Acta Tropica, 60(1995)3-13 3 © 1995 Elsevier Science B.V. All rights reserved 0001-706X/95/$09.50

ACTROP 00475

A field trial with Lambda-cyhalothrin (ICON) for the intradomiciliary control of malaria transmitted

by Anopheles darlingi Root in Rondonia, Brazil

J.D. Charlwood a'*, W.D. Alecrim b, N. Fe b, J. Mangabeira c and V.J. M a r t i n s d

aLiverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK, bHospital de Doen¢as Tropicais, Rua Pedro Teixeira s/n, Manaus, Amazonas, Brazil, ~SUCAM , Ministerio de Saude, Brasilia.,

Distrito Federal, Brasil, dSUCAM, Porto Velho, Rondonia, Brazil

(Accepted 24 March 1995)

A two stage field trial comparing the effects of Lambdacyhalothrin (ICON) and DDT when used as residual sprays on the inside surfaces of houses, was conducted in the Machadinho and Jaru areas of Rondonia, Brazil, in 1987 and 1988. In 1987 houses along two 16 km contiguous stretches of a main and a side road were sprayed and the effects on malaria vectors monitored for the succeeding year. In the second stage approximately 55 000 houses in both districts were sprayed with ICON and the effect on malaria incidence measured by passive case detection. Of the eleven species of Anopheles caught in indoor and peridomiciliary collections A. darlingi was the commonest and is recognised as the most important vector in Brazil. ICON at either of two concentrations in bioassays killed more mosquitoes than DDT at each test from seven to twelve months after spraying. A rise in the number of A. darlingi collected eight months after spraying with DDT was not so marked in the ICON areas. Side effects of the insecticide were limited. The number of reported Plasmodium falciparum cases in the second phase declined 76% in Machadinho after spraying with ICON to 2851 cases. In Jaru there was a 28% reduction. The observed efficacy of the insecticide, its ready acceptance by the local populace, and its cost effectiveness make it a more useful insecticide for anti-malaria campaigns than DDT.

Key words: Brazil; Anopheles darlingi; Control; Residual spray; ICON; DDT

Introduction

Early workers emphasised the domesticity of Anopheles darlingi Root (Davis 1931, Shannon 1933), the main vector of malaria in much of South America, and its eradication from coastal lowland areas of Venezuela and Guyana by indoor house spraying with DDT (Gabald6n 1952, Gabaldrn and Berti 1954, Giglioli 1951) was comparatively easy. Recently, however, malaria in Brazil has been increasing at an alarming rate (from 189318 cases in 1981 to 485357 in 1987 and 614431 in 1991, Malaria Control Program, unpubl.). Over 40% of the cases in 1987 occurred in the State of Rondonia. The mass movement of non-immune settlers into the area, large and small scale deforestation, the temporary nature of many houses and an increasing

*Corresponding author and present address: c/o P.O. Box 53, Ifakara, Tanzania.

SSDI 0001-706X(95)00092-5

emergence of parasite resistance to chloroquine and sulfadoxine/pyrimethamine are among the reasons for this upsurge. The other major difficulty concerns the behaviour of the vector An. darlingi. Throughout most of its distribution A. darlingi is exophilic and often predominantly exophagic (Charlwood and Hayes 1978). When it does enter houses it spends only about ten minutes resting on walls before feeding (Charlwood 1980, Hudson 1984). When those walls have been sprayed with DDT this time may be reduced or the mosquito may avoid them altogether (Hayes and Charlwood 1977, Charlwood and Paraluppi 1978).

Even with an entirely endophagic, endophilic species, for a control programme to be effective the coverage rate of any insecticide should be at least 90% (Bruce- Chwatt 1985). The deposit that DDT leaves on the walls is not welcomed by houseproud settlers who often refuse entry to spray teams. In some areas of the country a 40% refusal rate is not uncommon and, despite education campaigns, this figure is unlikely to improve while DDT or any other product that stains the walls is applied.

The more active synthetic pyrethroids offer a possible solution to some of the problems associated with DDT (Capel-Williams 1991). The relative efficacy of these insecticides against the indoor biting fraction of the mosquito population and ultimate effects on malaria incidence compared to DDT has been investigated in Africa (Mnzava et al. 1993) and Asia (Asinas et al. unpubl., Lin et al. 1994) but not in South America. A two part field trial was therefore conducted with the most potent of these new insecticides, lambda-cyhalothrin (ICON) compared with DDT against malaria vectors and disease incidence. Following a year's entomological assessment, houses in two of the most malarious districts of the state of Rondonia were sprayed with ICON and subsequent epidemiological evaluation undertaken.

Description of Study Site The study took place in the districts of Jaru and Machadinho, Rondonia (Fig. 1 ).

Jaru was the larger of the two. When censused in 1986 its three rural subdistricts contained 16083, 15000 and 20080 people. The area was sprayed with two rounds of DDT in 1987. In the first round 14076 and in the second 15516 out of a possible 19504 houses were sprayed giving a coverage rate of 80% which is higher than that achieved in many other areas of Rondonia.

Machadinho was settled after Jaru and many more of the houses were of a temporary construction, making malaria control by residual house spraying more difficult. In addition there were a number of gold mining sites with inadequate housing in the area. At the time of the trial the rural areas of both Jaru and Machadinho consisted of a nexus of unpaved, all weather roads radiating out from the urban centre. At approximately every two kilometres transverse side roads (Linhas) are built. Most malaria transmission occurs in communities on these side roads which are more recently colonised and more difficult of access.

In the first part of the study (Phase 1) houses along two contiguous 16 km sections of the Jaru-Machadinho Road (BR605), 190 km south of Porto Velho and a side- road were sprayed In one group of 67 houses DDT was used at 2 g/m 2 and in another group of 80 houses ICON was used at 0.025 g/m 2. Sixty three houses in a third group were sprayed with ICON at 0.05 g/m 2. This group of houses were on a recently opened side road which intersected BR605 at the junction of the other two areas (Fig. 1 ). A combined total of approximately 500 people lived in the area.

64,~, f r X. 62o 6oo

"-0"~ "1\ PORTO VEL.H x'°"~)

/--" .... / N i AMAZONAS -~ j ~ ~ ?

r " "~ ~ 1 "~MACHADINHO . STUDY A R E A ~ ( 70 ° 70 ° ~R4SO~ "~.

JARU"~ I MATO OROSSC

B R - 3 6 4

%..% • , •

7 2 o 0 100krn 7 2 °

6 4 ~' 6 2 o I I 1

Fig. 1. Map of the study area showing the location of the section of BR605 used in the first part of the trial and the approximate boundary of the area sprayed in the second part.

The roads were bisected by numbers of small streams and rivers. In some cases substantial wooden bridges had been built across them which meant that the rivers' flow was unimpeded by the road. In other cases, particularly on the side road, where the road crossed a river the flow of water was impeded and small lakes had formed on the upstream side. These lakes provided breeding sites for anopheline mosquitoes.

Many of the settlers locate their houses close to the streams because of the water they provide. Thus, although the population density in the area is low, this associa- tion between man and mosquito enhances malaria transmission. Timber was the usual material used in house construction. Bednets or other anti-mosquito devices were not used by the inhabitants.

In the second part of the trial (phase 2) all houses in the districts of Jaru and Machadinho were sprayed with ICON.

Mosquito collection Landing catches were performed, with the aid of a torch and an aspirator, between

1800 h and 2200 h for seven consecutive nights each month for one year by 16 settlers who were provided with 'Fansidar' prophylaxis. Collectors worked inside or outside their own houses alternating between locations on consecutive nights. Unannounced visits to collectors by supervisory staff were undertaken on collection nights. In the DDT treated area four of the collectors worked until midnight. In addition nightly collections were made for fourteen nights in April and seven nights in May prior to insecticide application. Mosquitoes were placed in netting covered plastic drinking cups and, the following morning or later that night, taken to the

field laboratory where they were identified and the A. darlingi dissected for parity (Detinova 1962).

Once a month contact bioassay (cone) tests were performed by standard WHO (1980) procedure on the wooden walls of houses from the three spray areas. Tests were performed 0.5, 1.0 and 1.5 m above floor level with an exposure time of 30 min. The number of mosquitoes knocked down and dead was recorded at the end of the test and after a 24 hr holding period in non-contaminated plastic cups. It was, unfortunately, not always possible to use solely A. darlingi in the tests, in which case a mixture of anopheline species were used.

Epidemiological evaluation Passive case detection was used to monitor the incidence of malaria in Machadinho

and Jaru in the years before and after spraying with ICON. When people in the areas had fever or felt unwell they could report to one of five malaria control aid posts in Machadinho or one of six in Jaru. One hundred fields of Giemsa stained blood slides were examined at high power for the presence of parasites. Parasites from people who had had treatment for malaria in the previous ten days were considered to be recrudescences. A similar system was in operation throughout the rest of Brazil. The results from the trial areas could therefore be compared to the data obtained in other areas of the state of Rondonia.

Spraying Following two months pre-intervention data collection, house-spraying was under-

taken by the local malaria control workers using Hudson 'X-pert' compression spraypumps. Lambda-cyhalothrin 10% wettable powder was supplied in soluble sachets containing 62.5 g of ICON 10 WP wrapped in waterproof foil envelopes. For filling each sprayer, one or two sachets were added to 10 litres of water in the tank and shaken to a fine suspension after compression. The preparation and mixing of the DDT wettable powder was undertaken according to standard procedures. New nozzles (80.02 tee jet) were used and at an average of 40 psi delivered 700 ml/min. Coverage rates were checked during preliminary trials. Spraymen used disposable paper face masks during spraying. A survey of possible secondary effects associated with the three treatments was conducted amongst both residents and spraymen.

RESULTS

Phase 1 In the first phase of the trial houses were sprayed between 5th and the 8th of

May 1987. Four spraymen and one supervisor performed the spraying in each area. Estimates of insecticide dosage were 2.25 g/m 2 (range 2.5-1.9 g/m 2 ) of DDT and 28.8 mg/m 2 (range 40.6-19.4 mg/m 2) and 52.3 mg/m 2 (range 62.5-40.0 mg/m 2 ) in the two ICON areas.

Seventy seven adults from the area sprayed with ICON at 25 mg/m 2 and 52 from the area in which 50 mg/m 2 had been applied were interviewed about possible side effects associated with the insecticide. All had perceived a reduction in insect pests including cockroaches and other 'beetles'. In the low dose area six people (7.8%)

reported a burning sensation on the face and one person (1.3%) reported sneezing. In the higher dose area these figures were 13 (25%) and 8 (15.3%) respectively. In the low dose area two children sat on a contaminated towel and experienced pruritis in the gluteal area and lower limbs. In the high dose area one person experienced pruritus on the back of the thorax, the dorsal and lumbar areas after lying with without a shirt on a bench that had been sprayed. Another experienced pruritus when he lay down in bed which increased when he scratched his back on the wall treated with ICON.

Among the spraymen no serious cases of skin reaction or other irritation were reported although some initial subjective skin sensations were noticed by some of them. All symptoms were transient and disappeared within a matter of hours or days. Spraymen soon learned how to prevent such symptoms by avoiding personal exposure.

Mosquito collection Chagasia bonnea and 11 species of Anopheles were collected near houses and seven

species of Anopheles were obtained indoors from nightly collections between March l lth and 21st (Table 1). Collectors from houses closest to blocked streams caught the most mosquitoes. In all locations the only species to continue biting indoors after an early evening peak was A. darlingi. (Fig. 2). Parous rates were similar between locations as were those from indoor and peridomiciliary collections (Table 2).

Following insecticide application mosquito population densities in all areas for most of the year were low. Highest densities of all species were reached at the end of the dry season in October-November (Fig. 3). Mean numbers of A. darlingi collected in the DDT and ICON areas were similar for six months of the project.

Bioassays There was no apparent difference in the response to the insecticides by any of the

species used in the tests and so, for the sake of simplicity, all species have been grouped together (Fig. 4). It is apparent that, in the first six months after treatment

TABLE 1

Numbers of mosquito caught in peridomiciliary and indoor landing collections conducted between 1900 and 2200 h between March 1 l th and 23rd

Species Peridomiciliary Indoor Proportion indoor

A. darlingi 328 211 0.39 A. triannulatus 127 9 0.07 A. oswoldoi 54 23 0.30 A. strodei 98 33 0.25 A. minor 21 4 0.16 A. norestensis 65 9 0.12 A. albitarsis 3 0 A. nuneztovari 4 0 A. galvoaoi 11 0 A. bennarrochi 4 1 0.20 AI rangeli 6 0 Ch. bonnae 1 0

100

18.oo 19,00 20.00 Zl.00 22.00 28,00 0.00

T ime (h)

Number oolleotecl

Fig. 2. Number of A. darlingi and other species collected in peridomiciliary landing collections between 1800 and 0000 h

TABLE 2

Number and proportion parous of the Anopheles darlingi caught in peridomicilliary and indoor landing collections

Area PeridomiciliarycoUection Indoor collection Parous A. darlingi/A, sp. rate ratio

NuUiparous Parous Nulhparous Parous

DDT 23 63 19 35 0.68 0.051 ICON 0.025 15 15 6 7 0.51 0.18 ICON 0.05 63 128 - - 0.67 0.45

there was little difference between I C O N at either concentration and DDT, all three giving high kill rates. Between months seven and 11 bioassay mortality on I C O N was always higher than on DDT. The knockdown effect of I C O N was also much more rapid than that of DDT.

Phase 2. The results f rom Phase 1, especially the enthusiastic response to the insecticide

f rom the local residents, were sufficiently encouraging for the second phase to proceed in 1988. Given the efficacy of the insecticide, a dose of 0.03g/m 2 of I C O N was used in this phase of the trial. In the second phase spraying in Machadinho commenced in April by a team of 32 spraymen and was completed by the end of May 1988 (see Fig. 5). This was a little more than six months after the last sprayround of DDT. Only one house out of about 32 000 houses was not sprayed. Spraying in Jaru took longer. It was started in April but did not finish until July. 22 681 houses were sprayed. There were 30 refusals and 825 buildings were closed.

The slide positivity rate f rom an unselected sample of 1993 rural residents in 1987 was 7.3%. The blood slide data f rom people reporting to aid posts or centres in Machadinho and Jaru for 1987 and 1988 before and after spraying are shown in

5

4

3

2

1

0 A

% Mortality

Number collected

" DDT /

ICON 0.025 I

)rMsyJun Jul AugSepOctNovDecJanFebMarApr 87 I 88 !

Date Fig. 3. Williams' mean number of A. darlingi caught per man hour of collection from peridomiciliary

landing collection before and after insecticide application.

100

80

60

40

20

0

Peridomicilliary collections

1 2 3 4 5 6 7 8 9 10 11 12

Month after application

DDT ~ ICON 0.025 ~ ICON 0.05

Fig, 4. Percentage mortality of Anopheles sp.(predominantly A. darlingi) in WHO cone bioassay tests (Columns without a histogram indicate missing data).

10

Number of poeltlve eUdee 2800

2000

18oo I

lOOO

8 o o t

0 I ~ I I I I i I I I I Jan Feb Mar Apr May Jun Jul Aug 8ep Oot Nov Deo

D a t e

Fig. 5. Number of Plasmodiumfalciparum infections diagnosed in Machadinho 1987 and 1988. The arrow indicates approximate time of insecticide application.

Table 4. Malaria rates in Machadinho, the more recently 'developed' area, were higher than in Jaru. There was also more Plasmodium falciparum compared to P. vivax in Machadinho than in Jaru. Many cases of P. vivax are likely to have been recrudescences indicating more active transmission in the latter area.

In both areas a remarkable drop in the number of cases of P. falciparum diagnosed was observed when houses were sprayed with ICON. In Machadinho only 2851 cases of P. falciparum were diagnosed compared with 12 085 in the same months of the previous year, a 76% reduction (Fig. 4). In Jaru a 28% reduction was observed in May-December from 6275 cases in 1987 to 4519 cases in the post spray months of 1988. There was less of an effect on the number of P. vivax infections diagnosed (Table 3) with the result that this became the most common parasite observed. Elsewhere in Rondonia, despite an estimated coverage rate of 74.6% (343095 out of 459832 houses sprayed), cases of both species of malaria showed increases compared with the same months of the previous year in the latter part of 1988 (Table 3).

TABLE 3

Number of malaria cases from Machadinho, Jaru and the remainder of Rondonia in 1987 and 1988 before and after spraying with ICON in May 1988 Machadinho and June/July in Jaru

Month Machadinho Jaru Rondonia

1987 1988 %change 1987 1988 %change 1987 1988 %change

P. fa~iparum 1-4 2636 4123 3561 6984 22490 40417 5-12 12085 2851 -76.4 6275 4 5 1 9 -28.0 7 2 5 1 2 89222 +23.0

P. vivax 1-4 2163 2716 4358 6049 22426 31656 5-12 6935 4807 -30.7 5444 4 9 9 1 -8 .3 66933 78230 +16.9

11

Discussion

Malaria in Rondonia remains the most important health risk to the settlers (Sawyer and Sawyer 1987). Spraying with ICON appears to have greatly reduced the amount of malaria transmitted in Jaru and Machadinho. Although the interpretation of historical controls, especially in such dynamic areas, may be misleading, the observed 28-76% reductions in P. falciparum incidence were contrasted with the 23% increase seen in the rest of Rondonia in 1988. The almost perfect coverage rates with ICON contributed but in 1987 the DDT coverage rate in Jaru was over 80%.

Although in bioassays ICON, even at the lower dose of 0.025 g/m 2, had a longer residual effect than DDT (Fig. 4) it was probably not this that was responsible for its greater impact, since for six months DDT was also virtually 100% effective. These tests were originally devised for work with endophilic mosquitoes. Using the conven- tional exposure time of half an hour the advantageous effect of a rapid knockdown synthetic pyrethroid compared to DDT against a mosquito such as A. darlingi is masked. For a more meaningful test exposure times should be tailored to the behaviour of individual species of mosquitoes. In the case of A. darlingi this would mean exposing the mosquitoes for no more than ten minutes to the insecticide. With 10 mins exposure ICON at 25 mg 2 knocked down and killed most A. darlingi whereas DDT killed none.

Although sporozoite determination was not undertaken and other anophelines in the Amazon region can transmit malaria (Arruda et al. 1986, Branquinho et al. 1993), A. darlingi was the mosquito that conformed to the pattern expected of an efficient vector. Survival rates were sufficiently high for this species to transmit the disease (Table 2), it was also the only species that bit throughout the night and approximately one third of the mosquitoes were caught inside houses. Hence it would be the species most affected by indoor residual spraying. If, as seems likely, there was a single homogeneous population in the study area, the insect would come in contact with the insecticide in one of three oviposition cycles on average. The rapid knockdown of ICON compared to DDT was probably responsible for its greater effectiveness.

Anopheles darlingi has been recaptured more than seven kilometres from a point of release (Charlwood and Alecrim 1989). In many areas of the Amazon there is a high refusal rate to DDT house spraying among settlers. Thus, even if house spraying with DDT was effective and even though houses are often more than a kilometre apart it is possible that unsprayed houses in a region may act as source for reinvasion to other areas. The enthusiastic reception given to ICON implies that coverage rates could be improved and this in itself would perhaps make it a more effective insecti- cide. Indeed the increased coverage was largely driven by settler demand since immediately after spraying all other insects disappeared from houses. Cockroaches, in particular, were seen to crawl out of houses and expire during spraying. It was the elimination of these and other pests that was regarded by settlers as the major benefit of ICON compared to DDT. Other perceived advantages were the absence of staining of the walls, or side effects on domestic animals. A number of residents went so far as to say that they would refuse any future DDT applications even though they had not refused in the past.

Schofield (1992) has recently described some of the hidden costs associated with the purchase of large quantities of DDT compared to the seemingly more expensive

12

pyrethroids. His analysis extended as far as the local storage costs. There are other costs associated with DDT compared to an insecticide such as ICON. It takes 670 g of DDT to charge a pump. This has to be carried for long distances on foot by the sprayman and it has to be mixed in a bucket before being loaded in the pump. This is often performed close to the local stream increasing the chances of environmental contamination. The low dosages of ICON used meant that there was a reduction in the amount of insecticide transported and it enabled the insecticide to be packaged in dissolvable sachets, resulting in the elimination of contact with the insecticide by the spraymen and a reduction in the likelihood of environmental contamination. DDT is also abrasive and nozzle tips rapidly degrade The supply of spare parts for equipment is a major problem for control programs and bad nozzles and leaking pumps were major problems for the spraymen in Machadinho and Jaru. The low dose of ICON results in longer lasting nozzle tips. This not only reduces costs but ensures a more even coverage of insecticide.

As Schofield (1992) and Curtis (1994) argue the continued use of DDT for malaria control is a costly mistake which denies the full application of the most effective methods for mosquito control that have so far been developed. Our results indicate that in Brazil the replacement of DDT with ICON is to be recommended for malaria control purposes.

Acknowledgements

We thank ZENECA Public Health (formerly ICI ) for supplying the insecticide and logistical support; the people of the BR605 and Linha 14, especially Sr. Manuel and his family, for their help and co-operation, and all the malaria control staff of Jaru, Machadinho and Porto Velho.

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