Mem lnst Oswaldo Cruz, RIO de Janeiro, Vol. 92(l): 1-8, Jan./Feb. 1997 1

Chagas Disease Vector Control in Tupiza, Southern Bolivia

G Cuillen”, R Diaz, A Jemio*, J Alfred Cassab**, C Teixeira Pinto***,CJ Schofield ****/+

Proyecto de Desarrollo Agropecuario Cotagaita San Juan de1 Oro, Componente Salud, Calle Suipacha, Tupiza,Bolivia * Secretaria National de Salud, Direccien National de Vigilancia y Control de Enfermedades y Riesgos,Capitan Ravelo 2 199, La Paz, Bolivia **Asociacion Fundacion Pro-Vida y Salud (PROVISA), Casilla I41 12,La Paz, Bolivia ***Hoechst Schering AgrEvo do Brasil, Av. das Nacdes Unidas 18001, 04795900 Sao Paulo,

SP, Brasil ****Department of Medical Parasitology, London School of Hygiene and Tropical Medicme,London WCI E7HT, UK

Heavy domestic andperidomestic infestations of Triatoma infestans were controlled in two villagesin southern Bolivia by the application of deltamethrin SC25 (2.5% suspension concentrate) at a targetdose of 25 mg a.i./m? Actual applied dose was monitored by HPLC analysis ofjlterpupers placed atvarious heights on the house walls, and was shown to rangefrom 0 to 59.6 about a mean of 28.5 mg a. i./m? Wall bioassays showed high mortality of T. infestans during the$rst month after the application ofdeltamethrin. Mortality declined to zero as summer temperatures increased, but reappeared with theonset of the following winter. In contrast, knockdown was apparent throughout the trial, showing nodiscernible temperature dependence.

House infestation rates, measured by manual sampling and use ofpaper sheets to collect bugfaeces,declined from 79% at the beginning of the trial to zero at the 6 month evaluation. All but one of thehouses were stillfree of T. infestans at the$nal evaluation 12 months after spraying, although a smallnumber of bugs werefound at this time in 5 of 355peridomestic dependencies. Comparative cost studiesendorse the recommendation of large-scale application of deltamethrin, or pyrethroid of similar cost-effectiveness, as a means to eliminate domestic T. infestans populations in order to interrupt transmis-sion of Chagas disease.

Key words: Triatoma infestans - Chagas disease - vector control - pyrethroids - Bolivia

Bolivia has amongst the highest indices ofChagas disease in the Americas. Between 1.1 and1.8 million people are believed to be infected withthe causative agent, Typanosoma cruzi, whichrepresents over 15% of the 1990 population (PAHO1984, Valencia 1990, WHO 1992). The endemicarea comprises around 55% of national territory(about 600,000 km2) where about 3.5 millionpeople are considered at risk to the infection (SNS1994). In highly endemic communities, especiallyin the Departments of Cochabamba, Chuquisaca,Tarija, Santa Cruz and Potosi, seroprevalence ratesmay reach close to 100% in older age groups. Theannual cost of the disease to the Bolivian economy,summing costs of symptomatic treatment for acuteand chronic cases together with estimates of pro-ductive years lost, has been estimated at just overUS$lZO million (SNSKCH 1994).

‘Corresponding author. 7 rue Maclonay, Pregnin, St.Genis-Pouilly, 01630 France. Tel/Fax: +33-4-50.206377Received 1 April 1996Accepted 21 October 1996

Throughout Bolivia, vectorial transmission ofT. cruzi is almost exclusively due to domestic popu-lations of Triatoma infestans, and the distributionof this species closely matches that of the humandisease (Fig. 1). In the absence of satisfactorytherapy or vaccines against Chagas disease, con-trol relies primarily on interrupting transmissionby eliminating domestic populations of T. infestuns.This generally involves insecticide spraying ofdomestic and peridomestic habitats, with or with-out attempts to improve the physical structure ofhabitats in order to eliminate cracks and creviceswhere the vectors may hide. However, althoughvector control has been carried out extensively inother countries of Latin America since the 1950scontrol activities in Bolivia were virtually non-ex-istent until the mid-1980s. Since 1982, severalNGOs and research organizations have been oper-ating projects incorporating aspects of Chagas dis-ease vector control (Table I). This paper reportson one such trial carried out in two villages in south-em Bolivia, near the town of Tupiza, under theauspices of the “Proyecto de DesarrolloAgropecuario Cotagaita San Juan de1 Ore”.

2 Chagas Disease Vector Control l G Guillen et al.

Fig. 1: map of Bolivia showing approximate Departmentalboundaries and estimated distribution of 7”iatoma infestans(shaded). Project area in southern Bolivia is indicated by solidsquare.

TABLE IActivities against Chagas disease vectors in Bolivia,

up to March 1995’

Houses Houses Totalsprayed sprayed and

only improved

Cochabamba 4524 3924 8448Chuquisaca - 4623 4623La Paz 301 301Potosi 2731 26039 b 28770 bSanta Cruz 753 1604 2357Tariia 103 103

a: source - Bolivian presentation to 4th Meeting of theIntergovernment Commission for the Elimination ofTriatoma infestam, Asuncion, March 1995.b: includes 23,649 houses treated by the ProyectoCotagaita San Juan de1 Oro.

MATERIALS AND METHODS

Background and trialprotocol - The Project0de Desarrollo Agropecuario Cotagaita San Juan de1Oro (here abbreviated to P Cotagaita) was set upin 1982 through a cooperative agreement involv-ing several different agencies (including FIDA,OPEC, CAF, and the Government of the Nether-lands) (P Cotagaita 1994). It was primarily de-signed to improve the agricultural basis of the threesouthernmost provinces of the Department ofPotosi: Nor Chichas (capital = Cotagaita), SudChichas (capital = Tupiza), and Modesto Omiste

(capital = Villazon). Since 1986 however, theproject has included a component of Chagas dis-ease vector control based partly on insecticidespraying and partly on house improvement. Todate, 23,649 houses have been sprayed andlor im-proved as part of these activities, and communityorganizations have been set up to maintain vigi-lance and report any reinfestation by T. infestans.

Although deltamethrin SC25 has been the pri-mary insecticide used by the P Cotagaita againstChagas disease vectors, the project provided op-portunity for a detailed trial and evaluation of thisformulation against T. infestans. The trial proto-col was submitted to and approved by the WHOPesticide Evaluation Scheme (WHOPES) in Feb-ruary 1994, and was also approved by the Boliv-ian Secretaria National de Salud (SNS) and the PCotagaita authorities for initiation in June 1994.The trial protocol specified complete indoor andoutdoor spraying of all dwellings and peridomestichabitats in the trial communities, using deltamethrinSC25 (2.5% suspension concentrate) at a targetdose of 25 mg a.i./m2. Filter papers were to befixed to the walls of a sample of houses for subse-quent analysis of spray deposit, in order to checkfor quantity of insecticide applied.

Evaluation was to include prespray investiga-tion of all houses for evidence of infestation withT. infestans, followed by similar postspray inves-tigations at 1,3,6,9 and 12 months. Houses werealso to be monitored by providing householderswith plastic bags in which to keep any bugs theyfound, and application of paper sheets on housewalls to monitor evidence of bug faecal deposits(Garcia Zapata et al. 1985, Schofield et al. 1986)although in the event, paper sheets were appliedonly to 11 houses. Insecticide deposits were alsoto be monitored by wall surface bioassays in 10houses using laboratory reared fifth instars of T.infestans.

Trial site - The trial was carried out in the twoneighbouring communities of San Jose de la PampaGrande and Entre Rios de Ajnapa. These commu-nities are 3 km apart and lie about 36 km from thecity of Tupiza. Although surrounding villages hadbeen sprayed by the P Cotagaita team during 1989-90, these two communities had not been sprayedbecause of severe flooding during that period. Pre-vious serological studies on 158 people from thesetwo communities (using indirect haemaglutinationand indirect immunofluorescence) had shown amean seroprevalence for T. cruzi of 63% (Fig. 2)with ECG studies revealing one or more abnor-malities in 90% of 58 seropositives, including 12people with complete right bundle branch block.

The trial site is about 2,900 m above sea level,and is an extremely arid region dominated by xe-

Mem lnst Oswaldo Cruz, Rio de Janeiro, Vol. 92(l), Jan&b. 1997 5

only in two of the houses (including one that wasnegative by paper sheets). This shows the sensi-tivity of the paper sheet method, and indicates thatinitial infestation rates were in fact higher than in-dicated by prespray manual sampling. However,subsequent examination of the paper sheets re-vealed no new faecal streaks after the spraying,suggesting that live bugs were either absent or un-able to obtain bloodmeals.

Manual capture reports indicated 14% and 17%residual infestations in houses after 1 month, inSan Jose and Entre Rios, respectively. In contrast,no bugs were found by manual sampling from anyof the houses at the 3 or 6 month evaluations. Atthe 9 month evaluation, a single live adult T.mfestuns was found in one house in Entre Rios,and the same house was also positive at the 12months evaluation when bugs (three adults, two4th instars and one 3rd instar) were also found inperidomestic habitats of two other houses in En-tre Rios and three in San Jose (Table IV, Fig. 4).

Fig. 4: house infestation rates for Triatoma infestam in SanJose and Entre Rios, before control intervention (month 0)and at successive evaluations. Prespray mfestatlon rates arethe sum of houses shown positive by manual sampling or bypaper sheets to collect fresh bug faeces. However, paper sheetswere negative on all subsequent evaluations.

Wall bioassays - Wall bioassays were carriedout in five houses of each of the two communitiesat 1, 3, 6, 9 and 12 months postspray. The results(Fig. 5) show significant residual mortality after 1month declining to zero at 6 months postspray, butthen rising again for the 9 and 12 month evalua-tions. Knockdown was apparent, especially onshaded interior walls, throughout the evaluationperiod. Control mortalities were zero in each evalu-ation.

Fig. 5: wall bioassays of knockdown at 24 hr, and mortality at24 hr, 7 days and I4 days, following 24 hr exposure of fifthinstar Triatoma infestam to house walls sprayed withdeltamethrin.

DISCUSSION

Because of its importance as the primary vec-tor of Chagas disease, elimination of domestic T.infestans has been given high priority by the south-em cone countries of Latin America (Argentina,Bolivia, Brazil, Chile, Paraguay and Uruguay)(PAHO 1993). The results presented here amplydemonstrate the effectiveness of the vector con-trol methods applied, and accord with similar ex-perience with deltamethrin and similar pyrethroidsin other countries (Pinchin et al. 1980, Diotaiuti &Texeira Pinto 1991). Most houses sprayed with

TABLE IV

Number of houses positive for Triatoma infestans, as evaluated by field teams

San Jose Entre Rios

Houses Houses Houses Housesevaluated positive % evaluated positive %

June 1994 (prespray) 63 48 16 41 29 71July 1994 (1 month postspray) 59 8 14 35 6 17Sep. 1994 (3 months postspray) 47 0 0 33 0 0Dec. 1994 (6 months postspray) 58 0 0 36 0 0Mar. 1995 (9 months postspray) 54 0 0 34 1 3June 1995 (12 months postspray) 56 3 5 34 3 9

6 Chagas Disease Vector Control l G Culllen et al

deltamethrin remained free of detectable infesta-tions for more than 12 months. However, even thelow levels of reinfestation detected at this time pointto the need for continual vigilance and selectiveretreatment where necessary.

The priority accorded to Chagas disease vectorcontrol is amply justified by the medical and eco-nomic impact of the disease (World Bank 1993,Del Rey et al. 1995) and by the calculated nett ben-efits accruing to any investment in vector elimina-tion (Schofield & Dias 1991). But the social ben-efits are also tangible, as shown by interviews withhouseholders in the two villages studied here. Priorto the control interventions, house infestation rateshad been so high that many people had beenobliged to sleep outside their houses because ofthe biting nuisance. Irrespective of the disease risktherefore, householders manifested extreme grati-tude for the control interventions, which allowedthem to make full use of their houses without theannoyance of bug infestations. Householders alsoappreciated the elimination - at least for the sum-mer months - of other domestic insect pests, espe-cially houseflies and fleas.

The initial intervention for this trial was car-ried out in June 1994, one of the coldest of thewinter months when T. infestans populations areat their most vulnerable (Gorla 1988). At this time,the deltamethrin was highly active and remainedso until July when its insecticidal activity (as mea-sured by wall bioassays) began to decline. Of par-ticular interest however, is that whereas knockdownactivity declined consistently but gently during the12 month course of the trial, insecticidal activitydeclined very markedly with the onset of summeronly to rise again during the following winter (Fig.5). This kind of inverse temperature dependencehas been noted for other pyrethroids (and is well-known for DDT) although it seems to vary bothwith the pyrethroid and with the insect species, andnot all combinations show negative temperaturedependence as seen here (Miller & Salgado 1985).Nevertheless, we feel that temperature dependenceis an important, but often overlooked, factor in as-sessing different products for their activity againstTriatominae.

Since earliest trials of organochlorine insecti-cides against domestic Triatominae (Dias &Pellegrino 1948, Romaiia & Abalos 1948) it hasbeen assumed that highly residual formulationswere required (Pinchin & Schofield 1979). Indeed,much effort has been expended to develop residualformulations, for example using slow-release la-tex or PVA matrices (Oliveira Filho 1988). How-ever, while it is clear that previously-used orga-nochlorine insecticides such as BHC or dieldrinhad greater stability and more prolonged residual

action, it is also becoming clear that pyrethroidssuch as deltamethrin are much more effective ineliminating domestic populations of Triatominae.In the results presented here, for example, all butone of the houses remained free of detectable in-festations for 12 months, even though the superfi-cial lethality of the product (as revealed by wallbioassay) had declined to low levels after 3 months.It may be, therefore, that the effectiveness of mod-em pyrethroids such as deltamethrin rest more withtheir initial impact in quickly eliminating domes-tic infestations, rather than in any longer term ef-fect designed to inhibit reinfestations (after all, re-sidual activity becomes irrelevant if there are nobugs left to kill). This in turn would imply that themost effective control strategy would involve widegeographic coverage in order to eliminate possiblesources of reinfestant bugs, rather than repeatedspraying to eliminate reinfestations.

For the trial reported here, we are unable toassess with certainty the source of the reinfesta-tions. Neighbouring communities - of which thenearest was about 5 km away, on the other side ofthe Rio San Juan de1 Oro - had been sprayed pre-viously and were being periodically evaluated,making them unlikely sources for the reinfestationsin Entre Rios and San Jose. In Entre Rios, the singlehouse where reinfestant bugs were found at the 9and 12 month evaluations, was the most distantfrom other occupied houses (about 500 m away).It had a single male occupant who travelled fre-quently to other parts of Bolivia in search of tem-porary work, which may suggest that the reinfestantbugs had been carried by him from another region.However, this house was close to three abandonedhouses which had been sprayed only about theirexternal walls, and which may have housed somebugs untouched by the intervention. Similarly, weassume that the bugs found at the 12 month evalu-ation in three chicken houses and two goat stablesin Entre Rios and San Jose may also have comefrom abandoned houses that had been sprayed onlyover their outside walls. At present, we discountthe possibility of reinvasion from a silvatic popu-lation because no such foci have been reported forthe Tupiza region (Dujardin et al. 1996) and wedid not find evidence of silvatic bugs during ex-amination of rockpiles and cactus stands wherewild rodents had been seen. Moreover, on mor-phometric evidence the reinfestant adult bugs com-plied with the known patterns of domestic bugsrather than with those of silvatic bugs from else-where in Bolivia (JP Dujardin, pers. comm.).

In the trial reported here, the control strategyinvolved insecticide spraying alone, and the twocommunities (24 1 houses in total) were treated bythe five two-man teams within five days (approxi-

Mem /nst Oswaldo Cruz, Rio de Janeiro, Vol. 92(I), Jan./F&. 1997 7

mately ten houses per day per team). Elsewhere inthe project area however, the control strategy alsoincluded elements of house improvement as a pre-requisite for spraying. This strategy was in re-sponse to the policies of the World FoodProgramme (WFP) which supported the Chagascontrol activities mainly through donations of foodaid given to householders as incentive to carry outthe house improvement work. Estimates carriedout elsewhere in the P Cotagaita area indicate thathouse improvement plus spraying required ap-proximately ten man days per house (excluding thework of the householders themselves) at an aver-age cost per house of 475 pesos bolivianos (approx.US$ loo), compared to less than a quarter man-dayper house for insecticide treatment alone at an av-erage cost of 235 pesos bolivianos per house(approx. US$49 per house) (Table V).

TABLE V

Proyecto Cotagaita San Juan del Oro: estimatedaverage costs per house treateda

Bolivianpesosb

Insecticide 168.00Operational costs (transport, per diems, etc.) 67.00Value of WFP Food Aid 120.00Local labour and mterials forhouse Improvement 120.00Total 475.00

a: source - P Cotagaita (1994); b: US$ I .OO = approxi-mately 4.76 Bolivian pesos

Clearly, improved housing is a valid objective,especially for poorer rural areas. But to includethis as a prerequisite for vector control brings fewadvantages. There may be a marginal improve-ment to insecticide performance on improved less-porous wall surfaces, and in some cases the im-provements may restrict the number of restingplaces for the triatomine bugs (Schofield &Marsden 1980). However the disadvantages aresubstantial. Firstly, the improvements themselvesdo not and cannot eliminate domestic bug popula-tions, since they cannot be carried out to a suffi-ciently high standard because of the cost implica-tions, but nevertheless the improvements do rep-resent a major cost in time as well as direct eco-nomic terms, leading to much slower implementa-tion of direct action against the vectors. Most im-portantly, there will always be, in any poor com-munity, families who enter without the possibilityto build a high quality house, so that programmesof house improvement can never keep pace withthe creation of new domestic sites at risk to bug

infestation. In contrast, insecticide application -without the constraint of concurrent house im-provement work - can be rapid, effective, and cankeep pace with erection of new buildings. Then,once domestic bug populations have been elimi-nated from within a community, house improve-ment programmes can proceed at their own pace,with no risk of reinfestation provided sufficientgeographic coverage has been achieved by the in-secticide programme to eliminate potential foci ofreinfestant bugs.

The work of the P Cotagaita has amply illus-trated this conclusion. The area of trial (San Juanand Entre Rios) had not been subject to house im-provement, and yet bugs appear to have been vir-tually eliminated, and the cost was much lower thanthat of other areas where house improvement wasbeen included in the control strategy. It must there-fore be recommended that the methodologyadopted by the trial be adopted as the primary ap-proach to large scale elimination of T. in&tans,and that such a programme be divorced from par-allel programmes of house improvement.

ACKNOWLEDGEMENTS

To the authorities and villagers of San Jose de laPampa Grande and Entre Rios de Ajnapa for their assis-tance and support for this work. To all those involved inthe control interventions and evaluations, especially JoseLuis Chambi, Raul Prieto, Octavia Colque, Albert0Leon, Francisco Solozano, Simon Flares, Willi Floresand Roberto Lopez. Analysis of spray deposits was car-ried out at Agrevo Environmental Health, Berkhamsted,UK.

REFERENCES

Dias E, Pellegrino J 1948. Alguns ensaios corn o“gammexane” no combate aos transmissores dadoenca de Chagas. Brasil Medico 62: 185- 19 1.

Del Rey EC, Basombrio MA, Rojas CL 1995.Beneficios brutos de la prevention del mal deChagas. Castanares (cuadernos de1 IIE) 4: I-75.

Diotaiuti L, Texeira Pinto C 1991. Susceptibilidadebiologica do Triatoma sordida e Triatoma infestansa deltametrina e lambdacyhalotrina em condicoes decampo: Rev Sot Bras A4ed Trop 24: 15 1-l 55.

Dujardin JP, Schofield CJ, Tibayrenc M 1997. Popula-tion structure of Andean Triatoma infestans: anisozymic study and its epidemiological relevance.Med Vet Entomol (in press).

Garcia Zapata MT, Schofield CJ, Marsden PD 1985. Asimple method for detecting the presence of livetriatomine bugs in houses sprayed with insecticides.Trans R Sot Trop Med Hyg 79: 558-559.

Gorla DE 1988. Seasonal effects on control strategiesof Chagas disease vectors. Rev Arg Microbial 20(supl): 71-80.

Miller TA, Salgado VL 1985. The mode of action ofpyrethroids on insects, p. 43-77. In JP Leahey ThePyrethroid Insecticides, Taylor & Francis, London.

8 Chagas Disease Vector Control l G Curllen et al.

Oliveira Filho AM 1988. Development of insecticideformulations and determination of dosages and ap-plication schedules to fit specific situations. Rev ArgMicrobiol20 (supl): 39-48.

PAHO 1984. Status of Chagas disease in the region ofthe Americas. P.4HO Epidenziol Bull 5: 5-9

PAHO 1993. Iniciativa de1 Cono Sur. PAHO documentno. PNSP/92-18. rev. 1. Pan American Health Orga-nization, Washington DC, 36 pp.

Pinchin R, Oliveira Filho AM de, Fanara DM, Gilbert B1980. Ensaio de campo para avalia@o daspossibilidades de uso da decametrina (OMS 1998)no combate a triatomineos. Rev Bras MalaviolDoeqas Trop 32: 36-41

Pinchin R, Schofield CJ 1979. The design of insecti-cides for the control of domestic vectors of Chagasdisease. II Congress0 International sobre a Doeqade Chagas, Rio de Janeiro, Brazil.

P Cotagaita 1994. Ejecucidn de Proyectos de DesarrolloRural. Proyecto Cotagaita San Juan del Oro, Tupiza.439 pp.

RomaAa C, Abalos JW 1948. Action de1 Gamexanesobre 10s triatomideos. Control domiciliario. AnalesInst Med Reg Tzrcunzan 2: 95-106.

Schofield CJ, Dras JCP 1991. A cost-benefit analysis ofChagas disease control. Menu hut Oswald0 Cruz 86:285-295.

Schofield CJ, Marsden PD 1980. The effect of wall plas-ter on a domestic population of Trlatoma znfestans.WHOiVBCi80.757, World Health Orgamzation,Geneva.

Schofield CJ, Williams NG, Knk ML, Garcia ZapataMT, Marsden PD 1986. A key for tdentifymg faecalsmears to detect domestic infestations of trratommebugs. Rev Sot Bras A4ed Trop 19: 5-8.

SIFS 1994. Programa Naclonal de Control de Chagas.Bohvza. Ministerio de Desarrollo Humano, SecretartaNational de Salud, La Paz, 29 pp.

SNXCH 1994. Chagas Dueuse in Bolzvza. CCH-USAID La Paz, 93 pp.

Valencia A 1990. lnvestzgacidn EpidenzlologxaNational de la Enfevmedad de Chagas. Ministeriode Previson Social y Salud Publica, La Paz, 184 pp.

WHO 1992. Control ofchugas Dueuse. Technical Re-port Series 811. WHO Geneva, 95 pp.

World Bank 1993. World Development Report 1993.Investmg in Health. Oxford University Press, NewYork, 329 pp.