temporo-spatial distribution of insecticide-resistance in …back.nimr.org.in/assets/542111.pdfof...

INTRODUCTION

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 (Range 149–303 million) and 438,000 malaria deaths (Range 236,000–635,000)1. In India ~1.17 million cases and 384 deaths were reported in 20152. Absence of protective malaria vaccine, spread of parasite-resistance to antimalarial drugs and insecticide- resistance 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. Since 2010, 60 of the 78 countries that monitor insecticide resistance have report-ed mosquito resistance to at least one insecticide used in nets and indoor spraying; of these, 49 reported resistance to two or more insecticide classes1.

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, name-ly An. annularis, An. philippinensis, An. jeyporiensis and An. varuna. The most dominant mosquito species respon-sible 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 plains3. 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 ecotypes4.

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

Review Article

Temporo-spatial distribution of insecticide-resistance in Indian malaria vectors in the last quarter-century: Need for regular resistance monitoring and management

Kamaraju Raghavendra1, Poonam Sharma Velamuri1, Vaishali Verma1, Natarajan Elamathi1, Tapan Kumar Barik1-2, Rajendra Mohan Bhatt3-4 & Aditya Prasad Dash1,5

1ICMR-National Institute of Malaria Research, New Delhi; 2Department of Zoology, Berhampur University, Berhampur; 3National Institute of Malaria Research, Field Unit, RLTRI Campus, Raipur; 4Jal Sagar Apartment, College Road, Nadiad; 5Central University of Tamil Nadu, Thiruvarur, India

ABSTRACT

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

J Vector Borne Dis 54, June 2017, pp. 111–130

J Vector Borne Dis 54, June 2017112

implementing effective management strategies for vector control. The available data sets are sometimes not very useful to arrive at decision for reasons, mainly incom-plete information on insecticide susceptibility status to different insecticides in use. For their appropriate appli-cation, vector susceptibility data needs to be generated using standard protocol, which should be relatively recent and easily accessible. However, due to various adminis-trative and logistic reasons this aspect was neglected and the true status of insecticide-resistance in the malaria vec-tors in India could not be ascertained routinely. Mean-while, WHO has embarked on total elimination of malaria by 2030 and efforts have been intensified. Many coun-tries including India have launched malaria elimination programme while, few countries have already achieved it. Sensing the importance of insecticide resistance for malaria control and its elimination, WHO has suggested a Global Plan for Insecticide Resistance Management (GPIRM)5 that can be followed for resistance manage-ment at country level, which also provides technical advocacy.

Until recently, there was no consolidation of histori-cal and up-to-date information on insecticide-resistance in malaria vectors in India. This review is an effort to pro-vide an updated report on the status of insecticide-resis-tance among the major malaria vectors in India based on the information available in last 25 yr drawn from vari-ous 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 insec-ticide-resistance with respect to different malaria vector species in India.

Insecticide resistance database A data base was collated through search of the pub-

lished peer-reviewed literature including PubMed/Co-chrane 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. Ma-jor keywords used for the search were Anopheles, insec-ticide, 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 Internation-al Health, American Journal of Tropical Medicine and Hygiene, Transactions of the Royal Society of Tropical Medicine and Hygiene, Journal of Vector Ecology, Jour-nal of Vector Borne Diseases (formerly Indian Journal of Malariology), Journal of Communicable Diseases, In-

dian Journal of Medical Research, Current Science, Jour-nal of Biosciences, Parasitology Research, South East Asian Journal of Tropical Medicine and Public Health, Acta Tropica, etc.

The search exercise was completed for all the ad-ministrative 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 institu-tional publications from the Indian Council of Medical Research (ICMR) institutes dealing with vector control, like the National Institute of Malaria Research (formerly, Malaria Research Centre), Vector Control Research Cen-tre, as well as other government research organizations. Since, the data contained information retrieved from pub-lished/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 suscepti-bility and resistance were : >98% mortality—Susceptible, >90 and < 98% mortality—Possible resistance/verifica-tion required, and <90% mortality—Resistant6; where mortality rates were reported in range format; the average of the highest and lowest values was used to assign suscep-tibility status. The locations could not be linked to the GPS coordinates as most of the available data was retrospec-tive 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, heterozygos-ity in the data, information in the sample size and dosages, etc. Such 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 non-prescribed diagnostic dosages of insecticides or specified number of mosquitoes, etc. Such 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) Spellings of locality; (ii) Information in the data fields; (iii) Homonyms among the localities; and (iv) Recent identification of the locations with respective administrative states that are bifurcated in the recent years (recently created districts). The infor-mation for the data sets included, name of state, name of district (with specified locality/village where available), period of mosquito collection, insecticide-wise percent-age mortality, dosages tested (e.g. DDT 4%, malathion

113

5%, deltamethrin 0.05%), number of mosquitoes exposed for test (n), susceptibility status [susceptible (S), possible resistance (designated as VR, verification required) and resistance (R)] categorized as per the WHO guidelines6.

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 de-picted in the form of pie chart with three different colour codes: Green for S, yellow for VR and red for confirmed R. 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 susceptibil-ity 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. Recently An. subpictus has been implicated to be a domi-nant vector in urban areas of Goa state. The compiled data, pertain to 145 districts from 21 states and two union ter-ritories 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 respon-sible for annual transmission of about two-thirds of total malaria cases.

For convenience of the data reporting, the geogra-phical area of India was divided into six zones, namely

North, South, East, West, Central and Northeast Zones comprising 29 states and seven union territories as de-picted in Table 1.

Insecticide susceptibility in malaria vectors

Single resistanceDDT: Resistance to DDT in An. culicifacies (Table 2)

was reported to be widespread in India except in Rithala, Northwest Delhi (Fig. 1) in 1991, where it was reported in VR 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 Rajasthan (Fig. 3). The species was reported sus-ceptible to DDT in Dakshina Kannada (Fig. 4) and under VR category in Jaisalmer, Rajasthan (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 Uttara-khand (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, Raya-gada, Sambalpur and Sundargarh of Odisha state (Fig. 6)

Table 1. Zonal distribution of India with prevalent vector species in each zone

S. No.

Zones States (Districts surveyed/Total no. of districts) Malaria vectorsPrimary Secondary

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)

An. culicifacies, An. fluviatilis and An. stephensi

An. subpictus

2. South 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)

An. culicifacies, An. fluviatilis, An. stephensi and An. sundaicus

3. East Zone Bihar ( 0/38), Jharkhand (8/24), Odisha (22/30), and West Bengal (5/20)

An. annularis, An. culicifacies, An. fluviatilis, An. minimus and An. stephensi

An. nivipes (philippinensis)

4. West Zone Goa (1/2), Gujarat (4/26), Rajasthan (6/33) and Maharashtra (2/35)

An. annularis, An. culicifacies,An. fluviatilis, An. stephensi andAn. subpictus

5. Central Zone Chhattisgarh (28/28), Madhya Pradesh (15/50) An. culicifacies and An. fluviatilis6. Northeast

ZoneArunachal Pradesh ( 0/20), Assam (16/33), Manipur ( 0/9), Meghalaya (2/11), Mizoram (0/8), Nagaland (0/11), Sikkim (0/4) and Tripura (3/8)

An. annularis, An. culicifacies, An. dirus and An minimus

An. nivipes (philippinensis)

Raghavendra et al: Insecticide resistance in Indian malaria vectors


Table 2. Insecticide susceptibility status on Anopheles culicifacies in different states of India

S.No.

State District (Location) Year Percentage mortality (n) and susceptibility status ReferenceDDT (4%) Status Malathion (5%) Status Deltamethrin (0.05%) Status

1. Andhra Pradesh

East Godavari 2009 36.6 (60) R 80 (60) R 70 (60) R 7Srikakulam 0 (21a) R 44.4 (135) R 77.7 (72) RVisakhapatanam 6.6 (15a) R 46.6 (15a) R 73.6 (19a) RVizianagaram 0 (17a) R 32.2 (62) R 93.3 (15a) VRVisakhapatanam (Allamput) 1999 40b R b S b S 8

2. Assam Chirang/Chirag 2009 25 (8a) R – – 30 (7a) R Raghavendra (Unpublished)Dhemaji, Lakhimpur 70 (40a) R – – – –

Dibrugarh (Sonitpur– Gorubandh)

1995 b S – – – – 9

Nalbari b S – – – – 103. Chhattis-

garhBaloda Bazar 2016 4.9 (101) R 60.9 (105) R 75.8 (112) R Bhatt

(Unpublished)Bemetara 3 (100) R 60.1 (103) R 82.6 (104) RDurg 4.5 (110) R 72.9 (111) R 70.5 (102) RJanjgir-Champa 14.2 (105) R 53 (83) R 64.1 (106) RKabirdham/Kabeerdham (Formerly Kawardha)

2.9 (102) R 60 (100) R 80.3 (102) R

Bastar 2015 – – 63.4 (112) R 77.3 (110) RBijapur 1 (100) R – – – –Bilaspur – – 67.5 (111) R 65.7 (105) RDantewada 0 (70) R 65 (20a) R – –Dhamtari – – 73.5 (132) R 61.2 (103) RGariyaband/Gariaband – – 67 (103) R 45 (100) RKanker – – 63.9 (111) R – –Kondagaon – – 54.3 (105) R 79.9 (105) RKorba – – – – 57.7 (109) RMahasamund – – 70.1 (104) R 30 (100) RMungeli – – – – 81 (100) RNarayanpur – – 81.8 (110) R 56.9 (105) RRaigarh 4 (126) R – – 75 (124) RRaipur 0 (100) R – – 26.5 (102) RRajnandgaon – – 35 (100) R 62.6 (127) RSukma 2.5 (80) R 73.3 (60) R – –Balod 2014 – – – – 60 (60) RBalrampur 5 (101) R – – 88.8 (107) RKanker – – – – 82.7 (98) RKoriya/Korea 10 (100) R – – 72.9 (107 RSurajpur 7.3 (109) R – – 87.9 (107) RSurguja 14 (100) R – – 85.3 (102) RBilaspur, Korba, Korea 2009 33.7 (95) R 42 (108) R 80.5 (118) R 11Dantewada 9.8 (82) R 55.3 (85) R 98.7 (96) SDhamtari, Raipur 4 (99) R 73.5 (98) R 78.6 (98) RJagdalpur 21 (100) R 39.4 (100) R 77 (100) RJashpur, Raigarh 10 (60) R 42.4 (66) R 68 (75) RKanker 3.2 (186) R 69.4 (216) R 83.3 (190) RJagdalpur 2002 – – 83.8 (40a) R 90.4 (46a) VR 12Kanker 22.9 (40a) R 74.1 (43a) R 89.4 (45a) RMahasamund 25 (78) R 87.9 (36a) R 89.5 (40a) RRaigarh 13.8 (79) R 59.3 (65) R 92.5 (40a) VR

4. Delhi Northwest Delhi(Mukundpur/Mukunpur)

1989–1991c

53.3 (15a) R 100 (15a) S 100 (15a) S 13

contd...

115

S.No.


Northwest Delhi (Rithala) 90 (10a) VR 100 (10a) S 100 (10a) S5. Gujarat Surat 2006 20 (168) R 57 (220) R 99 (190) S 14

Surat 2005 40 (66) R 68 (145) R 98 (62) SSurat 2001 9 (192) R – – 66 (322) RSurat 2001 – – – – 60–78b R 15Surat (Gangapore) 13.1 (74) R – – 60.4 (106) RSurat (Kakrapara) 6.7 (60) R – – 78.3 (106) RSurat (Limbi) 6.9 (58) R – – 61.3 (109) RSurat (Nidwada) – – – – 69.2 (117) RSurat 1993 8.8–22b R 11.11b R – – 16Surat 1992 6 (100) R 17 (60) R – – 17

6. Haryana Gurgaon (Mewat) 1997 – – – – 100 (45a) S 18Sonepat – – – – 100 (45a) SGurgaon (Prataphas) 1996 – – 78 (50a) R – – 19Gurgaon (Salamba) 73 (30a) R 87.9 (133) R 100 (30a) SGurgaon (Tekri) 45.9 (61) R 79.3 (92) R 100 (147) SGurgaon (Sirsa) 1994 b R b R – – 20Karnal (Gharaunda) – – 85 (34a) R – –Karnal (Kaiwala) – – 88 (35a) R – –Punchkula (Pinjore) – – 75 (30a) R – –Yamuna Nagar (Todarpur) – – 65 (26a) R – –

7. Jharkhand(Divided out of Bihar in 2000)

Koderma 2010 37.8 (180) R 98.3 (180) S 100 (180) S 21East Singhbhum 2009 23.7 (140) R 95.1 (110) VR 100 (120) S 7Gumla 26.3 (227) R 96.9 (152) VR 99.0 (191) SRanchi 10.4 (320) R 98.1 (170) S 98.1 (210) SWest Singhbhum 15.8 (180) R 98 (170) S 100 (160) SGumla 2007 38.4 (664) R 95.4 (611) VR 98.8 (566) S 22Hazaribagh 1992 37.5e (60) R 94.6e (60) VR – – 23

8. Karnataka Tumkur 2005 – – 97 (60) VR – – 249. Madhya

PradeshAnuppur 2012 33 (15–20a) R 100 (15–20a) S – – 25Chhindwara 54 (15–20a) R 80 (15–20a) R – –Dhindori/Dindori 26 (15–20a) R 100 (15–20a) S – –Katni 55 (15–20a) R 95 (15–20a) VR – –Mandla 50 (15–20a) R 100 (15–20a) S – –Narsinghpur/Narsingpur 30 (15-20a) R 100 (15–20a) S – –Satna 35 (15–20a) R 100 (15–20a) S – –Seoni 50 (15–20a) R 95 (15–20a) VR – –Umaria 40 (15–20a) R 100 (15–20a) S – –Balaghat 2009 6.7 (120) R 84 (150) R 92 (150) VR 26Betul 12.4 (225) R 72.4 (225) R 83.1 (225) RChhindwara 9.2 (315) R 74.9 (315) R 85.9 (315) RDhindori/Dindori 12.8 (180) R 80 (180) R 71.6 (180) RGuna 26.6 (300) R 100 (300) S 100 (270) SJhabua/Jhabula 6.6 (240) R 65.4 (240) R 87 (240) RMandla 13.3 (180) R 78.3 (180) R 76.6 (180) RShahdol 8.8 (180) R 77.8 (180) R 93.8 (180) VRSidhi 7.5 (360) R 78.8 (360) R 94.1 (360) VR

10. Maha-rashtra

Gadchiroli (Murumgaon) 2010 23.2 (100) R 96 (100) VR 94 (100) VR 27Gadchiroli (Malanda, Maveli, Chavela)

2001 51 (45) R 92.9 (33) VR 100 (60) S 28

contd...

Table 2 (Contd.)



Table 2 (Contd.)

S.No.


11. Odisha Kalahandi 2014 12.4 (105) R 60.4 (111) R 79.4 (131) R 29Koraput 15.3 (111) R 66.7 (111) R 76.8 (112) RMalkangiri 12.6 (111) R 76.2 (105) R 84.0 (119) RNabarangpur/Nawaranghpur 11.4 (105 R 70.9 (110) R 72.6 (113) RRayagada 12.6 (135) R 63.1 (130) R 81.7 (131) RBalangir/Bolangir 2010 12.3 (106) R 80 (105) R 94.2 (104) VR 30Gajapati 15.5 (103) R 83.8 (105) R 82.9 (105) RGanjam 14.7 (102) R 70.3 (101) R 95.2 (104) VRKalahandi 14.3 (105) R 86.7 (105) R 81.7 (104) RKandhamal 9.5 (105) R 77.6 (109) R 96.3 (109) VRKoraput 13.5 (111) R 76.6 (111) R 98.4 (123) SMalkangiri 15.2 (105) R 75.5 (110) R 86.2 (109) RNabarangpur/Nawaranghpur 13.8 (109) R 63.5 (126) R 96.5 (114) VRNuapada 15 (107) R 67.3 (98) R 100 (89) SRayagada 16.7 (102) R 77.6 (105) R 89.8 (108) RAngul 2009 9.7 (80) R 100 (40a) S 96.3 (30a) VR 7Bargarh/Baragarh 12.5 (300) R 72.3 (280) R 98.8 (340) SBalangir/Bolangir 7.8 (502) R 74.4 (511) R 96.0 (494) VRCuttack 20 (100) R 74 (90) R 100 (90) SDhenkanal, Subarnapur/Sonepur

9.3 (30a) R 100 (20a) S 100 (20a) S

Gajapati 12.6 (300) R 70.3 (280) R 98 (280) SGanjam 18.4 (30a) R 85 (20a) R 100 (30a) SJagatsinghpur 23 (100) R 85.5 (80) R 100 (90) SJharsuguda 12.6 (260) R 40.0 (240) R 96.7 (240) VRKalahandi 11.8 (76) R 78.3 (120) R 81.6 (120) RKendujhar/Keonjhar 11.1 (40a) R 100 (30a) S 100 (20a) SKhordha/Khurda 20 (20a) R 80 (20a) R 100 (30a) SMayurbhanj, Sambalpur 14.8 (30a) R 100 (20a) S 96.3 (27a) VRNuapada 3.3 (60) R 93.8 (49a) VR 88.1 (59a) RKandhamal (Phulbani) 6.4 (93) R 59.1 (98) R 93.7 (96) VRRayagada 23.1 (272) R 90.6 (278) VR 89.2 (270) RSundargarh 25.9 (280) R 70.7 (260) R 95.1 (260) VRSundargarh 2008 b R b S – – 31Gajapati (Guma) 2005 20 (15a) R – – 100 (15a) S Hazra

(Unpublished)Gajapati (Mohana) 26.6 (15a) R – – 100 (15a) SMayurbhanj (Badampahar, Rangamatia)

20 (15a) R – – 100 (15a) S

Nabarangpur (Nandahandi) 20 (15a) R – – 100 (15a) SNabarangpur (Papadahandi) 26.6 (15a) R – – 100 (15a) SNabarangpur (Tentulikhunti) 20 (15a) R – – 100 (15a) SRayagada (Bisamcuttack) 26.6 (15a) R – – 100 (15a) SRayagada (Muniguda) 13.3 (15a) R – – 100 (15a) SBalangir/Bolangir 2002 23.3 (60) R 68.3 (60) R 95 (60) VR 32Kalahandi 12 (60) R 88.3 (60) R 96.7 (60) VRKendujhar/Keonjhar 14 (50a) R – – 100 (80) SMayurbhanj 62.5 (40a) R 50 (40a) R 100 (60) SNuapada 8.3 (60) R 75 (60) R 81.7 (60) RKandhamal (Phulbani) 20 (60) R 100 (60) S 100 (60) SRayagada 15 (60) R 100 (60) S 100 (60) SSundargarh 12 (100) R 100(100) S 100 (100) SKoraput 21.2 (33) R – – – – 33Malkangiri 21.1 (90) R 35.3 (102) R 100 (51) SMalkangiri 1993 0–10 (925) R – – – – 34

contd...

117

S.No.


12. Rajasthan Jaisalmer 1999 b VR b S – – 35Jaisalmer (Pokaran) 1995 30 (10a) R 100 (10a) S – – 36Bikaner 1993 60.6 (94) R 98.6 (81) S – – 37

13. Tamil Nadu

Dharmapuri 2006 46.6 (60) R 100 (45a) S 73.3 (60) R 24Ramanathapuram 83.3 (180) R 100 (180) S 100 (180) SRamanathapuram (Rameshwaram)

1997 – – – – 100 (45a) S 18

14. Telangana Khammam 2009 23.3 (60) R 63.3 (60) R 43.3 (60) R 715. Uttar

PradeshMoradabad 2002d 42.5b R – – – – 38Gautam Buddh Nagar 2008 20b R b S b S 39Gautam Buddh Nagar[Delhi (Yamuna River)]

2006 26-45b R 100b S 100b S 40

Gautam Buddh Nagar (Noida) 26-45b R 100b S 100b SBareilly/Bareeily 2002 21.4 (40) R – – – – 41Bareilly/Bareeily 2001 15.5 (110) R – – – – Raghavendra

(Unpublished)Bahraich 1999 7.3 (60) R – – 100b (15 min) S 42Allahabad 1996 b R b R – 43

16. Uttara-khand

Haldwani (Nainital) 2002d – – 86.2b R 100b S 44Hardwar 2001 – – 80–90 (200) R – – Raghavendra

(Unpublished)Nainital (Formerly in UP) 1997 1.1 (90) R – – 100 (30a) S 45

17. West Bengal

Bankura, Paschim/West Medinipur (Midnapur)

2009 3.3 (60) R 88.3 (60) R 100 (40a) S 7

Birbhum, Purulia 6.6 (75) R 90.8 (65) VR 100 (45a) San <60; bPercentage mortality data not available; cFinal year considered as the collection year; dReported year considered as the collection year; eOne hour exposed data; f30 min exposure time; (–) Not reported; R—Confirmed resistance; VR—Possible resistance; S—Susceptible.

Fig. 1: Temporo-spatial distribution of insecticide susceptibility sta-tus of malaria vectors in the States 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 States of Assam, Tripura and Meghalaya of Northeast Zone, India.

Table 2 (Contd.)



Table 3. Insecticide susceptibility status of An. stephensi in different states of India

S. No.

State District (Location) Year Percentage mortality (n) ReferenceDDT (4%) Status Malathion

(5%)Status Deltamethrin

(0.05%)Status

1. Delhi Northwest Delhi(Jatkhore/Jatkhar)

1989–1991

46.6 (15a) R 66.6 (15a) R 100 (15a) S 13

Northwest Delhi (Madanpur)

86.6 (15a) R 93.3 (15a) VR 100 (15a) S

Northwest Delhi (Rithala)

22.2 (45a) R 43.3 (30a) R 100 (15a) S

2. Goa North Goa (Panaji) 1991 10 (100) R 26 (100) R – – 463. Gujarat Kutch (Bhuj) 2007 68.4 (20–40a) R 38.5 (20–40a) R 100 (20–40a) S 47

Jamnagar – – 95.4 (20–40a) VR 90 (20–40a) VRGandhinagar 2005 – – 77.2 (20–40a) R 100 (20–40a) SJamnagar – – 76 (20–40a) R 100 (20–40a) SSurat 2000 – – 51.7b R 93.3b VR 48

4. Karnataka Dakshina Kannada (Mangalore)

2006 98.1 (60) S 54.9 (106) R 86.1 (72) R 49

Bengaluru Rural(Dasarahalli)

1992d 50b R 100b S – – 50

Bengaluru Rural (Talaghattapura)

40b R 100b S – –

Bengaluru Urban (Koramangala)

50b R 100b S – –

Urban (Mathikere) 80b R 100b S – –Bengaluru Urban(Wilson Garden)

45b R 100b S – –

Ramanagar (Kanakapura)

40b R 80b R – –

Tumkur 40b R 100b S – –5. Rajasthan Bikaner 2007 – – 77.3 (20–40a) R – – 47

Jodhpur 71.8 (20–40a) R 94.7 (20–40a) VR 100 (20–40a) SBarmer 2006 59.9 (20–40a) R 100 (20–40a) S – –Jodhpur – – 72 (20–40a) R 92.9 (20–40a) VRBarmer 2005 – – 100 (20–40a) S – –Bikaner – – 66.6 (20–40a) R 100 (20–40a) SGanganagar(Sri Ganganagar)

– – 95.4 (20–40a) VR 94.1 (20–40a) VR

Jaisalmer 1999 b VR b S – – 35Jodhpur 1995 30–40b R 100b S – – 51Barmer b R b VR – – 52Jodhpur b R b VR – –Pali b R b VR – –Bikaner 1993 40 (85) R 91.3 (103) VR – – 37

6. Maha- rashtra

Pune/Poone 1992d 50b R 100b S – – 50

7. Uttar Pradesh

Gautam Buddh Nagar [Delhi (Yamuna River)]

2006 26–45b R 100b S 100b S 40

Gautam Buddh Nagar (Noida)

26–45b R 100b S 100b S

8. West Bengal

Kolkata 1998 80 (100) R 80 (100) R – – 531995 55 (60) R – – 100f (60) S 54

an <60; bPercentage mortality data not available; cFinal year considered as the collection year; dReported year considered as the collection year; eOne hour exposed data; f30 min exposure time; (–) Not reported; R—Confirmed resistance; VR—Possible resistance; S—Susceptible.

119

Fig. 3: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the States of Rajasthan, Gujarat, Maharashtra and Goa of West Zone, India.

Fig. 4: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the States of Telangana, Andhra Pradesh, Tamil Nadu, Karnataka and Andaman & Nicobar Islands of South Zone, India.

Fig. 5: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the States of Madhya Pradesh and Chhattisgarh of Central Zone, India.

Fig. 6: Temporo-spatial distribution of insecticide susceptibility status of malaria vectors in the States of Jharkhand, West Bengal and Odisha of East Zone, India.



Table 4. Insecticide susceptibility status of An. fluviatilis in different states of India

S. No.

State District Year Percentage mortality (n) Reference

DDT (4%) Status Malathion (5%)

Status Deltamethrin (0.05%)

Status

1. Andhra Pradesh

Visakhapatanam (Allamput)

1999 b S b S b S 8

2. Chhattisgarh Jashpur 2015 13.3 (105) R – – 100 (104) S Bhatt (Unpublished)

Raigarh 2009 50 (28a) R – – – – Raghavendra (Unpublished)

3. Himachal Pradesh

Una 1997 b R b S 43

4. Jharkhand(Divided out of Bihar in 2000)

Koderma 2010 64.03 (120) R 100 (118) S 100 (120) S 21

East Singhbhum 2009 76.2 (130) R 99.3 (110) S 100 (110) S Raghavendra (Unpublished)

Gumla 80.3 (240) R 100 (186) S 100 (172) S

Ranchi 80.8 (180) R 97.3 (135) VR 100 (120) S

West Singhbhum 78.2 (180) R 98.6 (165) S 100 (170) S

Gumla 2007 67.7 (619) R 100 (542) S 100 (438) S 22

Dhanbad 1997 b R b S – – 43

Hazaribagh 1992 96.4e (60) VR 100e (60) S – – 23

5. Karnataka Bangalore/Bengaluru 1997 b R b S – – 43

Belgaum b R b S – –

Bijapur b R b S – –

Kolar b R b S – –

Shimoga b R b S – –

6. Maharashtra Gadchiroli (Murumgaon) 2010 36.6 (60) R 95 (60) VR 96.4 (60) VR 27

7. Odisha Rayagada 2013 100 (100) S – – 100 (100) S 55

Balangir/Bolangir 2010 100 (56a) S 100 (54a) S 100 (54a) S 30

Gajapati 100 (62) S 100 (61) S 100 (57a) S

Ganjam 100 (50a) S 100 (52a) S 100 (52a) S

Kalahandi 100 (79) S 100 (62) S 100 (79) S

Kandhamal 100 (60) S 100 (64) S 100 (63) S

Koraput 100 (55a) S 100 (66) S 100 (55a) SMalkangiri 100 (67) S 100 (44a) S 100 (56a) S

Nabarangpur/Nawaranghpur 100 (32a) S 100 (20a) S 100 (24a) S

Nuapada 100 (54a) S 100 (54a) S 100 (58a) S

Rayagada 100 (60) S 100 (57a) S 100 (58a) S

Angul 2009 100 (8a) S – – – – Raghavendra (Unpublished)

Kendujhar/Keonjhar 100 (6a) S – – – –

Kendujhar/Keonjhar (Banspal)

100 (52a) S – – 100 (52a) S 56

Sambalpur, Mayurbhanj 100 (20a) S – – – – Raghavendra (Unpublished)

Sundargarh/Sundergarh 2008 b S b S – – 31

Kalahandi 2002 100 (60) S 100 (60) S 100 (60) S 32

Koraput 100 (557) S 100 (210) S 100 (290) S 33

Kendujhar/Keonjhar 100 (100) S 100 (40a) S 100 (120) S 32

Malkangiri 100 (493) S 100 (192) S 100 (108) S 33

contd...

121

S. No.

State District Year Percentage mortality (n) Reference



Status

Mayurbhanj 95.0 (40a) VR 87.5 (40a) R 100 (40a) S 32

Kandhamal (Phulbani) 100 (60) S 100 (40a) S 100 (40a) S

Sundargarh/Sundergarh 100 (100) S 100 (60) S 100 (100) S

2001 100b S 100b S 100b S 482000 100b S – – 100b S

Malkangiri 1993 100 (260) S – – – – 348. Tamil Nadu Coimbatore 1997 b R b S – – 43

9. Uttarakhand Nainital (Formerly in UP) 1997 21.6 (85) R – – 100 (70) S 45


Table 4 (Contd.)

and under VR category from Hazaribagh, Jharkhand (Fig. 6) in 1992. The species was resistant to DDT in the districts Jashpur and Raigarh of Chhattisgarh state (Fig. 5); Una in Himachal Pradesh (Fig. 1); Dhanbad, East Singhbhum, Koderma, Gumla, Ranchi and West Singh-bhum in Jharkhand (Fig. 6); Belgaum, Bengaluru, Bija-pur, Kolar and Shimoga, 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 second-ary 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, Hazarib-agh, Koderma, Ranchi and West Singhbhum of Jharkhand state (Fig. 6); Gadchiroli of Maharashtra state (Fig. 3); Gajapati, Nabarangpur, Rayagada and Sundergarh, Districts of Odisha state (Fig. 6) and Bikaner district of Rajasthan state (Fig. 3) except in Sahibganj 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 re-ported from Districts of Assam, Jharkhand, Meghalaya, Odisha and Tripura. The species was reported resistant to DDT from Kendujhar, Odisha (Fig. 6) in 2003, pos-sible resistance in the Districts of Kamrup, Kamrup Met-ropolitan and Sonitpur districts of Assam (Fig. 2) in 2002; Kendujhar of Odisha (Fig. 6) in 2009 and South 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 State of Assam (Fig. 2); Sahibganj from the State 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 Sibsagar and Dibrugarh of Assam (Fig. 2) in 1998, possible resistance in South Tripura (Fig. 2) in 2007 and susceptible in district Sahibganj, Jharkhand (Fig. 6) in 1998. Anopheles sundaicus (Table 4), a primary vector in Andaman and Nicobar Islands was reported re-sistant to DDT in Car Nicobar Island (Fig. 4) in 1989–91.

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 Singhbhum, Gumla and Hazaribagh of Jharkhand state (Fig. 6); Tumkur of Karnataka (Fig. 4); Katni and Seoni of Madhya Pradesh (Fig. 5); Gadchi-roli from Maharashtra (Fig. 3); Nuapada and Rayagada of Odisha (Fig. 6) and Districts Birbhum and Purulia of West Bengal state (Fig. 6).

Anopheles culicifacies was reported susceptible to malathion in village Rithala of Northwest Delhi (Fig. 1); Districts Koderma, Ranchi, West Singhbhum of Jharkhand state (Fig. 6); Anuppur, Dhindori, Guna, Man-dla, Narsinghpur, Satna, Umaria of Madhya Pradesh (Fig. 5); Angul, Dhenkanal, Kandhamal, Kendujhar, Mayurb-hanj, Sambalpur, Subarnapur, Sundargarh of Odisha (Fig. 6); Jaisalmer and Bikaner of Rajasthan (Fig. 3); Dhara-mapuri and Ramanathapuram 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 dis-tricts in Karnataka (Fig. 6) resistant in Mangalore and



Table 5. Insecticide susceptibility status of other anophelines in different states of India

S.No.

Species State District Year Percentage mortality (n) Reference



Status

1. An. annularis

Assam Kamrup(Chandubi Area– Kasi Hills)

2011 28.3 (60) R – – 97.7 (43a) VR 57

Kamrup(Rani Area– Kasi Hills)

11.9 (43a) R – – 98.1 (54a) S

Baksa (Tamulpur) 1995 82b R – – – – 10

Jharkhand(Divided out of Bihar in 2000)

Koderma 2010 40.35 (180) R 100 (180) S 99.44 (180) S 21

East Singhbhum 2009 23.0 (160) R 84.3 (110) R 100 (120) S Raghavendra (Unpublished)

Gumla 41.7 (180) R 98.4 (180) S 100 (100) S

Ranchi 29.8 (180) R 100 (170) S 100 (160) S

West Singhbhum 14.8 (180) R 94.7 (150) VR 99.3 (160) S

Gumla 2007 45.9 (335) R 97.7(438) VR 100 (360) S 22

Sahibganj (Rajmahal)

1998 100f (8a) S 100f (5a) S – – 58

Hazaribagh 1992 13.1e (60) R 100e (60) S – – 23

Maharashtra Gadchiroli (Murumgaon)

2010 21 (100) R 90.5 (100) VR 95 (100) VR 27

Odisha Sundargarh 2000 5.8b R – – 100b S 48

Gajapati (Guma) 2005 13.3 (15a) R – – – – Hazra (Unpublished)

Nabarangpur (Papadahandi)

13.3 (15a) R – – – –

Rayagada (Muniguda)

20.0 (15a) R – – – –

Rajasthan Bikaner 1993 36.2 (102) R 94.6 (92) VR – – 37

2. An. dirus Assam Dibrugarh 1997 100 (36a) S 100 (30a) S – – 59

3. An. minimus

Assam Chirang/Chirag 2009 100 (06a) S – – – – Raghavendra (Unpublished)

Goalpara and Dhubri

100 (176) S 100 (96) S 100 (90) S

Lakhimpur and Dhemaji

100 (40a) S 100 (10a) S 100 (10a) S

Udalguri 100 (02a) S – – – –

Darrang/Darang, Udalguri

2002 98.3 (60) S – – 100 (40a) S 60

Kamrup,Kamrup Metropoli-tan (Sonapur)

96.3 (80) VR – – 100 (60) S

Sonitpur (Balipara) 97.5 (80) VR – – 100 (40a) S

Morigaon 1999 100b S 100b S – – 61

Nagaon 1995 100 (40a) S 100 (40a) S – – 62

Nalbari b S 10

Dibrugarh (Sonit-pur-Gorubandh)

b S – – – – 9



1998 100f (30a) S 100f (26a) S – – 58

contd...

123

S.No.

Species State District Year Percentage mortality (n) Reference



Status

Meghalaya East & West Garo Hills

2009 100 (06a) S – – – – Raghavendra (Unpublished)

Odisha Kendujhar/Keonjhar (Banspal)

2009 96.2 (52a) VR 100 (52a) S 56

Kendujhar/Keonjhar 2003 86 (21a) R 100 (45a) S 63

Tripura Dhalai, West and South Tripura

2009 100 (10a) S – – – – Raghavendra (Unpublished)

South Tripura (Belonia)

2007 92.9 (30a) VR – – 100 (30a) S 64

4. An. nivipes (philip-pinensis)

Assam Chirang/Chirag 2009 – – 100 (7a) S – – Raghavendra (Unpublished)

Sivasagar/Sib Sagar and Dibrugarh

1998 b R – – – – 43



1998 100 (17a) S 100 (16a) S – – 58

Tripura Dhalai, West and South Tripura

2009 – – 100 (10a) S – – Raghavendra (Unpublished)

Tripura South Tripura (Belonia)

2007 96.6 (30a) VR – – 100 (30a) S 64

5. An. subpictus

Gujarat Kutch (Bhuj) 2007 57.1 (20–40a)

R 39.4 (20–40a) R 87.5 (20–40a) R 47

Gandhinagar 66.7 (20–40a)

R 44 (20–40a) R 100 (20–40a) S

Jamnagar 40.6 (20–40a)

R 50 (20–40a) R 100 (20–40a) S

Gandhinagar 2006 40.62b R 75 (20–40a) R 100 (20–40a) S

Jamnagar 46.15b R – – – –

Gandhinagar 2005 – – 40.6 (20–40a) R 100 (20–40a) S

Jamnagar – – 55 (20–40a) R 92 (20–40a) VR

Punjab Bathinda 2004 – – 89.4 (20–40a) R 90 (20–40a) VR

Rajasthan Barmer 2006 70.8 (20–40a)

R 36 (20–40a) R 100 (20–40a) S

Jodhpur 50 (20–40a) R 40.6 (20–40a) R 100 (20–40a) S

Barmer 2005 52b R 96.2 (20–40a) VR 90 (20–40a) VR

Jodhpur – – 64.3 (20–40a) R 88.2 (20–40a) R

Bikaner 2004 – – 37.5 (20–40a) R 92.3 (20–40a) VR

Ganganagar(Sri Ganganagar)

– – 64.3 (20–40a) R 100 (20–40a) S

Bikaner 1993 21.4 (103) R 100 (63) S – – 37

6. An. sundaicus

Andaman and Nicobar Islands

Car Nicobar Island (Kimios, Kakana, Sawai and Malaka)

1989–1991c

87.7 R 99 S – – 65


Table 5 (Contd.)

Ramanagar. It was variable resistant in Districts of Raj-asthan (Fig. 3) and mostly in the verification required cat-egory and the species reported resistant in District Jodh-pur. 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 re-sistant in Kolkata in West Bengal (Fig. 6).

Anopheles fluviatilis (Table 4) was reported sus-



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 Ranchi in Jharkhand, Gadchiroli in Maharashtra and District May-urbhanj in Odisha, where the species was reported under VR category.

Anopheles annularis (Table 5) was reported resistant to malathion in the States of Jharkhand (Fig. 6), Maha-rashtra (Fig. 3), Odisha (Fig. 6) and Rajasthan (Fig. 3) and was mostly susceptible to malathion with emerging possible resistance in few Districts of Jharkhand, Maha-rashtra and Rajasthan. The species was reported resistant in District East Singhbhum and under VR category in West Singhbhum and Gumla of Jharkhand; Gadchiroli in Maharashtra and from District Bikaner in Rajasthan state.

Anopheles dirus, prevalent in Northeast state was re-ported 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 Dis-tricts Goalpara, Dhubri, Lakhimpur, Dhemaji, Morigaon and Nagaon in Assam (Table 5, Fig. 2) and from Sahib-ganj 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), Sahibganj in Jharkhand (Fig. 6) and in Districts Dhalai, West and South Tripura in Tripura state (Fig. 2).

An. sundaicus prevalent in Andaman and Nicobar Is-lands, was reported susceptible to malathion in Car Nico-bar 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, Gandhi-nagar and Jamnagar in Gujarat (Fig. 3); Bhatinda in Pun-jab (Fig. 1) and in Districts Barmer, Jodhpur, Bikaner and Ganganagar in Rajasthan (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), Chhat-tisgarh (Fig. 5), Delhi (Fig. 1), Haryana (Fig. 1), Gujarat (Fig. 3), Jharkhand (Fig. 6), Madhya Pradesh (Fig. 5), Ma-harashtra (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, Sri-kakulam and Visakhapatnam of Andhra Pradesh; Chirang

in Assam; Balod and Mungeli districts of Chhattisgarh; Betul, Chhindwara, Dhindori, Jhabua and Mandla in Mad-hya Pradesh; Gajapati, Kalahandi, Koraput, Malakangiri, Nabarangpur, Rayagada in Odisha; Dharmapuri in Tamil Nadu and district Khammam in Telangana state. Possible resistance was reported from district Vizianagaram of Andhra Pradesh; Balaghat, Shahdol and Sidhi in Madhya Pradesh; Gadchiroli in Maharashtra; Angul, Bolangir, Ganjam, Jharsuguda, Kandhamal, Mayurbhanj, Sambal-pur and Sundargarh in Odisha state. This species was re-ported susceptible to deltamethrin in Northwest Delhi in the National Capital Region of Delhi; District Gurgaon and Sonepat in Haryana; East Singhbhum, Gumla, Ko-derma, Ranchi, West Singhbhum in Jharkhand; Guna in Madhya Pradesh; Bargarh, Cuttack, Dhenkanal, Ganjam, Jagatsinghpur, Kendujhar, Khordha, and Subarnapur in Odisha; Ramanathapuram in Tamil Nadu; Bahraich and Gautam Buddh Nagar in Uttar Pradesh; Nainital in Ut-tarakhand and from District Bankura, Birbhum, Paschim/West Midnapur and Purulia in West Bengal state. Howev-er, the species showed reversion of deltamethrin resistance in District Surat, Gujarat after three years of its withdrawal from indoor residual spray (IRS) in the year 20057.

Anopheles stephensi (Table 3) was reported resistant to deltamethrin in district Dakshina Kannada of Karna-taka (Fig. 4). The species was susceptible in Northwest Delhi (Fig. 1), Districts Kutch and Gandhinagar in Guja-rat (Fig. 3); Bikaner in Rajasthan (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 mostly-susceptible 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 Odi-sha (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 suscep-tible 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, Pun-jab and Rajasthan (Figs. 1 and 3 respectively).

Double resistanceDDT-Malathion: Anopheles culicifacies (Table 2)

reported double resistance, i.e. to DDT and malathion in Districts of Andhra Pradesh (Fig. 4), Chhattisgarh (Fig. 5),

125

Gujarat (Fig. 3), Haryana (Fig. 1), Madhya Pradesh (Fig. 5), Odisha (Fig. 6), Uttar Pradesh (Fig. 1), Ut-tarakhand (Fig. 1), and West Bengal (Fig. 6). The spe-cies was resistant to DDT and malathion in district/s of Vizianagaram of Andhra Pradesh state; Dantewada, Su-kuma of Chhattisgarh; Surat in Gujarat; Gurgaon in Hary-ana; Balaghat, Shahdol and Sidhi in Madhya Pradesh; Bargarh, Bolangiri, Cuttack, Ganjam, Jagatsinghpur, Jharsuguda, Kandhamal, Khorda, Mayurbhanj and Sun-dargarh in Odisha; Allahabad in Uttar Pradesh; Nainital in Uttarakhand and from Bankura and Paschim/West Mid-napur district in West Bengal state.

Similarly, the urban vector An. stephensi (Table 3) was reported double resistant in Northwest Delhi (Fig. 1), North Goa ( Fig. 3), Kutch, Gujarat (Fig. 3), Ramanagar (Karnataka; Fig. 4) and Kolkata (West Bengal state; Fig. 6), Bikaner and Jodhpur of Rajasthan (Fig. 3); An. annu-laris (Table 5) in District East Singhbhum 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 Rajasthan (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, Sura-jpur and Surgurja 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, Kondag-aon, Narayanpur and Rajnandgaon in Chhattisgarh state (Fig. 5). An. stephensi (Table 3) exhibited double resis-tance in Dakshina Kannada, Karnataka state (Fig. 4).

Triple resistanceDDT-Malathion-Deltamethrin: Anopheles culicifa-

cies (Table 2) were resistant to three insecticides, namely DDT-malathion-deltamethrin in East Godavari, Sri-kakulam and Visakhapatnam districts of Andhra Pradesh state (Fig. 4); and in most of the Districts of Chhattis-garh state (Fig. 5), viz. Baloda Bazar, Bemetara, Bilaspur, Dhamtari, Durg, Jagdalpur, Janjgir-Champa, Jashpur, Ka-beerdham, Kanker, Korba, Korea, Mahasamund, Raigarh and Raipur. Also, this species was reported triple resis-tant in Districts Betul, Chhindwara, Dhindori, Jhabua and Mandla in Madhya Pradesh (Fig. 5); Gajapati, Kalahandi, Koraput, Malkangiri, Nabarangpur, Nuapada and Raya-gada in Odisha (Fig. 6) and District Khamman in Telan-gana state (Fig. 4).

The analysis of the susceptibility data of An. culicifa-

cies showed single insecticide resistance to DDT in 32 districts, malathion in four and to deltamethrin in two districts. Double insecticide resistance to DDT and mala-thion 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 dis-tricts. Anopheles subpictus was reported triple resistant in Kutch, Gujarat (Table 5, Fig. 3).

DISCUSSION

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 territo-ries 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 contrib-uting about 2/3 of malaria cases annually.

The data presented in this article provides detailed susceptibility status of malaria vectors in India to dif-ferent insecticides used for IRS programmes in In-dia and also provides information on resistance to single insecticides (DDT/malathion/deltamethrin), dou-ble resistance (DDT+malathion/DDT+deltamethrin/ malathion+deltamethrin) and triple resistance (DDT+ malathion+deltamethrin).The data was not available sys-tematically, in time and space but most of the data obtained was for An. culicifacies. Substantial data were available from the states of Odisha and Chhattisgarh, followed by Madhya Pradesh, the three congruent states of India, en-demic 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 dif-ferential in time and space based on the criterion of delin-eating 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. Single insecti-cide resistance to DDT was reported from 32 districts, malathion from four and to deltamethrin in two districts.



Double insecticide resistance to DDT and malathion was reported in 22 districts, DDT and deltamethrin in five dis-tricts 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 in-formation on kinetics of development and possibility of reversal of resistance is important. Such studies are scarce but a study conducted in Surat, Gujarat on the sta-bility of insecticide resistance in An. culicifacies provide some insights14. It was observed that DDT-malathion-re-sistance did not reverse completely even after long-term withdrawal of DDT (>30 yr) and malathion (9 yr) from IRS,while complete reversal of resistance was observed in case of deltamethrin within 2–3 yr of withdrawal. Further, the reversion of resistance depends on intrinsic fitness ra-tios of homozygotes and heterozygotes and frequency of resistance gene and the nature of inheritance of the gene14.

Anopheles culicifacies, the major vector of malaria is reported multiple resistant to insecticides of different classes. Studies on resistance mechanisms have indicated involvement of carboxylesterases for malathion resis-tance17, glutathione S-transferase (GST) for DDT resis-tance66, monooxygenases for pyrethroid resistance. Some molecular resistance studies have shown involvement of L1014F mutation for pyrethroid resistance and L1014S for DDT resistance and frequency of the kdr gene is very low and mostly heterozygous67. Studies so far have in-dicated noninvolvement of voltage gated sodium chan-nel (VGSC) gene in conferring pyrethroid resistance. Anopheles culicifacies, exists as a complex of five sibling species that are reproductively isolated and provision-ally designated as A, B, C, D and E and exhibit variations in various biological aspects such as prevalence, breed-ing habitat preferences, vectorial capacity, host feeding preferences and insecticide susceptibility68.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 sympatricity69. The sibling species have exhib-ited differential susceptibility to different insecticides, therefore, insecticide spray strategy for control of An. cu-licifacies in stratified areas has been proposed taking into consideration, the sibling species distribution and the rate of development of resistance69. However, the sibling spe-cies 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 re-

gions in 1990s70. Such 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 vec-tor, 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 tar-geted for IRS in few peri-urban areas. Presently, as a strat-egy for vector control in India, IRS is not targeted for the control of An. stephensi, except in Rajasthan where this is the reported primary vector of malaria70. The species was earlier reported resistant to DDT4, malathion71 and also to pyrethroids53.

For other four important primary vector species, namely An. fluviatilis, An. minimus, An. dirus and An. sundaicus, and vector species with localized or lesser im-portance, namely An. annularis, An. nivipes and An. sub-pictus, the data were available for few districts in some states. Anopheles fluviatilis, vector prevalent in hilly for-ested and foothill regions was reported resistant to DDT in 17 districts and to malathion in one district and was sus-ceptible to deltamethrin. Anopheles minimus, a major vec-tor 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 sus-ceptible 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 Nico-bar 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 suscep-tible to malathion and deltamethrin. Anopheles subpictus, recently reported as vector of malaria from coastal region of Goa72 was reported resistant to malathion in four dis-tricts, DDT and malathion in eight districts, malathion and deltamethrin in one district and to DDT, malathion and deltamethrin in one district.

Similar to An. culicifacies, other vector species also

127

exist as species complexes, except An. nivipes. Anopheles fluviatilis is a complex of three sibling species S, T and U with differential prevalence and vectorial capacity; An. minimus is a complex of three species, A, C, D and only species A is reported in India; An. dirus includes seven species, and species D and E are prevalent in India; An. annularis, a vector of localized importance in eastern In-dia, is reported to be complex of two species, A and B; An. subpictus is reported to be a complex of four sibling spe-cies A, B, C and D, and all four are reported from India55. These species show variable geographical distribution as well as behavioural differences with differential vecto-rial capacity. The data on sibling species composition and different biological aspects could not be included as they were not available retrospectively and also not part of the experimentation of different investigations.

In India, a strategy for the change of insecticides has been always reactive73. Successive changes in insecticides were made as end point replacement, i.e. replacement of insecticide after failure of the insecticide in use. This led to development of multiple resistance to different classes of insecticides owing to sequential selection of resistance.

The insecticide resistance is mainly due to selection by insecticide IRS, but possibility of selection due to pes-ticide usage in agriculture can not be ignored, as there are several such reports73. The contribution of agricultural pesticides use on the quantum of development of insecti-cide resistance in malaria vectors has not yet been quanti-fied mainly due to lack of data for correlations. Hence, for decision making in insecticide resistance management, selection due to agricultural pesticide usage need to be considered especially for introduction of new classes of insecticide molecules.

In 2012, WHO has published a Global Plan for Insec-ticide Resistance Management (GPIRM) in malaria vec-tors owing to widespread development of resistance to all classes of insecticides including pyrethroids5. Illustrative guidelines are provided for management of resistance us-ing insecticidal interventions plan at global and country level, with identified responsibilities for stakeholders which have become highly relevant for the vector control programmes in the present scenario of multiple-insecti-cide-resistant malaria vectors vis-à-vis malaria control. The National Vector Borne Disease Control Programme (NVBDCP), India has recently published Operational Manual for Integrated Vector Management74 and Frame-work for Malaria Elimination75.

In the present scenario of insecticide resistance status in malaria vectors in India, especially in An. culicifacies, the future of vector control relies primarily on the strate-gies for management of insecticide resistance and intro-

duction of novel insecticides/interventions. Presently, the vector control programme in India is reliant on pyrethroid IRS and pyrethroid LLINs. In the Northeastern states, An. culicifacies is not a major vector of malaria; however, in other states it is the major vector for malaria. Moreover, it has reported widespread pyrethroid resistance in three states, viz. Chhattisgarh, Madhya Pradesh and Odisha, while in other states it is sporadic. There are no new insec-ticide molecules available right away for vector control and management; albeit few are in pipeline including im-proved interventions, such as, co-formulated insecticides of different classes for IRS (pyrethroids+neonicotinoids) and combination LLINs (pyrethroids+synergists) etc. and may take some time for introduction into vector control programmes.

CONCLUSION

Anopheles culicifacies, a major vector of malaria was found to be reported mostly resistant to DDT and mala-thion while, it was variably resistant to deltamethrin. The major threat for the vector control programme is devel-opment of multiple resistance in An. culicifacies, which needs urgent attention for resistance management in or-der to sustain the gains achieved so far, as the National Malaria Control Programme has entered the phase for elimination by 2030. The routine monitoring of insecti-cide resistance in malaria vectors is the immediate need as the programme is presently reliant on one class of insecti-cide, i.e. pyrethroids, used in IRS and LLINs; and sooner or later the species will develop widespread resistance to pyrethroids. Thus, for effective control of malaria vec-tors, interventions involving new insecticide molecules with novel mode of action need to be developed on pri-ority basis, along with implementation of strategies for the management of existing resistance in malaria vectors to limit its further spread. The strategy includes the use of available insecticide rationally, based on the GPIRM and/or integrated vector management (IVM) methods and its implementation in the ambit of framework for malaria elimination.

Conflict of interestThe authors declare that they have no conflict of

interest.

ACKNOWLEDGEMENTS

Authors sincerely thank the workers, scientists and programme personnel whose data were included in the study.



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Correspondence to: Dr Kamaraju Raghavendra, Scientist ‘G’‚ ICMR-National Institute of Malaria Research, Sector–8, Dwarka, New Delhi–110077, India.

E-mail: [email protected]

Received: 15 March 2017 Accepted in revised form: 15 May 2017

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