A note on the insecticide susceptibility status of principal malaria vector Anopheles culicifacies in four states of India.
Since early 19th century, chemical insecticides based vector control methods are in practice globally in the vector control programmes (1). Presently, among the available vector control interventions, indoor residual spraying (IRS) of insecticides and long-lasting insecticidal nets/ materials (LNs/LMs) are considered effective for limiting malaria transmission in disease control programmes (2). Currently, 12 insecticides are recommended by WHO for IRS to control mosquito vectors (3), while in India, DDT (organochlorine), malathion (organophosphate) and deltamethrin, cyfluthrin, alpha-cypermethrin and lambdacyhalothrin (pyrethroids) are in use in the vector control programme. Pyrethroids were introduced in India in mid-nineties for IRS and later for impregnation of mosquito nets. Presently, pyrethroid impregnated long-lasting insecticidal nets are being used in India and is poised for further scale up in future. The strategy of sequential end point replacement of insecticides practiced in the vector control programme in India has resulted in multiple-insecticide-resistance in An. culicifacies (Diptera: Culicidae). An. culicifacies is the major malaria vector that contributes about 65% of the total malaria cases reported in India (4). In India, widespread resistance in An. culicifacies to DDT has been reported (5-7). Resistance to malathion has been reported from some states (8-11), while there are few reports of decreased susceptibility to synthetic pyrethroids in few areas (12-14) and in some districts of Chhattisgarh (15) and Madhya Pradesh (16).
In the present investigation, we present the results of insecticide susceptibility status of An. culicifacies in 32 tribal districts of four states, viz. Andhra Pradesh, Odisha, Jharkhand and West Bengal against commonly used insecticides in public health.
MATERIAL & METHODS
The study was conducted in 32 districts of four states, Andhra Pradesh, Odisha, Jharkhand and West Bengal. These districts were suggested by National Vector Borne Disease Control Programme (NVBDCP) that are forested areas inhabited predominantly by tribals and are reported to be endemic for malaria. Surveys were carried out in individual districts or in groups of two districts, and the districts in the groups had similar ecotypes. Mosquitoes were collected from two groups of two districts each in West Bengal, while in Odisha of the 19 districts, 15 were surveyed individually and four in groups of two districts each. While in Andhra Pradesh and Jharkhand states, surveys were carried out individually in the suggested districts.
Adult insecticide susceptibility tests were conducted following WHO standard method (17) by exposing field-collected mixed age population of mosquitoes to DDT (4%), malathion (5%), deltamethrin (0.05%) and their respective control papers. The tests were carried out during October/November 2009-10. Mosquitoes were collected during the early morning hours using a mouth aspirator and torch light (18). The mosquitoes collected from field were held in a cloth cage with a wet towel around the cage and brought to the base laboratory. The species were identified based on morphological characters using a standard identification key for anophelines (19). Mosquitoes were exposed for 1 h followed by 24 h holding period at 27 [+ or -] 2[degrees]C temperature and 70-80% relative humidity using a carton lined with moist towel/filter papers at the bottom. At least 3-4 test replicates were used in the tests against the given insecticide and two replicates to respective control papers. Mortality was determined by scoring the dead and alive mosquitoes at the end of 24 h holding period and results were expressed as percent mortality. Test mortality was corrected by applying Abbott's formula (20), when control mortality was recorded between 5 and 20%, while tests with >20% control mortality were discarded. Based on the mortality, the data were categorized as susceptible: >98% mortality; verification required: 81-97% mortality; and resistant: <80% mortality.
Adult mosquitoes were collected from different localities as described above for the present investigation. However, in some tests, due to less availability of mosquitoes, the number of mosquitoes exposed to insecticide was very low. The results of the susceptibility tests are given in Table 1. An. culicifacies was found resistant to DDT in all the 32 districts surveyed.
To malathion, it was resistant in 14 districts, verification required category in 10 districts and susceptible in eight districts. Resistance to malathion was detected in all the five districts of Andhra Pradesh and nine districts of Odisha. To malathion the species was verification required category in two districts of Jharkhand (Gumla and East Singhbhum), four districts of Odisha (Nuapada, Rayagada, Jagatsinghpur and Ganjam) and in all the four districts of West Bengal. An. culicifacies was found susceptible to malathion in two districts of Jharkhand (Ranchi and West Singhbhum) and six districts of Odisha (Mayurbhanj, Sambalpur, Dhenkanal, Sonepur, Keonjhar and Angul).
To deltamethrin, it was found resistant in four districts, verification required category in 11 districts and susceptible in 17 districts. An. culicifacies was resistant to deltamethrin in four of the five districts surveyed in Andhra Pradesh except in Vizianagaram, while in Odisha, the species was verification required category in districts, Angul, Bolangir, Nuapada, Rayagada, Jharsuguda, Sundargarh, Kalahandi, Phulbani, Mayurbhanj and Sambalpur, and susceptible to deltamethrin in Keonjhar, Dhenkanal, Sonepur, Gajapati, Cuttack, Jagatsinghpur, Ganjam, Khurda and Baragarh districts of Odisha and all the districts of Jharkhand and West Bengal.
There are about 125 mosquito species with documented resistance to one or more insecticides (21). Development of insecticide resistance in malaria vectors is one of the serious limitation for effective vector control for programmes that rely on chemical insecticides. Lack of new insecticide molecules with new chemistries is becoming a serious impediment for effective management of existing insecticide resistance in malaria vectors. In the present study, An. culicifacies was found resistant to DDT in all the 32 districts surveyed in Andhra Pradesh, Odisha, Jharkhand and West Bengal. These results are not different from the results reported so far in other studies (5-7).
An. culicifacies was reported susceptible to malathion in villages of Haryana state (22), in Madhya Pradesh (16) and also in the present study in some districts of Jharkhand and Odisha. The species was reported in verification required category to malathion in Gumla and East Singhbhum districts of Jharkhand as reported earlier (23). Widespread resistance to malathion was earlier reported from Maharashtra (8), Gujarat (10, 24), Uttar Pradesh (11), Madhya Pradesh (16), Andhra Pradesh (24) and Odisha (RK Hazra, RMRC, Bhubaneswar personal communication).
There are few reports of decreased susceptibility to synthetic pyrethroids in various parts of the country (12-14). In the present study, An. culicifacies was found susceptible to deltamethrin in Jharkhand, West Bengal and some districts of Odisha, namely Keonjhar, Dhenkanal, Sonepur, Gajapati, Cuttack, Jagatsinghpur, Ganjam, Khurda and Baragarh. The species was reported susceptible to synthetic pyrethroids in some states like Uttar Pradesh, Maharashtra and Odisha (7,11,25), Gumla district of Jharkhand (23), Dantewada district of Chhattisgarh (15) and Guna district of Madhya Pradesh (16). An. culicifacies was reported in verification required category in Kanker, Bilaspur, Korea and Korba districts of Chhattisgarh (15, 26), Sidhi, Shahdol, Balaghat, Betul, Chhindwara and Jhabua districts of Madhya Pradesh (16). However, to deltamethrin, the species was reported resistant in Jagdalpur, Raipur, Dhamtari and Raigarh districts of Chhattisgarh (26), Mandla and Dindori districts of Madhya Pradesh (16) and in all the five districts of Andhra Pradesh in the present survey. Reported deltamethrin-resistance in some districts in the absence of reported use of pyrethroids in the malaria control programme needs further investigations and may be contemplated to its use in agriculture (15).
Results of this study in 32 districts in four states indicated variable levels of resistance to insecticides used in public health in this important vector. The study gains importance especially in view of the reported deltamethrin-resistance in this vector in some areas. Use of deltamethrin or other pyrethroids still remain a choice for vector control till an effective alternative insecticide is available for vector control for management of insecticide resistant vectors.
Indoor residual spraying of insecticides is the most preferred vector control option to manage vector borne diseases. Present study in 32 districts surveyed in four states indicated variable levels of insecticide-resistance to malathion and deltamethrin but resistance to DDT in An. culicifacies. Since, the introduction of pyrethroids in the 1980s, no new adulticide has been approved for vector control by the World Health Organization. Importantly, development of pyrethroid resistance in An. culicifacies, the major malaria vector in India is of concern as pyrethroids are presently the only viable choice for vector control. To overcome this, concern and for better insecticide resistance management strategies, there is a need for regular monitoring of insecticide resistance in malaria vectors.
The present investigation received financial support from National Vector Borne Disease Control Programme, Delhi. Authors are thankful to the technical staff of the NIMR Field Units, Hardwar, Bengaluru, Ranchi and Rourkela for carrying out the studies.
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Received: 10 February 2014
Accepted in revised form: 4 July 2014
Kamaraju Raghavendra , T.K. Barik [1,2], S.K. Sharma , M.K. Das , V.K. Dua , A. Pandey , V.P. Ojha , S.N. Tiwari , S.K. Ghosh  & A.P. Dash [1,6]
 National Institute of Malaria Research (ICMR), New Delhi;  P.G. Deptartment of Zoology, Berhampur University, Berhampur, Odisha;  National Institute of Malaria Research (Field Unit), Ranchi, Jharkhand;  National Institute of Malaria Research (Field Unit), Hardwar, Uttarakhand;  National Institute of Malaria Research (Field Unit), Bengaluru, Karnataka;  WHO-SEARO, New Delhi, India
Correspondence to: Dr K. Raghavendra, Scientist 'F', National Institute of Malaria Research, Sector 8, Dwarka, New Delhi-110 077, India.
Table 1. Insecticide susceptibility status of An. culicifacies in four states of India State District DDT (4%) % Mortality (n) Status Andhra Pradesh East Godavari 36.6 (60) R Khammam 23.3 (60) R Srikakulam 0.0 (21) R Visakhapatnam 6.6 (15) R Vizianagaram 0.0 (17) R Jharkhand Gumla 26.3 (227) R Ranchi 10.4 (320) R East Singhbhum 23.7 (140) R West Singhbhum 15.8 (180) R Odisha Angul 9.7 (80) R Keonjhar 11.1 (40) R Bolangir 7.8 (502) R Nuapada 3.3 (60) R Dhenkanal and Sonepur 9.3 (30) R Gajapati 12.6 (300) R Rayagada 23.1 (272) R Jharsuguda 12.6 (260) R Sundargarh 25.9 (280) R Kalahandi 11.8 (76) R Phulbani 6.4 (93) R Mayurbhanj and Sambalpur 14.8 (30) R Cuttack 20.0 (100) R Jagatsinghpur 23.0 (100) R Ganjam 18.4 (30) R Khurda 20.0 (20) R Baragarh 12.5 (300) R West Bengal Bankura and Midnapur 3.3 (60) R Purulia and Birbhum 6.6 (75) R State District Malathion (5%) % Mortality (n) Status Andhra Pradesh East Godavari 80.0 (60) R Khammam 63.3 (60) R Srikakulam 44.4 (135) R Visakhapatnam 46.6 (15) R Vizianagaram 32.2 (62) R Jharkhand Gumla 96.9 (152) VR Ranchi 98.1 (170) S East Singhbhum 95.1 (110) VR West Singhbhum 98.0 (170) S Odisha Angul 100.0 (40) S Keonjhar 100.0 (30) S Bolangir 74.4 (511) R Nuapada 93.8 (49) VR Dhenkanal and Sonepur 100.0 (20) S Gajapati 70.3 (280) R Rayagada 90.6 (278) VR Jharsuguda 40.0 (240) R Sundargarh 70.7 (260) R Kalahandi 78.3 (120) R Phulbani 59.1 (98) R Mayurbhanj and Sambalpur 100.0 (20) S Cuttack 74.0 (90) R Jagatsinghpur 85.5 (80) VR Ganjam 85.0 (20) VR Khurda 80.0 (20) R Baragarh 72.3 (280) R West Bengal Bankura and Midnapur 88.3 (60) VR Purulia and Birbhum 90.8 (65) VR State District Deltamethrin (0.05%) % Mortality (n) Status Andhra Pradesh East Godavari 70.0 (60) R Khammam 43.3 (60) R Srikakulam 77.7 (72) R Visakhapatnam 73.6 (19) R Vizianagaram 93.3 (15) VR Jharkhand Gumla 99.0 (191) S Ranchi 98.1 (210) S East Singhbhum 100.0 (120) S West Singhbhum 100.0 (160) S Odisha Angul 96.3 (30) VR Keonjhar 100.0 (20) S Bolangir 96.0 (494) VR Nuapada 88.1 (59) VR Dhenkanal and Sonepur 100.0 (20) S Gajapati 98.0 (280) S Rayagada 89.2 (270) VR Jharsuguda 96.7 (240) VR Sundargarh 95.1 (260) VR Kalahandi 81.6 (120) VR Phulbani 93.7 (96) VR Mayurbhanj and Sambalpur 96.3 (27) VR Cuttack 100.0 (90) S Jagatsinghpur 100.0 (90) S Ganjam 100.0 (30) S Khurda 100.0 (30) S Baragarh 98.8 (340) S West Bengal Bankura and Midnapur 100.0 (40) S Purulia and Birbhum 100.0 (45) S Susceptibility status as per WHO criteria: Resistant (R) = <80% mortality; Verification required (VR) = 81-97% mortality; Susceptible (S) = 98-100% mortality; n = No. of mosquitoes exposed.
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|Author:||Raghavendra, Kamaraju; Bank, T.K.; Sharma, S.K.; Das, M.K.; Dua, V.K.; Pandey, A.; Ojha, V.P.; Tiwar|
|Publication:||Journal of Vector Borne Diseases|
|Date:||Sep 1, 2014|
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