995 Bikaner 1993 Tamil Dharmapuri 2006 Nadu amanathapuram amanathapuram 1997 (ameshwaram) Telangana Khammam 2009 23.3 (60) Uttar Moradabad 2002d 42.5b Pradesh Gautam Buddh Nagar 2008 20b Gautam Buddh Nagar 2006 26-45b [Delhi (Yamuna iver)] Gautam Buddh Nagar (Noida) 26-45b Bareilly/Bareeily 2002 21.4 (40) Bareilly/Bareeily 2001 15.5 (110) 16. Uttarakhand 17. West Bengal Percentage mortality (n) and susceptibility status tatus Malathion (5%) tatus Deltamethrin (0.05%) V b 100 (10a) 98.6 (81) 100 (45a) 73.3 (60) 100 (180) 100 (180) 100 (45a) eference tatus 63.3 (60) b 100b 43.3 (60) b 100b 100b 100b Bahraich Allahabad Haldwani (Nainital) Hardwar 1999 7.3 (60) 1996 b 2002d 2001 b 86.2b 8090 (200) 100b (15 min) 100b Nainital (Formerly in UP) Bankura, Paschim/West Medinipur (Midnapur) Birbhum, Purulia 1997 2009 1.1 (90) 3.3 (60) 88.3 (60) 100 (30a) 100 (40a) 6.6 (75) 90.8 (65) V 100 (45a) 35 36 37 24 18 7 38 39 40 41 aghavendra 42 43 44 aghavendra 45 7 n <60; Percentage mortality data not available; Final year considered as the collection year; eported year considered as the collection year; One hour exposed data; f30 min exposure time; () Not reported; Confirmed resistance; V Possible resistance; usceptible. a b c d e Fig. 1: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the tates of Himachal Pradesh, Uttarakhand, Delhi, Uttar Pradesh, Haryana and Punjab of North Zone, India. Fig. 2: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the tates of Assam, Tripura and Meghalaya of Northeast Zone, India.

118 J Vector Borne Dis 54, June 2017. No. Table 3. Insecticide susceptibility status of An. stephensi in different states of India tate District (Location) Year Percentage mortality (n) eference DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus 1. Delhi Northwest Delhi (Jatkhore/Jatkhar) Northwest Delhi (Madanpur) Northwest Delhi (ithala) 1989 1991 46.6 (15 a ) 66.6 (15 a ) 100 (15 a ) 13 86.6 (15 a ) 93.3 (15 a ) V 100 (15 a ) 22.2 (45 a ) 43.3 (30 a ) 100 (15 a ) 2. Goa North Goa (Panaji) 1991 10 (100) 26 (100) 46 3. Gujarat Kutch (Bhuj) 2007 68.4 (2040 a ) 38.5 (2040 a ) 100 (2040 a ) 47 Jamnagar 95.4 (2040 a ) V 90 (2040 a ) V Gandhinagar 2005 77.2 (2040 a ) 100 (2040 a ) Jamnagar 76 (2040 a ) 100 (2040 a ) urat 2000 51.7 b 93.3 b V 48 4. Karnataka Dakshina Kannada 2006 98.1 (60) 54.9 (106) 86.1 (72) 49 (Mangalore) Bengaluru ural 1992 d 50 b 100 b 50 (Dasarahalli) Bengaluru ural 40 b 100 b (Talaghattapura) Bengaluru Urban 50 b 100 b (Koramangala) Urban (Mathikere) 80 b 100 b Bengaluru Urban 45 b 100 b (Wilson Garden) amanagar 40 b 80 b (Kanakapura) Tumkur 40 b 100 b 5. ajasthan Bikaner 2007 77.3 (2040 a ) 47 Jodhpur 71.8 (2040 a ) 94.7 (2040 a ) V 100 (2040 a ) Barmer 2006 59.9 (2040 a ) 100 (2040 a ) Jodhpur 72 (2040 a ) 92.9 (2040 a ) V Barmer 2005 100 (2040 a ) Bikaner 66.6 (2040 a ) 100 (2040 a ) Ganganagar 95.4 (2040 a ) V 94.1 (2040 a ) V (ri Ganganagar) Jaisalmer 1999 b V b 35 Jodhpur 1995 3040 b 100 b 51 Barmer b b V 52 Jodhpur b b V Pali b b V Bikaner 1993 40 (85) 91.3 (103) V 37 6. Maha- Pune/Poone 1992 d 50 b 100 b 50 rashtra 7. Uttar Gautam Buddh Nagar 2006 2645 b 100 b 100 b 40 Pradesh [Delhi (Yamuna iver)] Gautam Buddh Nagar 2645 b 100 b 100 b (Noida) 8. West Kolkata 1998 80 (100) 80 (100) 53 Bengal 1995 55 (60) 100 f (60) 54 a n <60; b Percentage mortality data not available; c Final year considered as the collection year; d eported year considered as the collection year; e One hour exposed data; f 30 min exposure time; () Not reported; Confirmed resistance; V Possible resistance; usceptible.

aghavendra et al: Insecticide resistance in Indian malaria vectors 119 Fig. 3: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the tates of ajasthan, Gujarat, Maharashtra and Goa of West Zone, India. Fig. 5: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the tates of Madhya Pradesh and Chhattisgarh of Central Zone, India. Fig. 4: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the tates of Telangana, Andhra Pradesh, Tamil Nadu, Karnataka and Andaman & Nicobar Islands of outh Zone, India. Fig. 6: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the tates of Jharkhand, West Bengal and Odisha of East Zone, India.

120 J Vector Borne Dis 54, June 2017. No. Table 4. Insecticide susceptibility status of An. fluviatilis in different states of India tate District Year Percentage mortality (n) eference 1. Andhra Pradesh Visakhapatanam (Allamput) DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus 1999 b b b 8 2. Chhattisgarh Jashpur 2015 13.3 (105) 100 (104) Bhatt 3. Himachal Pradesh 4. Jharkhand (Divided out of Bihar in 2000) aigarh 2009 50 (28 a ) aghavendra Una 1997 b b 43 Koderma 2010 64.03 (120) 100 (118) 100 (120) 21 East inghbhum 2009 76.2 (130) 99.3 (110) 100 (110) aghavendra Gumla 80.3 (240) 100 (186) 100 (172) anchi 80.8 (180) 97.3 (135) V 100 (120) West inghbhum 78.2 (180) 98.6 (165) 100 (170) Gumla 2007 67.7 (619) 100 (542) 100 (438) 22 Dhanbad 1997 b b 43 Hazaribagh 1992 96.4 e (60) V 100 e (60) 23 5. Karnataka Bangalore/Bengaluru 1997 b b 43 Belgaum b b Bijapur b b Kolar b b himoga b b 6. Maharashtra Gadchiroli (Murumgaon) 2010 36.6 (60) 95 (60) V 96.4 (60) V 27 7. Odisha ayagada 2013 100 (100) 100 (100) 55 Balangir/Bolangir 2010 100 (56 a ) 100 (54 a ) 100 (54 a ) 30 Gajapati 100 (62) 100 (61) 100 (57 a ) Ganjam 100 (50 a ) 100 (52 a ) 100 (52 a ) Kalahandi 100 (79) 100 (62) 100 (79) Kandhamal 100 (60) 100 (64) 100 (63) Koraput 100 (55 a ) 100 (66) 100 (55 a ) Malkangiri 100 (67) 100 (44 a ) 100 (56 a ) Nabarangpur/Nawaranghpur 100 (32 a ) 100 (20 a ) 100 (24 a ) Nuapada 100 (54 a ) 100 (54 a ) 100 (58 a ) ayagada 100 (60) 100 (57 a ) 100 (58 a ) Angul 2009 100 (8 a ) aghavendra Kendujhar/Keonjhar 100 (6 a ) Kendujhar/Keonjhar 100 (52 a ) 100 (52 a ) 56 (Banspal) ambalpur, Mayurbhanj 100 (20 a ) aghavendra undargarh/undergarh 2008 b b 31 Kalahandi 2002 100 (60) 100 (60) 100 (60) 32 Koraput 100 (557) 100 (210) 100 (290) 33 Kendujhar/Keonjhar 100 (100) 100 (40 a ) 100 (120) 32 Malkangiri 100 (493) 100 (192) 100 (108) 33 contd...

aghavendra et al: Insecticide resistance in Indian malaria vectors 121. No. Table 4 (Contd.) tate District Year Percentage mortality (n) eference DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus Mayurbhanj 95.0 (40 a ) V 87.5 (40 a ) 100 (40 a ) 32 Kandhamal (Phulbani) 100 (60) 100 (40 a ) 100 (40 a ) undargarh/undergarh 100 (100) 100 (60) 100 (100) 2001 100 b 100 b 100 b 48 2000 100 b 100 b Malkangiri 1993 100 (260) 34 8. Tamil Nadu Coimbatore 1997 b b 43 9. Uttarakhand Nainital (Formerly in UP) 1997 21.6 (85) 100 (70) 45 a n <60; b Percentage mortality data not available; c Final year considered as the collection year; d eported year considered as the collection year; e One hour exposed data; f 30 min exposure time; () Not reported; Confirmed resistance; V Possible resistance; usceptible. and under V category from Hazaribagh, Jharkhand (Fig. 6) in 1992. The species was resistant to DDT in the districts Jashpur and aigarh of Chhattisgarh state (Fig. 5); Una in Himachal Pradesh (Fig. 1); Dhanbad, East inghbhum, Koderma, Gumla, anchi and West inghbhum in Jharkhand (Fig. 6); Belgaum, Bengaluru, Bijapur, Kolar and himoga, Karnataka (Fig. 4); Gadchiroli in Maharashtra (Fig. 3); Coimbatore, Tamil Nadu (Fig. 5) and District Nainital of Uttarakhand state (Fig. 1). Anopheles annularis (Table 5) reported as secondary vector and as vector of prominence in some eastern states, exhibited resistance to DDT in Kamrup and Baksa districts of Assam state (Fig. 2); Gumla, Hazaribagh, Koderma, anchi and West inghbhum of Jharkhand state (Fig. 6); Gadchiroli of Maharashtra state (Fig. 3); Gajapati, Nabarangpur, ayagada and undergarh, Districts of Odisha state (Fig. 6) and Bikaner district of ajasthan state (Fig. 3) except in ahibganj of Jharkhand state (Fig. 6) where this species was reported susceptible. Anopheles dirus (Table 4) was reported susceptible to DDT from District Dibrugarh in Assam (Fig. 2). Another important primary vector An. minimus (Table 4) was reported from Districts of Assam, Jharkhand, Meghalaya, Odisha and Tripura. The species was reported resistant to DDT from Kendujhar, Odisha (Fig. 6) in 2003, possible resistance in the Districts of Kamrup, Kamrup Metropolitan and onitpur districts of Assam (Fig. 2) in 2002; Kendujhar of Odisha (Fig. 6) in 2009 and outh Tripura (Fig. 2) in 2007. This species was reported susceptible from Chirang, Darang, Dhemaji, Dhubri, Dibrugarh, Goalpara, Lakhimpur, Morigaon, Nagaon, Nalbari and Udalguri in the tate of Assam (Fig. 2); ahibganj from the tate of Jharkhand (Fig. 6); East and West Garo Hills from Meghalaya (Fig. 2); and Dhalai and West Tripura from Tripura state (Fig. 2). Another vector of prominence in Northeast Zone, An. nivipes (philippinensis) (Table 5) was reported resistant to DDT in districts ibsagar and Dibrugarh of Assam (Fig. 2) in 1998, possible resistance in outh Tripura (Fig. 2) in 2007 and susceptible in district ahibganj, Jharkhand (Fig. 6) in 1998. Anopheles sundaicus (Table 4), a primary vector in Andaman and Nicobar Islands was reported resistant to DDT in Car Nicobar Island (Fig. 4) in 198991. Malathion: Malathion resistance in An. culicifacies (Table 2) was reported from Districts Karnal, Punchkula, Yamunanagar in Haryana (Fig. 1) and Hardwar in Uttarakhand (Fig. 1) The species exhibited possible resistance status in the Districts of East inghbhum, Gumla and Hazaribagh of Jharkhand state (Fig. 6); Tumkur of Karnataka (Fig. 4); Katni and eoni of Madhya Pradesh (Fig. 5); Gadchiroli from Maharashtra (Fig. 3); Nuapada and ayagada of Odisha (Fig. 6) and Districts Birbhum and Purulia of West Bengal state (Fig. 6). Anopheles culicifacies was reported susceptible to malathion in village ithala of Northwest Delhi (Fig. 1); Districts Koderma, anchi, West inghbhum of Jharkhand state (Fig. 6); Anuppur, Dhindori, Guna, Mandla, Narsinghpur, atna, Umaria of Madhya Pradesh (Fig. 5); Angul, Dhenkanal, Kandhamal, Kendujhar, Mayurbhanj, ambalpur, ubarnapur, undargarh of Odisha (Fig. 6); Jaisalmer and Bikaner of ajasthan (Fig. 3); Dharamapuri and amanathapuram of Tamil Nadu (Fig. 4) and District Gautam Buddh Nagar of Uttar Pradesh (Fig. 1). Anopheles stephensi reported mostly susceptible to malathion (Table 3) in Bengaluru urban and rural districts in Karnataka (Fig. 6) resistant in Mangalore and

122 J Vector Borne Dis 54, June 2017. No. Table 5. Insecticide susceptibility status of other anophelines in different states of India pecies tate District Year Percentage mortality (n) eference 1. An. annularis Assam Jharkhand (Divided out of Bihar in 2000) DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus Kamrup 2011 28.3 (60) 97.7 (43 a ) V 57 (Chandubi Area Kasi Hills) Kamrup 11.9 (43 a ) 98.1 (54 a ) (ani Area Kasi Hills) Baksa (Tamulpur) 1995 82 b 10 Koderma 2010 40.35 (180) 100 (180) 99.44 (180) 21 East inghbhum 2009 23.0 (160) 84.3 (110) 100 (120) aghavendra Gumla 41.7 (180) 98.4 (180) 100 (100) anchi 29.8 (180) 100 (170) 100 (160) West inghbhum 14.8 (180) 94.7 (150) V 99.3 (160) Gumla 2007 45.9 (335) 97.7(438) V 100 (360) 22 ahibganj 1998 100 f (8 a ) 100 f (5 a ) 58 (ajmahal) Hazaribagh 1992 13.1 e (60) 100 e (60) 23 Maharashtra Gadchiroli 2010 21 (100) 90.5 (100) V 95 (100) V 27 (Murumgaon) Odisha undargarh 2000 5.8 b 100 b 48 Gajapati (Guma) 2005 13.3 (15 a ) Hazra Nabarangpur 13.3 (15 a ) (Papadahandi) ayagada 20.0 (15 a ) (Muniguda) ajasthan Bikaner 1993 36.2 (102) 94.6 (92) V 37 2. An. dirus Assam Dibrugarh 1997 100 (36 a ) 100 (30 a ) 59 3. An. minimus Assam Chirang/Chirag 2009 100 (06 a ) aghavendra Goalpara and 100 (176) 100 (96) 100 (90) Dhubri Lakhimpur and 100 (40 a ) 100 (10 a ) 100 (10 a ) Dhemaji Udalguri 100 (02 a ) Jharkhand (Divided out of Bihar in 2000) Darrang/Darang, 2002 98.3 (60) 100 (40 a ) 60 Udalguri Kamrup, 96.3 (80) V 100 (60) Kamrup Metropolitan (onapur) onitpur (Balipara) 97.5 (80) V 100 (40 a ) Morigaon 1999 100b 100 b 61 Nagaon 1995 100 (40 a ) 100 (40 a ) 62 Nalbari b 10 Dibrugarh (onitpur-gorubandh) ahibganj (ajmahal) b 9 1998 100f (30 a ) 100f (26 a ) 58 contd...

aghavendra et al: Insecticide resistance in Indian malaria vectors 123. No. pecies tate District Year Percentage mortality (n) eference 4. An. nivipes (philippinensis) 5. An. subpictus 6. An. sundaicus Meghalaya Odisha Tripura East & West Garo Hills Kendujhar/Keonjhar (Banspal) DDT (4%) tatus Malathion (5%) tatus Deltamethrin (0.05%) tatus 2009 100 (06 a ) aghavendra 2009 96.2 (52 a ) V 100 (52 a ) 56 Kendujhar/Keonjhar 2003 86 (21 a ) 100 (45 a ) 63 Dhalai, West and outh Tripura outh Tripura (Belonia) 2009 100 (10 a ) aghavendra 2007 92.9 (30 a ) V 100 (30 a ) 64 Assam Chirang/Chirag 2009 100 (7 a ) aghavendra ivasagar/ib agar and Dibrugarh 1998 b 43 Jharkhand (Divided out of Bihar in 2000) Tripura Tripura ahibganj (ajmahal) Dhalai, West and outh Tripura outh Tripura (Belonia) 1998 100 (17 a ) 100 (16 a ) 58 2009 100 (10 a ) aghavendra 2007 96.6 (30 a ) V 100 (30 a ) 64 Gujarat Kutch (Bhuj) 2007 57.1 39.4 (2040 a ) 87.5 (2040 a ) 47 (2040 a ) Gandhinagar 66.7 44 (2040 a ) 100 (2040 a ) (2040 a ) Jamnagar 40.6 50 (2040 a ) 100 (2040 a ) (2040 a ) Gandhinagar 2006 40.62 b 75 (2040 a ) 100 (2040 a ) Jamnagar 46.15 b Gandhinagar 2005 40.6 (2040 a ) 100 (2040 a ) Jamnagar 55 (2040 a ) 92 (2040 a ) V Punjab Bathinda 2004 89.4 (2040 a ) 90 (2040 a ) V ajasthan Barmer 2006 70.8 36 (2040 a ) 100 (2040 a ) (2040 a ) Jodhpur 50 (2040 a ) 40.6 (2040 a ) 100 (2040 a ) Andaman and Nicobar Islands Barmer 2005 52 b 96.2 (2040 a ) V 90 (2040 a ) V Jodhpur 64.3 (2040 a ) 88.2 (2040 a ) Bikaner 2004 37.5 (2040 a ) 92.3 (2040 a ) V Ganganagar 64.3 (2040 a ) 100 (2040 a ) (ri Ganganagar) Bikaner 1993 21.4 (103) 100 (63) 37 Car Nicobar Island (Kimios, Kakana, awai and Malaka) Table 5 (Contd.) 1989 87.7 99 65 1991 c a n <60; b Percentage mortality data not available; c Final year considered as the collection year; d eported year considered as the collection year; e One hour exposed data; f 30 min exposure time; () Not reported; Confirmed resistance; V Possible resistance; usceptible. amanagar. It was variable resistant in Districts of ajasthan (Fig. 3) and mostly in the verification required category and the species reported resistant in District Jodhpur. The species was reported susceptible to malathion in District Pune of Maharashtra (Fig. 3) and Gautam Buddh Nagar in Uttar Pradesh ( Fig. 1) while it was reported resistant in Kolkata in West Bengal (Fig. 6). Anopheles fluviatilis (Table 4) was reported sus-

124 J Vector Borne Dis 54, June 2017 ceptible to malathion in several districts of the states of Chhattisgarh (Fig. 5), Jharkhand (Fig. 6), Karnataka (Fig. 4), Odisha (Fig. 6), Andhra Pradesh (Fig. 4), Himachal Pradesh (Fig. 1), Maharashtra (Fig. 3), Tamil Nadu (Fig. 4) and Uttarakhand (Fig. 1) except in District anchi in Jharkhand, Gadchiroli in Maharashtra and District Mayurbhanj in Odisha, where the species was reported under V category. Anopheles annularis (Table 5) was reported resistant to malathion in the tates of Jharkhand (Fig. 6), Maharashtra (Fig. 3), Odisha (Fig. 6) and ajasthan (Fig. 3) and was mostly susceptible to malathion with emerging possible resistance in few Districts of Jharkhand, Maharashtra and ajasthan. The species was reported resistant in District East inghbhum and under V category in West inghbhum and Gumla of Jharkhand; Gadchiroli in Maharashtra and from District Bikaner in ajasthan state. Anopheles dirus, prevalent in Northeast state was reported susceptible to malathion in District Dibrugarh in Assam (Table 5, Fig. 2). Anopheles minimus, in Eastern and Northeastern states was reported susceptible to malathion in the Districts Goalpara, Dhubri, Lakhimpur, Dhemaji, Morigaon and Nagaon in Assam (Table 5, Fig. 2) and from ahibganj in Jharkhand state (Fig. 6). Another vector species, An. nivipes (philippinensis) (Table 5) found in Eastern and Northeastern states, was found susceptible to malathion in District Chirang in Assam (Fig. 2), ahibganj in Jharkhand (Fig. 6) and in Districts Dhalai, West and outh Tripura in Tripura state (Fig. 2). An. sundaicus prevalent in Andaman and Nicobar Islands, was reported susceptible to malathion in Car Nicobar Islands (Fig. 4). Anopheles subpictus (Table 5),primarily a non-vector species (but recently reported as vector species in Goa) was reported mostly resistant in Districts Kutch, Gandhinagar and Jamnagar in Gujarat (Fig. 3); Bhatinda in Punjab (Fig. 1) and in Districts Barmer, Jodhpur, Bikaner and Ganganagar in ajasthan (Fig. 3). Deltamethrin: Anopheles culicifacies susceptibility data is given in Table 2, and in maps for respective states, namely Andhra Pradesh (Fig. 4), Assam (Fig. 2), Chhattisgarh (Fig. 5), Delhi (Fig. 1), Haryana (Fig. 1), Gujarat (Fig. 3), Jharkhand (Fig. 6), Madhya Pradesh (Fig. 5), Maharashtra (Fig. 3), Odisha (Fig. 6), Tamil Nadu (Fig. 4), Telangana (Fig. 4), Uttar Pradesh (Fig. 1), Uttarakhand (Fig. 1) and West Bengal (Fig. 6). The species was reported resistant to deltamethrin in Districts East Godavari, rikakulam and Visakhapatnam of Andhra Pradesh; Chirang in Assam; Balod and Mungeli districts of Chhattisgarh; Betul, Chhindwara, Dhindori, Jhabua and Mandla in Madhya Pradesh; Gajapati, Kalahandi, Koraput, Malakangiri, Nabarangpur, ayagada in Odisha; Dharmapuri in Tamil Nadu and district Khammam in Telangana state. Possible resistance was reported from district Vizianagaram of Andhra Pradesh; Balaghat, hahdol and idhi in Madhya Pradesh; Gadchiroli in Maharashtra; Angul, Bolangir, Ganjam, Jharsuguda, Kandhamal, Mayurbhanj, ambalpur and undargarh in Odisha state. This species was reported susceptible to deltamethrin in Northwest Delhi in the National Capital egion of Delhi; District Gurgaon and onepat in Haryana; East inghbhum, Gumla, Koderma, anchi, West inghbhum in Jharkhand; Guna in Madhya Pradesh; Bargarh, Cuttack, Dhenkanal, Ganjam, Jagatsinghpur, Kendujhar, Khordha, and ubarnapur in Odisha; amanathapuram in Tamil Nadu; Bahraich and Gautam Buddh Nagar in Uttar Pradesh; Nainital in Uttarakhand and from District Bankura, Birbhum, Paschim/ West Midnapur and Purulia in West Bengal state. However, the species showed reversion of deltamethrin resistance in District urat, Gujarat after three years of its withdrawal from indoor residual spray (I) in the year 2005 7. Anopheles stephensi (Table 3) was reported resistant to deltamethrin in district Dakshina Kannada of Karnataka (Fig. 4). The species was susceptible in Northwest Delhi (Fig. 1), Districts Kutch and Gandhinagar in Gujarat (Fig. 3); Bikaner in ajasthan (Fig. 3); Gautam Buddh Nagar in Uttar Pradesh (Fig. 1) and district Kolkata in West Bengal state (Fig. 6). Anopheles fluviatilis (Table 4) was reported mostlysusceptible to deltamethrin in Andhra Pradesh (Fig. 2), Chhattisgarh (Fig. 5), Jharkhand (Fig. 6), Odisha (Fig. 6) and Uttarakhand (Fig.1) states while it showed possible resistance in district Gadchiroli in Maharashtra (Fig.3). Anopheles annularis (Table 5), a secondary vector was reported susceptible in Jharkhand (Fig. 6) and Odisha (Fig. 6), while it was in possible resistant category in District Kamrup of Assam (Fig. 2) and Gadchiroli in Maharashtra state (Fig. 3). Anopheles minimus (Table 5) was reported susceptible in Assam (Fig. 2), Odisha (Fig. 6) and Tripura (Fig. 2) and An. nivipes (philippinensis) (Table 5) in Tripura (Fig. 2). Anopheles subpictus (Table 5), showed varied susceptibility to deltamethrin in Districts of Gujarat, Punjab and ajasthan (Figs. 1 and 3 respectively). Double resistance DDT-Malathion: Anopheles culicifacies (Table 2) reported double resistance, i.e. to DDT and malathion in Districts of Andhra Pradesh (Fig. 4), Chhattisgarh (Fig. 5),

aghavendra et al: Insecticide resistance in Indian malaria vectors 125 Gujarat (Fig. 3), Haryana (Fig. 1), Madhya Pradesh (Fig. 5), Odisha (Fig. 6), Uttar Pradesh (Fig. 1), Uttarakhand (Fig. 1), and West Bengal (Fig. 6). The species was resistant to DDT and malathion in district/s of Vizianagaram of Andhra Pradesh state; Dantewada, ukuma of Chhattisgarh; urat in Gujarat; Gurgaon in Haryana; Balaghat, hahdol and idhi in Madhya Pradesh; Bargarh, Bolangiri, Cuttack, Ganjam, Jagatsinghpur, Jharsuguda, Kandhamal, Khorda, Mayurbhanj and undargarh in Odisha; Allahabad in Uttar Pradesh; Nainital in Uttarakhand and from Bankura and Paschim/West Midnapur district in West Bengal state. imilarly, the urban vector An. stephensi (Table 3) was reported double resistant in Northwest Delhi (Fig. 1), North Goa ( Fig. 3), Kutch, Gujarat (Fig. 3), amanagar (Karnataka; Fig. 4) and Kolkata (West Bengal state; Fig. 6), Bikaner and Jodhpur of ajasthan (Fig. 3); An. annularis (Table 5) in District East inghbhum of Jharkhand state (Fig. 6); An. subpictus (Table 5) in the Districts Gandhinagar and Jamnagar of Gujarat (Fig. 3) and from districts Barmer and Jodhpur of ajasthan (Fig. 3). DDT -Deltamethrin: Anopheles culicifacies (Table 2) was reported double resistant to DDT and deltamethrin in District Chirang of Assam state (Fig. 2); Balrampur, urajpur and urgurja in Chhattisgarh (Fig. 5) and Dahrmapuri district in Tamil Nadu (Fig. 4). Malathion-Deltamethrin: Anopheles culicifacies (Table 2) was reported double resistant to malathion and deltamethrin in Districts of Bastar, Gariyaband, Kondagaon, Narayanpur and ajnandgaon in Chhattisgarh state (Fig. 5). An. stephensi (Table 3) exhibited double resistance in Dakshina Kannada, Karnataka state (Fig. 4). Triple resistance DDT-Malathion-Deltamethrin: Anopheles culicifacies (Table 2) were resistant to three insecticides, namely DDT-malathion-deltamethrin in East Godavari, rikakulam and Visakhapatnam districts of Andhra Pradesh state (Fig. 4); and in most of the Districts of Chhattisgarh state (Fig. 5), viz. Baloda Bazar, Bemetara, Bilaspur, Dhamtari, Durg, Jagdalpur, Janjgir-Champa, Jashpur, Kabeerdham, Kanker, Korba, Korea, Mahasamund, aigarh and aipur. Also, this species was reported triple resistant in Districts Betul, Chhindwara, Dhindori, Jhabua and Mandla in Madhya Pradesh (Fig. 5); Gajapati, Kalahandi, Koraput, Malkangiri, Nabarangpur, Nuapada and ayagada in Odisha (Fig. 6) and District Khamman in Telangana state (Fig. 4). The analysis of the susceptibility data of An. culicifacies showed single insecticide resistance to DDT in 32 districts, malathion in four and to deltamethrin in two districts. Double insecticide resistance to DDT and malathion was reported in 22 districts, DDT and deltamethrin in five districts and to malathion and deltamethrin it was reported from five districts. Triple insecticide resistance, i.e. to DDT, malathion and deltamethrin was reported from 31 districts. Anopheles culicifacies susceptibility data was reported from 105 districts from 16 states and it was found resistant to atleast one insecticide in 101 districts. Anopheles subpictus was reported triple resistant in Kutch, Gujarat (Table 5, Fig. 3). DICUION This study discusses the available data on insecticide resistance in primary and secondary vectors of malaria from 21 of the 29 states and two of the seven union territories in India, collated from different modes of data sources that yielded 62 reports and >300 susceptibility data sets (tested by standard WHO methods) between 1991 and 2016. Data were abundant for An. culicifacies owing to its wide distribution in plain areas of India and received attention being important major vector of malaria contributing about 2 /3 of malaria cases annually. The data presented in this article provides detailed susceptibility status of malaria vectors in India to different insecticides used for I programmes in India and also provides information on resistance to single insecticides (DDT/malathion/deltamethrin), double resistance (DDT+malathion/DDT+deltamethrin/ malathion+deltamethrin) and triple resistance (DDT+ malathion+deltamethrin).the data was not available systematically, in time and space but most of the data obtained was for An. culicifacies. ubstantial data were available from the states of Odisha and Chhattisgarh, followed by Madhya Pradesh, the three congruent states of India, endemic for malaria. Insecticide interventions were being used regularly in some states such as Andhra Pradesh, Chhattisgarh, Odisha, Madhya Pradesh and Northeast states; while for the other states the disease prevalence was sporadic and hence, the use of interventions was differential in time and space based on the criterion of delineating areas for intervention. The collated data included 145 districts, of which 70% (101/145) reported resistance to at least one insecticide in An. culicifacies. Anopheles culicifacies susceptibility data is reported from 105 districts of 16 states, and it was found resistant to atleast one insecticide in 101 districts. ingle insecticide resistance to DDT was reported from 32 districts, malathion from four and to deltamethrin in two districts.

126 J Vector Borne Dis 54, June 2017 Double insecticide resistance to DDT and malathion was reported in 22 districts, DDT and deltamethrin in five districts and to malathion and deltamethrin it was reported from five districts. Triple insecticide resistance, i.e. to DDT, malathion and deltamethrin was reported from 31 districts. Thus, the vector management of An. culicifacies is important for disease control as this species hypostatize the burden of insecticide resistance in malaria vectors. For effective management strategies, classified information on kinetics of development and possibility of reversal of resistance is important. uch studies are scarce but a study conducted in urat, Gujarat on the stability of insecticide resistance in An. culicifacies provide some insights 14. It was observed that DDT-malathion-resistance did not reverse completely even after long-term withdrawal of DDT (>30 yr) and malathion (9 yr) from I,while complete reversal of resistance was observed in case of deltamethrin within 23 yr of withdrawal. Further, the reversion of resistance depends on intrinsic fitness ratios of homozygotes and heterozygotes and frequency of resistance gene and the nature of inheritance of the gene 14. Anopheles culicifacies, the major vector of malaria is reported multiple resistant to insecticides of different classes. tudies on resistance mechanisms have indicated involvement of carboxylesterases for malathion resistance 17, glutathione -transferase (GT) for DDT resistance 66, monooxygenases for pyrethroid resistance. ome molecular resistance studies have shown involvement of L1014F mutation for pyrethroid resistance and L1014 for DDT resistance and frequency of the kdr gene is very low and mostly heterozygous 67. tudies so far have indicated noninvolvement of voltage gated sodium channel (VGC) gene in conferring pyrethroid resistance. Anopheles culicifacies, exists as a complex of five sibling species that are reproductively isolated and provisionally designated as A, B, C, D and E and exhibit variations in various biological aspects such as prevalence, breeding habitat preferences, vectorial capacity, host feeding preferences and insecticide susceptibility 68.The rate of development of insecticide resistance varied and it was faster in species C in areas with species B and C major sympatricity, and faster in species B in areas with species A and B sympatricity 69. The sibling species have exhibited differential susceptibility to different insecticides, therefore, insecticide spray strategy for control of An. culicifacies in stratified areas has been proposed taking into consideration, the sibling species distribution and the rate of development of resistance 69. However, the sibling species distribution could not be represented for the reported data due to non-availability, but can be logically assigned based on widespread studies undertaken in different regions in 1990s 70. uch strategies based on sibling species distribution are not being implemented in the country, as it is technically intensive and require regular monitoring of field population. For An. stephensi, a predominantly urban malaria vector, data were available from 18 districts in eight states; the species was resistant to DDT in seven districts and to malathion in three districts. The species showed double resistance to DDT and malathion in seven districts and to malathion and deltamethrin in one district. It is necessary to mention that for urban areas in India, larviciding is the only intervention measure, as per modified operational plan for vector control since 1980, and this species is targeted for I in few peri-urban areas. Presently, as a strategy for vector control in India, I is not targeted for the control of An. stephensi, except in ajasthan where this is the reported primary vector of malaria 70. The species was earlier reported resistant to DDT 4, malathion 71 and also to pyrethroids 53. For other four important primary vector species, namely An. fluviatilis, An. minimus, An. dirus and An. sundaicus, and vector species with localized or lesser importance, namely An. annularis, An. nivipes and An. subpictus, the data were available for few districts in some states. Anopheles fluviatilis, vector prevalent in hilly forested and foothill regions was reported resistant to DDT in 17 districts and to malathion in one district and was susceptible to deltamethrin. Anopheles minimus, a major vector prevalent in Northeast region is reported susceptible to DDT, malathion and deltamethrin with only one report of resistance to DDT in Eastern state of Odisha. Another primary malaria vector An. dirus, in Northeastern region (behaviourally exophilic and exophagic) is reported susceptible to all three insecticides namely, DDT, malathion and deltamethrin. Anopheles sundaicus, a coastal vector prevalent only in Andaman and Nicobar Islands is reported resistant to DDT and susceptible to malathion in Car Nicobar Island. Anopheles annularis, a secondary vector with localized importance in some Eastern states, is reported resistant to DDT in 13 districts of five states and resistant to DDT and malathion in one district in Jharkhand and was susceptible to deltamethrin. Anopheles nivipes, a vector of limited influence in Northeast states is reported resistant to DDT in two districts in Assam and was reported susceptible to malathion and deltamethrin. Anopheles subpictus, recently reported as vector of malaria from coastal region of Goa 72 was reported resistant to malathion in four districts, DDT and malathion in eight districts, malathion and deltamethrin in one district and to DDT, malathion and deltamethrin in one district. imilar to An. culicifacies, other vector species also