Journal of the American Mosquito contror Association, 2o(4):424-42g,2004 Copyright @ 2OO4 by the American Mosquito Control Association, Inc.
FOLLOW-UP STUDIES AFTER WITHDRAWAL OF DELTAMETHRIN SPRAYING AGAINST ANOPHELES CULICIFACIES AND MALARIA INCIDENCE
MUSHARRAF ALI ANSARI eNo RAMA KRISHNA RAZDAN
Malaria Research Centre (ICMR), 2}-Madhuban, Delhi_ll0 092, India
ABSTRACT. Follow-up studies were carried out from 1989 to 1998 after withdrawal of deltamethrin indoor spraying to evaluate the-recovery rate of a population of Anopheles culicifacies resistant to dichlorodiphenyltri- chloroethane (DDT) and hexachlorocyclohexane (HCH) in selected villages in Uttar pradesh State, I;dia. The study revealed 82.4-96.5Ea reduction in adult density of An. culicifacies and 72.7-967o reduction in malaria incidence in the area sprayed with deltamethrin at 20 mg/m, as compared to a control area sprayed with HCH, for 5 successive years even after withdrawal of deltamethrin spray. The impact was very clear when the annual falciparum incidence was compared with that of the control area. The vector population gradually started re- covering after 5 years. However, the slide falciparum rate remained below 4 even after 10 years of withdrawal of spraying. The study revealed that indoor residual spraying of deltamethrin would be cost-effective, at least in areas where malaria is transmitted by An. culicifacies, which is primarily a zoophilic species and associated with malaria epidemics. In view of this, a review of the insecticide policy and strategy of vector control is urgently needed because of the possible risks associated with the presence of nonbiodegradable insecticide in the environment, as well as to minimize the costs of operation and to enhance the useful life of insecticides.
KEY WORDS Anopheles culicifacies, deltamethrin, vector control, impact of residual spraying
INTRODUCTION in agriculture. Major crops of this area are wheat, rice, maize, and pulses. The area of the Dadri PHC Anophele s culicifac ie s Giles (Diptera: Culicidae) is about 22'7 km2 and the population is about is a principal vector of malaria and is responsible 144,000 distributed in 65 villages. Both experimen- for 7O-75Vo of malaria transmission in the northern tal and control PHCs are situated on the bank of plains of India. Resistance to dichlorodiphenyltri- the upper Ganga canal and the area is irrigated chloroethane (DDT), hexachlorocyclohexane (HCH), through irrigation channels supplemented by tube- and malathion is detectable in Maharashtra, Guja- wells. The ratio of humans to cattle is 4:1 in Ra- rat, and Haryana states (Pillai 1996). A field trial zapur PHC and 7:l in Dadri PHC. The control PHC was carried out in Razapur Primary Health Centre (PHC), Ghaziabad District (Uttar Pradesh), during was sprayed with HCH at 2OO mg/m' in 1989 and not Razapur PHC 1986-88 to evaluate the efficacy of deltamethrin later the PHC was sprayed. The applied at 12.5, 2O, and 25 mglm2 against DDT- was initially divided into 3 zones. Zone I was and HCH-resistant An. culicifacies and the impact sprayed with 3 rounds of deltamethrin at 12.5 mg of spraying on malaria incidence. Results revealed m2 at an interval of 6 wk with stimrp pumps by the drastic reduction in the vector population and ma- trained spray team as per World Health Organiza- laria incidence in the sprayed villages (Ansari et al. tion (WHO) guidelines, whereas in only 2 rounds 1990). Because the cost of the synthetic pyrethroid were sprayed zone II and zone III at 2O a,nd 25 mg/ was much higher than that of the commonly used m2, respectively, at an interval of 8 wk during 1986, insecticides DDT and HCH, follow-up studies were 1987, and 1988. No insecticide has been sprayed in carried out after the 3 years of deltamethrin spray- Razapur PHC since 1989. All the structures in the ing to assess the cost-benefit ratio of synthetic pyr- selected villages, including temporary structures ethriods in comparison to convential insecticides and cattle sheds, were sprayed both inside and out- which are generally used every year without effec- side. All necessary precautions were taken during tively suppressing the vector population or inci- the spraying operation both in control and experi- dence of malaria. Results of follow-up studies car- mental villages as per WHO guidelines (WHO ried out from 1989 to 1998 after withdrawal of 1986). insecticide pressure are presented in this paper. Initially, village-wise data on the annual parasite incidence (API), mosquito prevalence, malaria cas- es from 1983 to 1985 in both Razapur and Dadri MATERIALS AND METHODS PHCs were collected from the National Malaria The study was carried out from 1989 to 1998 in Eradication Programme, Goverment of India. Ra- Razapur PHC, which is situated in Ghaziabad Dis- zapur PHC was selected for deltamethrin spraying trict about 35 km from Delhi. The population of the because of high mosquito density, DDT and HCH PHC is about 140,000 distributed in 46 villages in resistance in An. culicifacies, and high malaria an area of 185 km' . There are about 18,000 human transmission. Five villages from each zone and dwellings and most of the inhabitants are engaged PHC were selected for the present study, based on DecgMsen 2OO4 FoIIow-up SruoIEs oN DELTAMETHruNSPNNYNC AGAINST AN, CULICIFACIES the average API in the 3 years before the spraying 1m 1m operation (1983-85). During the prespray period, & 80 trc was comparable between the control and E@ the API f,ao 4? (Ansari 1990). experimental villages et al. E8 mI Mosquitoes were collected by hand by using a "20 tube and flashlight between 0600 and 0800 I,a I suction {0 made { h in each village and zone. Collections were s { every 2 wk in 16 randomly selected human dwell- {0 s ings in each village. Collected mosquitoes were J@ {m 1S 1S71S8 1S 1m 1S1 1S? 1S3191S 19S 1S7 1S identified and the data of all villages in each zone YEARS h.ffi o(.d*E/6fa# were pooled and annual density per structure was G€zoml Iben @hill +zmel +hil +bncill calculated. Door-to-door fortnightly active surveil- lance also was carried out to detect fever cases. Percentreduction in mosquito density over the Both thick and thin blood smears were collected Fig.l. control in experimental villages sprayed with deltameth- from the patients with a fever and were examined rin. microscopically under oil immersion with Giemsa stain. Presumptive treatment (600 mg chloroquine) was given to all patients with a fever, and radical spraying (1986-88). This confirms the earlier find- treatment was given to all patients with microscop- ings of Ansari et al. (1986), who demonstrated ef- ically confirmed malaria (600 mg chloroquine with fective malaria control in the village Bhanera of 45 mg primaquine for Plasmodium falciparum and Loni PHC in Ghaziabad District. The impact of ear- 15 mg primaquine for 5 day for Plasmodiumvivax). lier spraying was evident for about 5 years, even The data of all 5 villages in each zone were pooled after withdrawal of the deltamethrin spraying. Dur- separately and slide positivity rate (SPR), API, an- ing 1989-93, the percent reduction ranged from nual blood examination rate, slide falciparum rate 67.O to 9O.87oin zone I, 82.4 to 96.5% in zone II, (SFR), and annual falciparum incidence (AFI) were and 85.8 to 97.1Va in zone III. The entomological calculated by using standard formulae. Susceptibil- impact gradually started diluting from 1994 onward ity tests were also carried out on mosquitoes col- and the degree of dilution was directly proportional lected from all the zones by using WHO standard to the dosages used. In other words, the dilution procedures, by exposing fully fed field-collected was more pronounced with the single dose (12.5 An. culicifacies and Culex quinquefasciatus Say mg/m' ) as compared to 20 and 25 mg/m2. Never- (Diptera: Culicidae) for I h to papers impregnated theless, a reduction in the densities of An. culici- with DDT (4Vo), malathion (5Vo), and deltamethrin facies was evident up to 10 years even after with- (O.O25Vo)according to WHO standard procedures. drawal of spraying in zone I, zone II, and zone III, Percent reduction was calculated by using the fol- in comparison to control PHC and was significant lowins formula: at ttre SVo level (P < 0.5). The study revealed that 3 years of continuous indoor residual spraying control - treated of clo reduction = x 100 deltamethrin was sufficient to produce entomolog- control ical impact even after 10 years of withdrawal. How- Data were statistically analyzed by using Student's ever, recurring spraying is required with conven- /-tests for significance. Further meteorological data, tional insecticides such DDT and HCH to obtain such as rainfall and temperature, also were collect- some impact. The impact of indoor residual spray- ed from the Meterological Department of Ghazia- ing of deltamethrin was observed during spraying bad District during the study period to check for years on Cx. quinquefasciatus, a vector of lym- any adverse fluctuations in meteorological indica- phatic filariasis and a pest mosquito; howeveq the tors that might affect mosquito breeding and sur- population quickly recovered and resistance to del- vival, and malaria transmission. tamethrin was detected in this species during the 2nd and 3rd year of spraying (Ansari et al. 1990). The reduction in density of Cx. quinquefasciatus RESULTS was not significant at the 5Vo level. Entomological evaluation Current susceptibility status Percent reduction based on control density of ex- perimental and control villages was calculated and Results of susceptibility test are presented in Ta- is presented in Fig. 1. Spraying of deltamethrin at ble 1. It is clear from the table that DDT- and HCH- 12.5 mg/m2 (zone I), 2O mg/m2 (zone II), and 25 resistant An. culicifacies remained susceptible to rng/m2 (zone III) resulted in drastic reduction in deltamethrin even after 3 years of spraying. How- adult densities of An. culicifacies. The percent re- ever, resistance to deltamethrin was detected in Cr. duction of adult density was from 76.4 to 96.4Voin quinquefasciatus after 2 years of spraying. The re- zone l, from 89.6 to 97.9Vo in zone II, and from sistance developed in Cx. quinquefasciatus dtting 97.1 to 99.4Vo in zone III in successive years of initial spraying reverted back to its original suscep- 426 JounN,qr- or. tHr AvsntcnN Mosquno CoNrnor_Assocrarror.t VoL. 20, No. 4 ll il o\o { tl K E.: ?a?o?o ?o ?oQoQ^ e^ il qg* 898888 88 sssses s3 il -o tl il tl a tl sb ?o?o?o ?o q-g-q^*g.gog q^ :.ll R8R89g Xg :s Htl Qtl Ftl "ll o tl o\o - o itl -^-^-^ 6 tl E.S xtl K otl ssssssss r3s3sgr€ i -o otl + E OII >\ tl o tl L 9ll -r -- -r otl Nax - -:'- - ^gog-g oI x3s8R8 X3 1g cd ll xtl 9= Ello tl Etl 6^ trtl s6 -.- ::t--rlir -^-.^-,^ :^ K E.E OOOOC)O oO r'-O<+Oo\O oB Flls qs* OOOOOO OO l\O@OooO 6 7ll a -il L -o ;il d N ;il o o\ tril >' € il .. !il = -E '^a *8 Eilg Ae e^q^q^ ?^ Y^Y^Y^ Y^ !il o vo -ONO-O NO ?il-o .'l Fo €lla s n= qR 8ll.= t H> o\o ':! 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Fig.2. Annual slide positivity rate and slide falcipa- Fig. 3. Annual parasiteincidence and annual falcipa- rum rate from 1986 to 1998 in 1 control and 3 experi- rum incidence from 1986 to 1998 in I control and 3 ex- mental zones. perimental zones.
tibility level when the selection process was with- ticide policy, DDT is replaced by HCH and if re- drawn for about l0 years. sistance to both these insecticides is detected, they are replaced by malathion. In areas where resis- tance to DDT HCH, and malathion is reported, use Epidemiological evaluation of synthetic pyrethroids is recommended. The cost Epidemiological indicators are presented in Figs. of HCH is almost double that of DDT and, further, 2 and 3. The initial indoor residual spraying of del- malathion or a synthetic pyrethroid are 3 times tamethrin at 12.5,20, and 25 mg/m2 in zones I, II, more costly than DDT which is still the cheapest and III, respectively, resulted in drastic reduction of insecticide for the malaria control program. A plan all epidemiological indicators during the spraying was made to phase out use of DDT in India. How- years (1986-88) in comparison to the control PHC. ever, because of existing manufacturing capacity in The residual spraying was completely withdrawn India and large stockpiles, use of DDT is allowed from 1989 onward. However, all indicators (i.e., in the public heath program up to 2008. The DDT SPR, SFR, API, and AFI) remained low up to 1993 replacement options are now restricted to either in all zones, followed by a gradual increase in sub- malathion or synthetic pyrethroids. The cost of sequent years. The impact was highly pronounced these insecticides also is similar. However, mala- when AFI was compared. The AFI remained below thion is not socially and environmentally acceptable 2 up to 5 years in deltamethrin-sprayed areas. Sta- because of its unpleasant odor, staining of walls, tistical analysis revealed that the difference in both and environmental pollution. The present study re- API and AFI up to 1995 was highly significant (P vealed that the hazardous burden of DDT in the > 0.005). The impact gradually started diluting environment can be reduced by selective use of from 1996 onward. Nevertheless, the SFR remained synthetic pyrethroids, which have broad-spectrum (4 even after l0 years of withdrawal of spraying. activity and appear to be cost-effective, provided Marginal increases in SFR, API, and AFI may be that the room coverage is more thart 9OVo and cor- attributed to frequent movement of the population rect dosages are used. The deltamethrin at 2O or 25 for social and economic reasons. Further relapses mg/mz has produced desirable entomological and in patients with P. vivax might have occurred be- epidemiological impact, even after withdrawal of cause of insufficient or irregular medication. Me- insecticide for about 10 years, against An. culici- teorological data remained more or less stable dur- facies (Ansari et al. 2001). However, the impact of ing the study period. The mean precipitation in deltamethrin on Cx. quinquefasciatas diluted rap- deltamethrin-sprayed areas was 1,147 mm, as com- idly when compared to that of An. culicifacies, pared to 1"063 mm recorded in the control area dur- which may be due to rapid development of resis- ing 1989-98. tance in Cx. quinquefasciatus. The development of resistance to synthetic pyrethroids is primarily due to tlre kdr gene, a recessive knock-down-resistance DISCUSSION gene that also shows cross-resistance to DDT in C-r. The strategy of National Anti Malaria Pro- quinquefasciaras (Halliday and Georghiou, 1985). grarnme (NAMP) is to carry out indoor residual The species is resistant to DDT, HCH, and mala- spraying in rural areas, with DDT HCH, malathion, thion in Maharashtra, Gujarat, and Haryana (Shar- or synthetic pyrethroids to interrupt the transmis- ma and Samnotra 1962, Rajagopal 1977, Sharma sion of malaria. The criteria for change of the in- 1987); therefore, deltamethrin should be sprayed in secticides are detection of resistance under field multiresistant areas continuously for 3 years and conditions or inadequate effectiveness of the insec- subsequently withdrawn to prevent epidemics up to ticide in a particular district or state. As per insec- 10 years and also to reduce the risk of occurrence 428 JounNer- op rng AugntcaN Mosquno CoNrroL AssocrATroN Vol. 20, No. 4 of pyrethroid resistance. The cost of indoor residual tance of S. N. S. Kachhawaha, K. C. pushap, Janak spraying with different insecticides have been es- Singh, Santosh Vashistha, B. D. Sati, M. D. Tiwari, timated by Phillips and Mills (1991) in Nepal and M. R. Sethi, U. Sreehari, and Sharadchandra War- Konradsen et al. (1999) in Sri Lanka, and recently kade is gratefully acknowledged. We are also was reviewed by Walker (2000). Although DDT thankful to the Director of the Malaria Research still emerged as the cheapest insecticide, the envi- Centre for providing necessary facilities to conduct ronmental impact and human safety of DDT remain this study. major concerns. Moreover, the cost of DDT is in- creasing because of a decline in production and the cost of synthetic pyrethroids is showing a down- REFERENCES CITED ward trend. Insecticide and operational costs vary considerably because of differences in production Abbott WS. 1925. A method for computing the effective- ness of an insecticide. J Econom Entomol costs, equipment, transportation, wages, and orga- 18:265-267. Ansari MA, Sharma VR Batra CP, Razdan RK, Mittal pK. nizational costs. Therefore, the most cost-effective 1986. Village scale trial of the impact of deltamethrin insecticide in any given area or country should be (K-othrine) spraying in areas with DDT and HCH re- determined by considering local situations. In India, sistant Ar?. culicifacies. 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