R.K. Singh , P.K. Mittal , M.P. Gourshettiwar , S.J. Pande  & R.C. Dhiman

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J Vector Borne Dis 49, March 2012, pp. 42–44Susceptibility of malaria vectors to insecticides in Gadchiroli district(Maharashtra), IndiaR.K. Singh1, P.K. Mittal1, M.P. Gourshettiwar2, S.J. Pande3 & R.C. Dhiman11National Institute of Malaria Research (ICMR), New Delhi; 2Primary Health Centre, Murumgaon, Gadchiroli district; 3District MalariaOffice, Gadchiroli district, MaharashtraKey words Anopheles annularis Van der Wulp; An. culicifacies Giles; An. fluviatilis James; insecticide resistance; malaria;susceptibilityMalaria is hyperendemic in central parts of India with95% of the population at risk of infection1.  In Maharashtrastate, Gadchiroli district is one of the high malaria en-demic districts  where 13,553 malaria positive cases werereported in the year 2010, out of which Plasmodiumfalciparum accounted for 82.4%2. Slide positivity rate(SPR) in Gadchiroli district has been ranging from as lowas 1.43 to as high as 2.5% between the years 2006 and20102. But it has been substantially higher (2.5%) in 2010.Geographical area of Gadchiroli district is 14,412  km2and it is located on the north-eastern side of the state ofMaharashtra. It is situated at 18.43' to 21.50' north lati-tude and 79.45' to 80.53' east longitude and has uneventerrain with hills, valleys and forests at different altitudesand having total population of 10,71,795 (as of census2011)3. The average rainfall is 1743.5 mm, temperatureminimum 11.3 and maximum 47.7oC. Since 1958, the district has been receiving two roundsof sprays of DDT every year. An. culicifacies has devel-oped resistance to DDT, dieldrin and malathion (triple re-sistance) in about 30 districts of Maharashtra. Presently,this area is receiving two rounds of spray with a syntheticpyrethroid, alpha-cypermethrin. In spite of these controlmeasures, malaria remains a major public health prob-lem. The primary vectors of malaria in Gadchiroli districtare An. culicifacies and An. fluviatilis4,5.In India, An. culicifacies Giles alone contributes about65% of the total cases of malaria annually and is the wide-spread malaria vector of rural and peri-urban areas.  How-ever, this species has developed resistance to DDT in 286districts, to malathion in 81 and to pyrethroids in 2 dis-tricts in India6–8. In order to find out the rationale aboutusing alpha-cypermethrin in vector control, this study wascarried out on insecticide susceptibility in 10 endemic vil-lages of PHC, Murumgaon, Gadchiroli district ofMaharashtra state.Insecticides susceptibility tests were carried out in thethe year 2010 by using WHO procedure against variousinsecticides9–10. In the morning hours (0600 to 0800 hrs)with the help of suction  tube, An. culicifacies Giles, An.fluviatilis James and An. annularis Van der Wulp werecollected from cattlesheds, human dwellings and mixeddwellings of different villages of Murumgaon PHC.  Thecollected female mosquitoes were provided with 10% glu-cose solution soaked in cotton pads and transported incaged cloth to the field laboratories at the PHC ofMurumgaon, Gadchiroli district. Insecticide-impregnatedpapers with different diagnostic doses received from Uni-versity Sans Malaysia were used for detection of resis-tance to DDT (4%), malathion (5%) and deltamethrin(0.05%).Only full-fed and semi-gravid mosquitoes were usedto determine the susceptibility status. Mosquitoes were ex-posed against the diagnostic doses of insecticides for anhour, as per standard WHO technique9,10. Three to fourreplicates of each vector species containing 15–25 femalemosquitoes were taken simultaneously for each insecti-cide. Two replicates for control were also held parallel toeach test. The mosquitoes were exposed for 1 h and keptfor observation for 24 h.The percent mortalities werescored after 24 h of recovery period and if the controlmortality remained within 5–20%, test mortality was cor-rected  using Abbott’s formula11 and expressed as cor-rected percent mortality. If the mortality is >20%, the testswere discarded.Results of susceptibility tests on An. culicifacies, An.fluviatilis and An. annularis against DDT (4%), malathion(5%) and deltamethrin (0.05%) are given in Table 1. Thecorrected percent mortality of adult An. culicifacies, An.fluviatilis and An. annularis to DDT (4%) ranged between21 and 36.66%; to malathion (5%) between 90.52 and96%; and to deltamethrin (0.05%) between 94 and 96.42%.These results indicate that the tested mosquito speciesare resistant to DDT but tolerant to malathion anddeltamethrin.In India, resistance in malaria vectors to DDT at sev- 43 Singh et al: Insecticide susceptibility of mosquito vectors to insecticides in Gadchiroli district, Indiaeral places has been reported6–8. First indication of resis-tance to DDT in An. culicifacies malaria vectors was foundin Maharashtra state by Rao and Bhatia12 in the year 1957.However, first confirmed report on DDT resistance waspublished by Rahman et al13 in 1959. Later,Krishnamurthy and Singh14 recorded resistance in An.culicifacies to DDT in a village of Uttar Pradesh in theyear 1962. Double or triple resistance to DDT, dieldrinand malathion was recorded in An. culicifacies from 30districts of Maharashtra12,15–18. Resistance in An.culicifacies to malathion was first time observed from theadjoining state of Gujarat by Rajagopal et al19 in the year1977. Raghavendra et al20 in the year 1991 reportedmalathion resistance in adjoining state of Andhra Pradesh.Dhiman et al21 in the year 2005 reported resistance toDDT in An. culicifacies from Dhanora taluka in Gadchirolidistrict, but it was found susceptible to other insecticides.Our study confirmed this finding in Murumgaon PHC areaof District Gadchiroli, where  An. culicifacies, as well asAn. fluviatilis and An. annularis were found resistant toDDT only, while tolerant to other insecticides tested.Anopheles fluviatilis has been reported as a primaryvector of malaria in the forests of adjoining States ofChhattisgarh including Maharashtra4,5. Anophelesfluviatilis is found to transmit malaria throughout the yearin these areas, whereas An. culicifacies transmit malariain post-monsoon months between July and September.Anopheles fluviatilis is mainly distributed in hilly tractvillages and the preferential breeding habitat is stream22,23,where the chances of exposure to the agriculture pesti-cides are relatively less. Anopheles fluviatilis is resistanceto DDT in 11 districts from 8 states includingMaharashtra7. Resistance to DDT in adult An. fluviatilishas also been reported from Orissa (now Odisha)24. How-ever, Sharma et al25 reported that An. fluviatilis was foundsusceptible to DDT, malathion and deltamethrin in sevendistricts of Odisha. Singh et al26 recently reported resis-tance in An. culicifacies, An. fluviatilis and An. annularisto DDT from Jharkhand in the year 201027. In our study,An. fluviatilis was found resistant to DDT only, while theyare tolerant to other insecticides tested.  Resistance to DDTin An. fluviatilis may be due to prolonged use of DDT inindoor residual spray since 1958.  However, presently thisarea is receiving two rounds of IRS with synthetic pyre-throids to which these species are in tolerant stages (veri-fication required).For the first time, An. annularis resistance to DDTwas detected in the year1962 from Meerut district of UttarPradesh14.  Later on resistance was reported from variousparts of the country6–8, 24–28.  Anopheles annularis hasdeveloped double resistance to DDT and dieldrin fromAssam7. In our study, An. annularis was found resistantto DDT only, while they are at verification required stageto malathion and deltamethrin.Present study indicated that An. culicifacies, An.fluviatilis and An. annularis are resistant to DDT whiletolerant in case of other insecticides tested. Malathion re-sistance has been reported in An. culicifacies and An.annularis in earlier studies in Maharashtra, but our studyshowed no indication of malathion resistance in any of thetested mosquitoes species in this study area.  High ende-micity of malaria in the study area, which is receiving tworounds of IRS with synthetic pyrethroids, warrants thatsynthetic pyrethroids use should be undertaken as pernorms of the National Vector Borne Disease ControlProgramme, where, there is a need to educate communityfor enhanced spray coverage of houses and rooms. Thereis also need to strictly monitor whether two rounds of IRSactivities are done during coverage of houses. To delaythe precipitation of resistance to synthetic pyrethroid, otherinsecticides can be used in rotation with synthetic pyre-throids. District-wise susceptibility status of mosquitoesTable 1. Susceptibility of Anopheles mosquitoes to insecticides in Murumgaon, Gadchiroli district (Maharashtra), IndiaMosquito species Insecticide     No. of mosquitoes exposed No. of mosquitoes dead Corrected Status(% conc. tested) mortalityTest Control Test Control (%)An. culicifacies DDT (4)   100 40   29 3  23.24 RMalathion (5)   100 40   96 0 96 VRDeltamethrin (0.05)   100 40   94 1 94 VRAn. fluviatilis DDT (4)   60 30   22 0   36.66 RMalathion (5)   60 30   57 0   95 VRDeltamethrin (0.05)   60 30   58 2   96.42 VRAn. annularis DDT (4)   100 40   21 0 21 RMalathion (5)   100 40  91 2 90.52 VRDeltamethrin (0.05)   100 40   95 1 95 VRR—Resistant; VR—Verification required (tolerant). J Vector Borne Dis 49, March 2012 44to the insecticides being used in the programme should bemonitored for judicious use of appropriate insecticides formalaria control in these areas.ACKNOWLEDGEMENTSThe laboratory and field assistance provided by thestaff of NIMR and Mr. Surendra Kumar is gratefully ac-knowledged. Authors are also thankful to Mr. MatherBoina, ADMO and his staff for providing the informationon malaria incidence and use of insecticide in IRS in vec-tor control in Gadchiroli district of Maharashtra state.REFERENCES1. Delhi, India: National Vector Borne Disease Control Programme,Ministry of Health and Family Welfare. Available from: http://www.nvbdcp.gov.in/malaria (accessed on June 20, 2011).2. Government of Maharastra Public Health Department, Direc-torate of Health Services. Available from: http://maha-arogya.gov.in/programs/nhp/antimaleria/perfdistwise.htm3. Census 2011. Available from:  http:/www.census2011.co.in/cen-sus/district/346-gadchirolil.htm.4. Sharma MD. Vectors of malaria An. fluviatilis James 1902—vectors of malaria in India. Nat Soc Bull Ind Mal Mosq Dis1961; 77–90.5. Rao TR. The Anopheline of India 1984. Delhi: Malaria ResearchCentre (ICMR) 1984; p. 154–8.6. Pillai, MKK. Vector resistance to insecticides. Proc Nat AcadSci 1996; 68(B): 77–97.7. Kumari R, Thapar BR, Dasgupta RK, Kaul SM, Lal S. Suscep-tibility status of malaria vectors to insecticides in India. JCommun Dis 1998; 30(3): 179–85.8. Mittal PK, Wijeyratne P, Pandey S.  Status of insecticide resis-tance of malaria, kala-azar, Japanese encephalitis vectors inBangladesh, Bhutan, India and Nepal (BBIN). Available from:http//:ehpproj.org/pdf/Activity report 129. EHP Project 26568/EXANEMDR.9. Manual on practical entomology in malaria. Pt. II. Methodsand techniques. Geneva: World Health Organization 1975; p.191.10. Instructions for determining the susceptibility or resistance ofadult mosquito to organochlorine, organophosphate and carbonateinsecticides — diagnostic test. WHO/VBC/1981, 81-806, p. 7.11. Abbott WS. A method of computing the effectiveness of an in-secticide. J Ecol Entomol 1925; 18: 265–467.12. Rao TR, Bhatia SC. A note on the degree of susceptibility ofAnopheles culicifacies to DDT in some parts of Bombay state,India. Indian J Malariol 1957; 11(3): 261–9.13. Rahman J, Roy ML, Singh NN. Development of increased   toler-ance to DDT in Anopheles culicifacies Giles in the Panchmahal dis-trict in Bombay state, India. Indian J Malariol 1959; 12: 125–30.14. Krishnamurthy BS, Singh NN. DDT resistance in Anophelesculicifacies Giles, 1901 and Anopheles annularis Van der Wulp1884 in a village of Meerut district, U.P. Indian J Malariol1962; 16: 375–7.15. Vittal M, Bhate MR. Bioassay tests on the effectiveness ofmalathion spraying on Anopheles culicifacies  resting on differ-ent wall surfaces in Aurangabad town, Maharashtra. Indian JMalariol 1981; 18: 124–5.16. Vittal M, Deshpande LB. Development of malathion resistancein a DDT, HCH resistant Anopheles culicifacies population inThane district (Maharashtra). J Commun Dis 1983; 15: 144–5.17. Deobhankar RK, Pelkar ND. Magnitude of DDT resistance inAnopheles culicifacies in Maharashtra state. J Commun Dis1990; 22: 77.18. Sharma MID, Samnotra KG. A note on gamma BHC and dieldrenresistance in Anopheles culicifacies Giles in adjoining areas ofGujarat and Maharashtra states. Bull Natl Soc India Malar MosqDis 1962; 10: 151–7.19. Rajagopal R. Malathion resistance in Anopheles culicifacies inGujarat. Indian J Med Res 1977; 66: 27–8.20. Raghavendra K, Vasantha K, Subbarao SK, Pillai MKK, SharmaVP. Resistance in Anopheles culicifacies sibling species B andC to malathion in Andhra Pradesh and Gujarat states in India. JAmer Mosq Control Assoc 1991; 7(2): 255–9.21. Dhiman RC, B Shahi, Sharma SN, Khargiwarkar VN, SubbaraoSK. Persistence of malaria transmission in a tribal area inMaharashtra. Curr Sci 2005; 88(3): 754–8.22. Singh N, Khare KK. Forest malaria in Madhya Pradesh: chang-ing scenario of disease and its vectors. Indian J Parasit Dis1999; 23: 105–12.23. Das PK, Gunasekaran K, Sahu SS, Sadanandane C,Jambulingam P. Seasonal prevalence and resting behaviour ofmalaria vectors in Koraput district of Orissa.  Indian J Malariol1990; 27: 173–81.24. Sahu SS, Patra KP. A study on insecticides resistance in Anoph-eles fluviatilis and An. culicifacies to HCH and DDT inMalkangiri district of Orissa. Indian J Malariol 1995; 32(3):112–8.25. Sharma SK, Upadhyay AK, Haque MA, Singh OP, Adak T,Subbarao SK. Insecticide susceptibility status of malaria vec-tors in some hyper-endemic tribal districts of Orissa. Curr Sci2004; 87(12): 1718–26.26. Singh RK, Dhiman RC, Mittal PK, Das MK. Susceptibility ofmalaria vectors to insecticides in Gumla district, Jharkhand state,India. J Vector Borne Dis 2010; 47: 116–8.27. Azeez SA. Susceptibility status of Anopheles fluviatilis andAnopheles annularis to DDT in an area near Dhanbad. Bull In-dian Soc Mal Commun Dis 1964; 1: 53–4.28. Singh RK, Dhiman RC,  Kumar G, Sinha ATS, Dua VK. Sus-ceptibility of malaria vectors to insecticides in Koderma,Jharkhand. J Commun Dis 2011; 43: 273–6.Correspondence to: Dr R.K. Singh, Research Scientist, National Institute of Malaria Research (ICMR), Sector-8, Dwarka, New Delhi–110 077.E-mail: singhriku@yahoo.co.inReceived: 3 November 2011 Accepted in revised form:17 January 2012

Susceptibility of malaria vectors to insecticides in Gadchiroli district (Maharashtra), India

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