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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 Raghavendra

1

, Poonam Sharma Velamuri

1

, Vaishali Verma

1

, Natarajan Elamathi

1

, Tapan Kumar Barik

1-2

, Rajendra Mohan Bhatt

3-4

& Aditya Prasad Dash

1,5

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

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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

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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 resistance

DDT: 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 vectors

Primary 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 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), Sikkim (0/4) and Tripura (3/8)

An. annularis, An. culicifacies,

An. dirus and An minimus An. nivipes (philippinensis)

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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 Reference DDT (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 7

Srikakulam 0 (21a) R 44.4 (135) R 77.7 (72) R

Visakhapatanam 6.6 (15a) R 46.6 (15a) R 73.6 (19a) R

Vizianagaram 0 (17a) R 32.2 (62) R 93.3 (15a) VR

Visakhapatanam (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 10

3. Chhattis-

garh Baloda 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) R

Durg 4.5 (110) R 72.9 (111) R 70.5 (102) R

Janjgir-Champa 14.2 (105) R 53 (83) R 64.1 (106) R

Kabirdham/Kabeerdham

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

Bastar 2015 – 63.4 (112) R 77.3 (110) R

Bijapur 1 (100) R

Bilaspur 67.5 (111) R 65.7 (105) R

Dantewada 0 (70) R 65 (20a) R

Dhamtari 73.5 (132) R 61.2 (103) R

Gariyaband/Gariaband 67 (103) R 45 (100) R

Kanker 63.9 (111) R

Kondagaon 54.3 (105) R 79.9 (105) R

Korba 57.7 (109) R

Mahasamund 70.1 (104) R 30 (100) R

Mungeli 81 (100) R

Narayanpur 81.8 (110) R 56.9 (105) R

Raigarh 4 (126) R 75 (124) R

Raipur 0 (100) R 26.5 (102) R

Rajnandgaon 35 (100) R 62.6 (127) R

Sukma 2.5 (80) R 73.3 (60) R

Balod 2014 – 60 (60) R

Balrampur 5 (101) R 88.8 (107) R

Kanker 82.7 (98) R

Koriya/Korea 10 (100) R 72.9 (107 R

Surajpur 7.3 (109) R 87.9 (107) R

Surguja 14 (100) R 85.3 (102) R

Bilaspur, Korba, Korea 2009 33.7 (95) R 42 (108) R 80.5 (118) R 11

Dantewada 9.8 (82) R 55.3 (85) R 98.7 (96) S

Dhamtari, Raipur 4 (99) R 73.5 (98) R 78.6 (98) R

Jagdalpur 21 (100) R 39.4 (100) R 77 (100) R

Jashpur, Raigarh 10 (60) R 42.4 (66) R 68 (75) R

Kanker 3.2 (186) R 69.4 (216) R 83.3 (190) R

Jagdalpur 2002 – 83.8 (40a) R 90.4 (46a) VR 12

Kanker 22.9 (40a) R 74.1 (43a) R 89.4 (45a) R

Mahasamund 25 (78) R 87.9 (36a) R 89.5 (40a) R

Raigarh 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...

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S.No. State District (Location) Year Percentage mortality (n) and susceptibility status Reference DDT (4%) Status Malathion (5%) Status Deltamethrin (0.05%) Status

Northwest Delhi (Rithala) 90 (10a) VR 100 (10a) S 100 (10a) S

5. Gujarat Surat 2006 20 (168) R 57 (220) R 99 (190) S 14

Surat 2005 40 (66) R 68 (145) R 98 (62) S

Surat 2001 9 (192) R 66 (322) R

Surat 2001 – 60–78b R 15

Surat (Gangapore) 13.1 (74) R 60.4 (106) R

Surat (Kakrapara) 6.7 (60) R 78.3 (106) R

Surat (Limbi) 6.9 (58) R 61.3 (109) R

Surat (Nidwada) 69.2 (117) R

Surat 1993 8.8–22b R 11.11b R 16

Surat 1992 6 (100) R 17 (60) R 17

6. Haryana Gurgaon (Mewat) 1997 – 100 (45a) S 18

Sonepat 100 (45a) S

Gurgaon (Prataphas) 1996 – 78 (50a) R 19

Gurgaon (Salamba) 73 (30a) R 87.9 (133) R 100 (30a) S

Gurgaon (Tekri) 45.9 (61) R 79.3 (92) R 100 (147) S

Gurgaon (Sirsa) 1994 b R b R 20

Karnal (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 21

East Singhbhum 2009 23.7 (140) R 95.1 (110) VR 100 (120) S 7

Gumla 26.3 (227) R 96.9 (152) VR 99.0 (191) S

Ranchi 10.4 (320) R 98.1 (170) S 98.1 (210) S

West Singhbhum 15.8 (180) R 98 (170) S 100 (160) S

Gumla 2007 38.4 (664) R 95.4 (611) VR 98.8 (566) S 22

Hazaribagh 1992 37.5e (60) R 94.6e (60) VR – 23

8. Karnataka Tumkur 2005 – 97 (60) VR – 24

9. Madhya

Pradesh Anuppur 2012 33 (15–20a) R 100 (15–20a) S 25

Chhindwara 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 26

Betul 12.4 (225) R 72.4 (225) R 83.1 (225) R

Chhindwara 9.2 (315) R 74.9 (315) R 85.9 (315) R

Dhindori/Dindori 12.8 (180) R 80 (180) R 71.6 (180) R

Guna 26.6 (300) R 100 (300) S 100 (270) S

Jhabua/Jhabula 6.6 (240) R 65.4 (240) R 87 (240) R

Mandla 13.3 (180) R 78.3 (180) R 76.6 (180) R

Shahdol 8.8 (180) R 77.8 (180) R 93.8 (180) VR

Sidhi 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 27

Gadchiroli (Malanda,

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

contd...

Table 2 (Contd.)

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Table 2 (Contd.)

S.No. State District (Location) Year Percentage mortality (n) and susceptibility status Reference DDT (4%) Status Malathion (5%) Status Deltamethrin (0.05%) Status

11. Odisha Kalahandi 2014 12.4 (105) R 60.4 (111) R 79.4 (131) R 29

Koraput 15.3 (111) R 66.7 (111) R 76.8 (112) R

Malkangiri 12.6 (111) R 76.2 (105) R 84.0 (119) R

Nabarangpur/Nawaranghpur 11.4 (105 R 70.9 (110) R 72.6 (113) R

Rayagada 12.6 (135) R 63.1 (130) R 81.7 (131) R

Balangir/Bolangir 2010 12.3 (106) R 80 (105) R 94.2 (104) VR 30

Gajapati 15.5 (103) R 83.8 (105) R 82.9 (105) R

Ganjam 14.7 (102) R 70.3 (101) R 95.2 (104) VR

Kalahandi 14.3 (105) R 86.7 (105) R 81.7 (104) R

Kandhamal 9.5 (105) R 77.6 (109) R 96.3 (109) VR

Koraput 13.5 (111) R 76.6 (111) R 98.4 (123) S

Malkangiri 15.2 (105) R 75.5 (110) R 86.2 (109) R

Nabarangpur/Nawaranghpur 13.8 (109) R 63.5 (126) R 96.5 (114) VR

Nuapada 15 (107) R 67.3 (98) R 100 (89) S

Rayagada 16.7 (102) R 77.6 (105) R 89.8 (108) R

Angul 2009 9.7 (80) R 100 (40a) S 96.3 (30a) VR 7

Bargarh/Baragarh 12.5 (300) R 72.3 (280) R 98.8 (340) S

Balangir/Bolangir 7.8 (502) R 74.4 (511) R 96.0 (494) VR

Cuttack 20 (100) R 74 (90) R 100 (90) S

Dhenkanal, Subarnapur/

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

Gajapati 12.6 (300) R 70.3 (280) R 98 (280) S

Ganjam 18.4 (30a) R 85 (20a) R 100 (30a) S

Jagatsinghpur 23 (100) R 85.5 (80) R 100 (90) S

Jharsuguda 12.6 (260) R 40.0 (240) R 96.7 (240) VR

Kalahandi 11.8 (76) R 78.3 (120) R 81.6 (120) R

Kendujhar/Keonjhar 11.1 (40a) R 100 (30a) S 100 (20a) S

Khordha/Khurda 20 (20a) R 80 (20a) R 100 (30a) S

Mayurbhanj, Sambalpur 14.8 (30a) R 100 (20a) S 96.3 (27a) VR

Nuapada 3.3 (60) R 93.8 (49a) VR 88.1 (59a) R

Kandhamal (Phulbani) 6.4 (93) R 59.1 (98) R 93.7 (96) VR

Rayagada 23.1 (272) R 90.6 (278) VR 89.2 (270) R

Sundargarh 25.9 (280) R 70.7 (260) R 95.1 (260) VR

Sundargarh 2008 b R b S 31

Gajapati (Guma) 2005 20 (15a) R 100 (15a) S Hazra

(Unpublished)

Gajapati (Mohana) 26.6 (15a) R 100 (15a) S

Mayurbhanj (Badampahar,

Rangamatia) 20 (15a) R 100 (15a) S

Nabarangpur (Nandahandi) 20 (15a) R 100 (15a) S

Nabarangpur (Papadahandi) 26.6 (15a) R 100 (15a) S

Nabarangpur (Tentulikhunti) 20 (15a) R 100 (15a) S

Rayagada (Bisamcuttack) 26.6 (15a) R 100 (15a) S

Rayagada (Muniguda) 13.3 (15a) R 100 (15a) S

Balangir/Bolangir 2002 23.3 (60) R 68.3 (60) R 95 (60) VR 32

Kalahandi 12 (60) R 88.3 (60) R 96.7 (60) VR

Kendujhar/Keonjhar 14 (50a) R 100 (80) S

Mayurbhanj 62.5 (40a) R 50 (40a) R 100 (60) S

Nuapada 8.3 (60) R 75 (60) R 81.7 (60) R

Kandhamal (Phulbani) 20 (60) R 100 (60) S 100 (60) S

Rayagada 15 (60) R 100 (60) S 100 (60) S

Sundargarh 12 (100) R 100(100) S 100 (100) S

Koraput 21.2 (33) R 33

Malkangiri 21.1 (90) R 35.3 (102) R 100 (51) S

Malkangiri 1993 0–10 (925) R 34

contd...

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S.No. State District (Location) Year Percentage mortality (n) and susceptibility status Reference DDT (4%) Status Malathion (5%) Status Deltamethrin (0.05%) Status

12. Rajasthan Jaisalmer 1999 b VR b S 35

Jaisalmer (Pokaran) 1995 30 (10a) R 100 (10a) S 36

Bikaner 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 24

Ramanathapuram 83.3 (180) R 100 (180) S 100 (180) S

Ramanathapuram

(Rameshwaram) 1997 – 100 (45a) S 18

14. Telangana Khammam 2009 23.3 (60) R 63.3 (60) R 43.3 (60) R 7

15. Uttar

Pradesh Moradabad 2002d 42.5b R 38

Gautam Buddh Nagar 2008 20b R b S b S 39

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

Bareilly/Bareeily 2002 21.4 (40) R 41

Bareilly/Bareeily 2001 15.5 (110) R Raghavendra

(Unpublished)

Bahraich 1999 7.3 (60) R 100b (15 min) S 42

Allahabad 1996 b R b R 43

16. Uttara-

khand Haldwani (Nainital) 2002d 86.2b R 100b S 44

Hardwar 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) S

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.

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.)

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

S. No. State District (Location) Year Percentage mortality (n) Reference

DDT (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 46

3. 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) VR

Gandhinagar 2005 77.2 (20–40a) R 100 (20–40a) S

Jamnagar 76 (20–40a) R 100 (20–40a) S

Surat 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) S

Barmer 2006 59.9 (20–40a) R 100 (20–40a) S

Jodhpur 72 (20–40a) R 92.9 (20–40a) VR

Barmer 2005 100 (20–40a) S

Bikaner 66.6 (20–40a) R 100 (20–40a) S

Ganganagar

(Sri Ganganagar) 95.4 (20–40a) VR 94.1 (20–40a) VR

Jaisalmer 1999 b VR b S 35

Jodhpur 1995 30–40b R 100b S 51

Barmer b R b VR 52

Jodhpur 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 53

1995 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.

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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.

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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) S

Malkangiri 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...

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Endri Endri Tue, Sep 15, 2020, 4:43 PM to Research Dear Harrison Rogers Editorial Assistant, Research in World Economy Sciedu Press I have revised our paper entitled "The Effects