Evaluation of the Chagas’ Disease Vector Control Program in , Brazil, with Special Reference to Triatoma sordidal

LILBIA DIOTAIUTI,~ OSMAR RIBEIRO DE PAULA,~ PATRICIA LIMA FALCAO,~ & Joiio CARLOS PINTO DIAS~

444

As of 2979, data gathered by the Chagas’ Disease Control Program (CDCP) in the Brazilian state of Minus Gerais indicated that Triatoma infestans was the Chagas’ disease vector most commonly found in and around human dwellings. A decade later, however, this picture had changed, presumably as a result of control efforts; few specimens of T. infestans were collected; and Triatoma sordida had become the most commonly collected vector insect. The aim of the work reported here was to assessthe effecfiveness of fhe CDCP in Minus Gerais in 1979-1989, with special referencefo T. sordida. For this purpose, 1979-1989 triatomine collection data were reviewed for the two Minus Gerais health districts (Mantes Claros and ) believed to have the heaviest T. sordida infestations. In addition, 1987 dafafrom a serologic survey for human Trypanosoma cruzi infecfions in seven municipalities of these regions were compared with earlier (1978) serologic data from the same locales. In general, the triafomine collection data documented the precipitous decline of T. infes- tans in and around human dwellings. They also indicated that while the T. sordida collections had remained stable (in Uberaba) or increased markedly (in Mantes Claros), fhere had been no great upsurge in the numbers of T. sordida collected inside dwellings. It was concluded that control measures were preventing extensive house reinfestations in both Mantes Claros and Uberaba; that the situation in Uberaba was relatively stable; and that the marked increase in T. sordida populations around homes in was associated with forest clearing and changing settlement patterns. A marked drop in the incidence of human T. cruzi infections, indicated by comparison of the 1978 and 1987 serologic surveys, provided further supporting evidence that the control program activities carried out in this period were effective.

t the beginning of the 198Os, the captured under the National HeaIth A apparent prevalence of human Cha- Foundation’s Chagas’ Disease Control gas’ disease cases in Minas Gerais State Program (CDCP), with 84.4% of that total (obtained by surveying a rural popula- being captured inside dwellings. The in- tion sample in 717 municipalities) was fection rate of these bugs with Trypano- found to be 0.8% (1). Official reports at soma cruzi was 10.3%. the time indicated that Triufoma infesfans Triatoma sordida accounted for 28.6% of accounted for 64.6% of the triatomines the triatomine captures. Three-quarters

‘This article will also be published in Spanish in 3National Health Foundation, Ministry of Health, the Boletin de la Ojicina Sanitaria Panamericana,Vol. , Brazil. 118, No. 1, January 1995. 4Ren6 Rachou Research Center, Belo Horizonte, ZRene Rachou Research Center, FIOCRUZ, C.P. 1743, Brazil. CEI? 30.190, Belo Horizonte, Minas Gerais, Brazil; 5Rene Rachou Research Center, Belo Horizonte, and Minas Gerais Federal University, Department of Brazil; and Minas Gerais Federal University, School Parasitology, Belo Horizonte, Minas Gerais, Brazil. of Medicine, Department of Clinical Medicine.

Bulletin of PAHO 2813), 1994 211 (75.6%) of these insects were captured in agricultural use, making production for areas around dwellings, and 2.4% were public health purposes economically im- found infected with T. cruzi. practical. In searching for alternative in- The third most common species in terms secticides, a series of tests was run using of numbers captured was Punstrungyhs pyrethroids, which were found superior to megistus, which accounted for 18.5% of BHC (4)7 in terms of being biodegradable, the captures. Most (70.7%) of these bugs protecting the home for longer periods of were captured in areas around resi- time, offering greater knock-down power, dences, and 2.0% were found infected having low toxicity for humans and do- with T. cruzi. mestic anirnal~,~ leaving no residue on walls, T. sordida, a species whose endemic and being odorless (which helps ensure center is Brazil’s densely vegetated scrub- better acceptance by the population). lands (“cerrado”) (2), is widespread Therefore, pyrethroids were firmly in- throughout the country. Indeed, in terms corporated into the CDCP (3). of post-spray captures made under the The purpose of the present study was CDCP, nationwide 1983-1985 observa- to assess the effectiveness of the CDCP tions indicated that T. sordida was then in Minas Gerais between 1979 and 1989, the most commonly captured triatomine with special reference to T. sordida, and species in the country.6 Despite this, at on that basis to propose alternative or the time little was known of this triato- additional elements for the program. mine’s role in the epidemiologic profile of Minas Gerais as a vector of Chagas’ MATERIALS AND METHODS disease in humans. As part of its basic working method- Secondary data from the CDCP (Na- ology, once or twice a year the CDCP (3) tional Health Foundation, Minas Gerais) performs residual insecticide sprayings were used to calculate the “capture in- of triatoma-infested homes and their im- dex,” defined as follows: mediate surroundings until the percent- age of infested households falls below No. of triatomines 5%, and until no T. infestans are observed Capture = captured x 100 in areas where the occurrence of this spe- index No. of households cies has been noted. A system of epide- surveyed during miologic surveillance is then instituted the period whereby National Health Foundation workers spray triatomine foci identified by household residents, who provide no- tification of such foci through a local in- 7Dias JCP, Chedvilli JM, Vasconcelos JVA. Emprego da decametrina contra triatomineos brasileiros em drea formation network. endCmica. Paper presented at the XVII Congress of Until 1985, the CDCP sprayed with the Brazilian Tropical Medicine Association, Cal- benzene hexachloride (BHC). In 1984, das Novas, Brazil, 1981; and Dias JCP, Benedito however, this pesticide was banned for VA, Vasconcelos JA, Diotaiuti L. Ensaio de campo corn permetrina e cipermetrina contra triatomineos em Minas Geruis, Brasil. Paper presented at the XX Congress of the Brazilian Tropical Medicine As- 6Dias JCP, Silveira AC, Cunha RA. kdices triutom- sociation, Salvador, Brazil, 1984. inico~tripanosbmicos observados no Programa de Con- BDias JCP, Benedito VA, Vasconcelos JA, Diotaiuti bole da Doeqa de Chagas (SUCAM) em ambienfe dom- L. Ensaio decampo corn permetrina e cipermetrina contra iciliar, no Brasil, de 1983 a 1985. Paper presented at triatomineos em Minas Gerais, Brasil. Paper presented the XXIV Congress of the Brazilian Tropical Med- at the XX Congress of the Brazilian Tropical Med- icine Association, Manaus, Brazil, 1988. icine Association, Salvador, Brazil, 1984.

212 Bulletin of PAHO 28(3), 1994 Since the regions of the Montes Claros collected from 2 135 subjects in the Trian- and Uberaba health districts (shown in gulo Mineiro and 132 in Mato Verde. Figure 1) were found to be infested pre- dominantly by T. sordida in 1989, they RESULTS were selected as the subjects of a longi- tudinal study covering the 1979-1989 pe- Table 1 shows the numbers of triatom- riod. A new stage of the CDCP had been ines captured by the CDCP in Minas Ge- launched in the “Triangulo Mineiro” (the rais in 1979 and 1989. As may be seen, western area of Minas Gerais State be- after this decade of CDCP activity the tween the Paranaiba and Grande Rivers relative proportions of captured T. infes- corresponding roughly to the area of tans, T. sordida, and P. megisfus had Uberaba) in 1976 and in Montes Claros changed dramatically. in 1979. The response of these triatomines to To assess the impact of the CDCP, ser- spraying in Montes Claros and Uberaba ologic surveys were carried out in six mu- is shown in Figure 2. In Montes Claros nicipalities within the Triangulo Mineiro (northern Minas Gerais), the overall cap- (Itapagipe, Conceicao das Alagoas, Sao ture index for T. infestans plummeted from Francisco de Sales, Capinopolis, Doura- 46.5 in 1979 to levels of 5 or less from doquara, and Cachoeira Dourada) and in 1982 onward. This was accompanied by one municipality of northern Minas Ge- parallel drops in the household capture rais (Mato Verde). Sample size determi- index and the overall infection rate of the nation followed the guidelines presented insects with T. cruzi. in a WHO document (5), using preva- In Uberaba (Triangulo Mineiro), the lences published in 1984 (1). overall capture index for T. infestans was Blood was collected in 1987 by fingertip 0.9 in 1979 (Figure 2D). This index fell to puncture and absorption onto filter pa- virtually zero from 1984 onward, reflect- per. The samples were subsequently ing captures of 19, 5, 5, 7, 5, and 10 tria- processed by indirect immunofluores- tomines per year, respectively, from 1984 cence (6), considering as positive a titer through 1989. of 1:40, the same used in the National The observed P. megistus population also Serologic Survey (1). In all, blood was fell sharply, especially in Montes Claros (Figure 2B). As may be seen, the overall Figure 1. A map of Minas Cerais State capture index in Montes Claros fell from showing the administrative divisions of the 2.6 in 1979 to 0.2 in 1989. Regarding National Health Foundation, including the household captures, the index dropped districts of Montes Claros and Uberaba. from 1.0 in 1979 to values approaching zero in 1989, with a corresponding de- crease in the overall infection rate of the -2OOKm insects with T. cruzi. These data indicate some residual presence of P. megistus re- mained in 1989, mainly in areas outside but near homes. The observed P. megisfus population fell more slowly in Uberaba (Figure 2E) than in Montes Claros, though the overall cap- ture index did eventually decline to 0.8 (from 2.4 in 1979) and the household cap- ture index dropped from 1.0 to 0.1. There

Diotaiufi et aI. Chagas’ Disease Vector Control 213 Table 1, Triatomine captures in Minas Gerais State in 1979 and 1989 by the National Health Foundation, Ministry of Health, Coordinating Office for Minas Cerais, Chagas’ Disease Control Program. Insect specimens Positive Year Species No. captured No. examined No. (%I 1979 Triatoma infestam 55 713 47 401 4 a73 (10.3) I, J. sordida 30 404 25 330 597 (2.4) 0 Panstrongylus megistus 19 644 13 072 257 (2.0) ,, Rhodnius neglectus 365 245 0 - n J. pseudomaculata 240 211 0 ,, J. vitticeps 28 28 0 I, P. geniculatus 20 19 0 I, T. brasiliensis 1 0

1979 total 106 415 86 307 5 727 (6.6)

1989 J. sordida 124 512 80 960 388 (0.5) I, P. megistus 8 254 7 136 139 (1.9) I, J. pseudomaculata 1 339 923 11 (1.2) v R. neglectus 1 254 760 3 (0.4) I, J. vitticeps 805 580 21 (3.6) I, J. infestans 503 298 12 (4.0) I, P. geniculatus 139 57 5 (8.8) J. brasiliensis 19 2 0 - I, P. diasi 10 0 0 - I, J. melanocephala 2 1 0 - ,I Unidentified 69 10 3 (30.0)

1989 total 136 806 90 727 582 (0.6) Source, NatIonal Health Foundation. Mmlstrv of Health: Coordinating Office for Minas Cerals (Chagas’ Dwase Control Program).

was also a consistent rise in the percent- observed, and the household capture in- age of P. megistus infected with T. cruzi, dex showed no long-term trend toward from 2.1% in 1979 to 6.9% in 1987, before household invasion by this species over that percentage declined to 2.6% in 1989. the study period. This increase in the natural T. crtrzi in- For Minas Gerais as a whole, the data fection rate was observed in both adults in Figure 3 show a 68.8% drop in the and nymphs. number of T. infesfans specimens cap- Meanwhile, the observed T. sordida tured in 1981 as compared to 1979, fol- population in Montes Claros shot up- lowing the first two years of spraying. ward, the overall capture index rising from However, the overall T. sordida capture 2.7 in 1979 to levels around 30 during index rose, slowly at first and then faster, 1987-1989 (Figure 2C). However, the mainly as the result of foci located in the household capture index remained rela- immediate vicinity of dwellings rather tively low, and the initial years of the than in them-a situation contrasting with CDCP saw a significant drop in the nat- T. infesfans’ predilection for infesting ural T. cruzi infection rate that persisted dwellings. to a greater or lesser degree through 1989. Regarding the aforementioned sero- In Uberaba this marked overall growth logic survey of 1987, the prevalence of of captured T. sordida (Figure 2F) was not Chagasic infection in 2 135 subjects from

214 Bulkfin of PAHO 28(3), 1994 Figure 2. Household and total (household plus peridomiciliary) capture indexes, and T. cruzi infection rates found for the three species of triatomines captured most frequently by the Chagas’ Disease Control Program (CDCP) in the Minas Gerais districts of Montes Claros and Uberaba, 1979-l 989. Black bars show household capture indexes, stippled bars show total capture indexes, and dots show rates of T. cruzi infection. Source: National Health Foundation, Coordinating Office for Minas Gerais.

A. 7 infestam, Montes Claros B. I? megistus,Montes Claros C. 7:sordda, Montes Claros Captureindex % infected Captureindex % Infected Captureindex % infected 501 l-16 r5 35-I r4 30 -4 25 3 -3 20 2 15 10 1 5 0 ” 79 80 81 82 83 84 85 86 87 88 89 ” ’ 79 80 81 82 83 84 85 86 87 88 89 Year Year Year

D. 7:infestans, Uberaba E. F! megistus,Uberaba F. 7:sordida, Uberaba Captureindex % infected Captureindex % infected Captureindex % infected 30 i-5 301 r8 50 r4 25 4 20 3 15 2 10 5 1 0 0 79 80 81 82 83 84 85 86 87 88 89 79 80 81 82 83 84 85 86 87 88 89 Year Year Year

1 Household @!jTotal +- % infected Figure 3. Numbers of T. infestans and The years of the most recent T. infeskzans T. sordida triatomines captured in Minas captures in each municipality are shown Gerais under the National Health at the bottom of the chart. Foundation’s Chagas’ Disease Control Program (CDCP), 1979-l 989. DISCUSSION AND CONCLUSIONS

According to a 1940 survey done in Minas Gerais State (7), P. megistus ac- counted for 79.8% of the triatomines cap- tured, T. sordida for 9.7%, and T. infestans for 9.3%. The respective rates of T. cruzi infection in these insects were found to be 41.3%, 6%, and 15%. As of 1951 the 1979 1981 1983 1985 1987 1989 situation did not appear to have changed much (a), aside from a noteworthy spread six municipalities in the Triangulo Mi- of T. infestans into the western part of the neiro was found to be 11.9%. The prev- state. alence was quite age-specific, however, Around the end of the 197Os, National ranging from 0.4% among children under Health Foundation data showed that T. 10 years of age to 32.9% among subjects infestans had spread up to the northern over 50. border of Minas Gerais; at that point (see A similar pattern was found in the mu- Table 1) this bug accounted for nearly nicipality of Mato Verde, where the prev- twice the number of triatomine captures alence of Chagasic infection among the as did the next most commonly captured 132 people examined was found to be species, T. sordida (28.6%), which in turn 11%. Only 1 child under 10 years old (out had pushed P. megistus down into third of 47 children examined in this age group) place on the list (18.5%). No major changes was found to be infected. were noted in the geographic distribution Figure 4 compares these 1987 data for of T. sordida within the state. each municipality with earlier (1978) data During the 198Os, efforts to control T. from the National Serologic Survey (I). infestans in Minas Gerais achieved the same

Figure 4. Human prevalences of T. cruzi infection in seven study municipalities in 1978 and 1987, as indicated by serologic surveys. The most recent year of T. infestans capture in each municipality is shown below the bars.

1981 1981 1980 1979 1982 1982 1989 C. Alagoas Capindpolis C Dourada Douradoquaraltapagipe SF Sales M Verde

Year of last Tinfestmscapture I1978 H 1987

216 Bulletin of PAHO .X%3), 1994 success observed in SBo Paulo (9). The vasion of artificial habitats by T. cruzi- capture index for this species fell off positive triatomines from wild habitats. sharply, accompanied by a drop in the However, the available data revealed an percentage of infected bugs. Dias (10) at- increase in the infection rates of both tributes this to elimination of household adults and nymphs. This noteworthy ob- infestations and the resulting lower servation, which has also been reported household density of the vector. Also in from Bahia State by Italo Sherlock (Gon- the 198Os, reduction of acute Chagas’ dis- gala Muniz Center, FIOCRUZ, 1993, per- ease cases and T. cruzi infections in young sonal communication), merits further patients-undoubtedly the major source investigation. of infection for household triatomines- Turning to T. sordida, the Montes Cla- led to a drop in the overall natural in- ros District showed a marked increase in fection rate of these insects. The lower T. sordida captures in peridomiciliary areas. 1979 capture index for T. infestans in Inside the home, this triatomine did not Uberaba as compared to Montes Claros show-at any time during the period an- (see Figures 2A and 2D) is explained by alyzed-any of the significant densities the fact that the spraying program in that have been observed by Garcia Za- Uberaba had been launched in 1976, sev- pata at Mambai in Goias State (12). (Gar- eral years earlier than in Montes Claros. cia Zapata noted an increase of T. sordida A similar response to the control pro- inside dwellings between 1985 and 1990, gram was seen in the numbers of P. meg- leading to a warning of imminent colo- istus collected in Uberaba and Montes nization by the species in the near future Claros. Early studies had shown that these if control measures were discontinued.) triatomines adapted well to the house- The lower response of outdoor triato- hold environment, especially in the mine populations to control measures is northern part of the state (7, 8, 21). It was to be expected. For one thing, insecti- this mainly domestic population that de- cides deteriorate more rapidly in this en- clined quickly in response to spraying, vironment (13). Also, spraying the entire yielding the lower capture indices shown area around a house is a major under- by National Health Foundation data (see taking that involves removing all the items Figures 2B and 2E). It is not surprising, accumulated there which can facilitate however, that the data also revealed a survival of triatomines in inaccessible residual presence of this triatomine, which hiding places. Active or passive reinva- is native to Minas Gerais and has made sion by wild specimens is another pos- persistent attempts to move into and col- sibility to be considered; and easy access onize new habitats. to food renders areas around dwellings Regarding infection with T. cruzi, in- auspicious for T. sordida colonization, es- fection of P. megisfus in Montes Claros pecially when a continuous food supply displayed a downward trend-easily ex- is offered by such activities as keeping plainable by removal of this species from chickens in coops (24). the artificial habitats that were the main In the Triangulo Mineiro (Uberaba area), targets of the National Health Founda- the maximum level of T. sordida control tion program. In Uberaba, however, the attainable with the National Health rates of T. cruzi infection detected in P. Foundation’s current methods appears to megistus rose. We feel that if there had have been reached. Although more land been higher infection rates in captured is being used for planting crops and pro- adults than in captured nymphs, this ducing charcoal, livestock raising contin- could have indicated an increased in- ues to be the region’s main economic

Diotaiuti et al. Chagas’ Disease Vector Control 217 activity (15). Ecologically, the region transmission of human Chagas’ disease underwent modification some time ago is currently irrelevant in Minas Gerais, as and is currently experiencing fewer in- has also been observed in Sao Paula (9) terventions than the northern areas. As and Mambai (12), a circumstance made a result, less pressure is being exerted possible at great cost in terms of human upon wild T. sordida populations. effort and monetary expense (4, 18). This explains the greater stability of It should also be noted that Brazil’s Uberaba’s T. sordida collection rates over experience in working against Chagas’ the course of the study period. Montes disease has confirmed the effectiveness Claros, on the other hand, has been the and workability of the epidemiologic sur- site of many new colonization projects, veillance system employed (19). How- with forest clearing and expansion of cul- ever, bearing in mind the relationship that tivated areas (14). These projects have exists between peridomiciliary infesta- been very irregular, resulting in uncon- tion and peridomiciliary order, it seems trolled environment interventions (26). As clear that this system should include, be- a result, habitat destruction is forcing wild sides eradication of triatomine foci, es- triatomines such as T. sordida to seek sur- tablishment of a process of discussion with vival alternatives. Despite this circum- the population that over the long run will stance, T. sordida has not established a inculcate a conscious change in behavior marked household presence in the north- encouraging cleanliness in and around ern part of the state-thanks to the con- the home (20). tinued efforts of the CDCP in the area and also to the fact that spraying protects homes Acknowledgments. We would like to for relatively long periods of time (13). thank the Parasitology Laboratory at the The comparison between 1987 preva- Ezequiel Dias Foundation (Fundacao lences of Chagasic infection among hu- Ezequiel Dias-FUNED) for performing mans in seven municipalities (see Figure the serologic tests, Dr. Carlos Mauricio 4) and those found in 1978 by the Na- Antunes for his assistance with sample tional Serologic Survey (I) points to a size determination for the serologic sur- marked drop over this period. The fact vey, and the National Health Foundation that the decline was roughly concurrent for granting us access to archives as well with the T. infesfans control activities de- as for its invaluable support in the study scribed would seem to reinforce data in- areas. dicating that this insect is the principal vector of Chagas’ disease in the region. One conclusion to be drawn from the REFERENCES reported data is that the CDCP has been 1. Camargo ME, Silva GR, Castilho EA, Sil- successful in areas infested predomi- veira AC. Inquerito sorol6gico da preva- nantly by T. sordida under the peridom- lencia da infeccao chag&ica no Brasil, 1975- iciliary colonization conditions we have 1980. Rev lnst Med Trop %o Paula 1984; observed. According to Martins (17), 26(4):192-204. “human infection in an endemic form is 2. Forattini OP. Biogeografia, origem e dis- only possible in regions where domicili- tribui@o da domiciliacso de triatomineos no Brasil. Rev Salide Pliblica 1980;14:265- ary triatomines exist.” The CDCP has 299. prevented any such colonization, or else 3. Dias JCP. Control of Chagas’ disease in has kept household densities at very low Brazil. Parasifol Today 1987;3(11):336-341. levels, and so has achieved its goal. Under 4. Pinchin R, Oliveira Filho AM, Fanara DM, these conditions, T. sordida’s role in the Gilbert B. Ensaio de campo para avaliacso

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Diotaiufi ef al. Chagas’ DiseaseVector Control 219