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Triatomine fauna in the state of Bahia, Brazil: What changed after 40 years of the vector-control program?

ABSTRACT

Background:

Neglected tropical diseases are a growing threat to global health, and endemic Chagas disease has emerged as one of the most important health problems in America. The main strategy to prevent Trypanosoma cruzi transmission is chemical control of vectors. This study presents a descriptive analysis of synanthropic triatomines before and after the implementation of a vector-control program in Bahia, Brazil.

Methods:

Descriptive analysis and geospatial statistics were performed on triatomine data, (1) the relative abundance and (2) proportional spatial distribution, from Bahia during two periods: (A) 1957 to 1971 and (B) 2006 to 2019.

Results:

We observed a decrease in the relative abundance of Panstrongylus megistus (A: n=22.032, 61.9%; B: n=1.842, 1.0%) and Triatoma infestans (A: n=1.310, 3.7%; B: n=763, 0.43%), as well as an increase in the relative abundance of T. sordida (A: n=8.314, 23.4%, B: n=146.901, 81.6%) and T. pseudomaculata (A: n=894, 2.5%, B: n=16.717, 9.3%).

Conclusions:

Our results indicate a clear reduction in the occurrence of P. megistus and T. infestans (last record in 2015) and an increase in the relative abundance and geographical distribution of T. sordida and T. pseudomaculata after 40 years of the vector-control program. The high frequency of other triatomine species in the municipalities of the state of Bahia and their abundance in recent years highlight the need to reinforce permanent entomological surveillance actions to prevent Chagas disease.

Keywords:
Triatominae; Northeastern Brazil; Trypanosoma cruzi; Chagas disease; Public health

INTRODUCTION

Triatomines are blood-sucking insects (Hemiptera: Reduviidae) that are vectors of the parasite Trypanosoma cruzi (Chagas, 1909), the etiological agent of Chagas disease, also known as American trypanosomiasis. Some synanthropic triatomine species adapt to anthropic changes within their natural landscape, colonizing the household environment (animal breeding sites) and occasionally inside houses, increasing the risk of T. cruzi transmission11. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas' disease. Bull Am Mus Nat Hist. 1979;163(3):123-520.,22. Galvao C, Justi SA. An overview of the ecology of Triatominae (Hemiptera: Reduviidae). Acta Trop. 2015;151:116-25. Available from: https://doi.org/10.1016/j.actatropica.2015.06.006
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. Many triatomines invade houses, but few can initiate the processes of colonization and domiciliation, which depend on the characteristics of the invasive species33. Barbu CM, Hong A, Manne JM, Small DS, Calderon JEQ, Sethuraman K, et al. The effects of city streets on an urban disease vector. PLoS Comput Biol. 2013;9(1):e1002801. Available from: https://doi.org/10.1371/journal.pcbi.1002801
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,44. Waleckx E, Gourbiere S, Dumonteil E. Intrusive versus domiciliated triatomines and the challenge of adapting vector-control practices against Chagas disease. Mem Inst Oswaldo Cruz. 2015;110(3):324-38. Available from: https://doi.org/10.1590/0074-02760140409
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, the invaded dwelling55. Tah ARV, Gomez LH, Beutelspacher AN, Canto JO, Ramsey JM. Human vulnerability to Trypanosoma cruzi vector transmission through health-disease processes and social appropriation of the territory. Salud Colect. 2015;11(2):191-210. Available from: http://dx.doi.org/10.1590/S1851-82652015000200004
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,66. Gurtler RE, Yadon ZE. Eco-bio-social research on community-based approaches for Chagas disease vector-control in Latin America. Trans R Soc Trop Med Hyg. 2015;109(2):91-8. Available from: https://dx.doi.org/10.1093%2Ftrstmh%2Ftru203
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, and the environment around the household77. Rossi JCN, Duarte EC, Gurgel-Gonçalves R. Factors associated with the occurrence of Triatoma sordida (Hemiptera: Reduviidae) in rural localities of Central-West Brazil. Mem Inst Oswaldo Cruz . 2015;110(2):192-200. Available from: https://doi.org/10.1590/0074-02760140395
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.

In Brazil, some triatomine species have succeeded in occupying the domestic environment and expanding their spatial distribution beyond their original biomes88. Forattini OP, Rabello EX, Pattoli DGB, Corrêa RR. Residual house infestations by Triatoma infestans. Rev Saude Publica. 1971;5(1):17-21. Available from: https://doi.org/10.1590/S0034-89101971000100002
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through active and passive dispersal99. Ribeiro-Jr G, Silva-Santos C, Noireau F, Dias-Lima A. Potencial de dispersão de algumas espécies de triatomíneos (Hemiptera: Reduviidae) por aves migratórias. Sitientibus Ser Ci Biol. 2006;6(4):324-8.,1010. Stevens L, Monroy MC, Rodas AG, Dorn PL. Hunting, swimming, and worshiping: human cultural practices illuminate the blood meal sources of cave-dwelling Chagas vectors (Triatoma dimidiata) in Guatemala and Belize. PLoS Negl Trop Dis 2014;8(9):e3047. Available from: https://dx.doi.org/10.1371%2Fjournal.pntd.0003047
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. One of these species is Triatoma infestans (Klug, 1835), which occupied household units among 12 states of Brazil and was considered the main vector involved in T. cruzi transmission in Brazil1111. Silveira AC. Entomological survey (1975-1983). Rev Soc Bras Med Trop. 2011;44(2):26-32. Available from: https://doi.org/10.1590/s0037-86822011000800005
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,1212. Silveira AC, Dias JC. The control of vectorial transmission. Rev Soc Bras Med Trop . 2011;44(2):52-63. Available from: https://doi.org/10.1590/S0037-86822011000800009
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. After the first standardized chemical-based control actions were implemented by the National Chagas Disease Control Program in 1975 and by the integrated initiatives of the Southern Cone of Latin America to eliminate T. infestans in 1991, a sustained decrease in domestic populations of vectors was observed1313. World Health Organization (WHO). Control of Chagas disease: report of a WHO expert committee. Expert Committee on the Control of Chagas Disease & World Health Organization. 1991;811. Available from: https://apps.who.int/iris/handle/10665/37686
https://apps.who.int/iris/handle/10665/3...

14. World Health Organization (WHO). Chagas disease, Brazil. Wkly Epidemiol Rec. 2000;75(17):153-5. Available from: https://apps.who.int/iris/handle/10665/231143
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-1515. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. General situation and perspectives of Chagas disease in Northeastern Region, Brazil. Cad Saude Publica. 2000;16(2):13-34. Available from: https://doi.org/10.1590/S0102-311X2000000800003
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. In 2006, Brazil received certification of interruption of Chagas disease transmission by T. infestans from the Pan American Health Organization (PAHO) and the World Health Organization (WHO)1616. Dias JC. Southern Cone Initiative for the elimination of domestic populations of Triatoma infestans and the interruption of transfusional Chagas disease. Historical aspects, present situation, and perspectives. Mem Inst Oswaldo Cruz . 2007;102(1):11-18. Available from: http://dx.doi.org/10.1590/S0074-02762007005000092
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. However, many regions of Brazil, such as the state of Bahia, still have several species of native vectors that can transmit T. cruzi to humans and domestic animals.

Pirajá da Silva initially described the existence of triatomines in the state of Bahia in 1911, shortly after T. cruzi was described by Carlos Chagas1717. Falcão EC. Pirajá da Silva: o incontestável descobridor do Schistosoma mansoni. vol. 1, 2edn ed. Brasília: Ministério da saúde; 2008. 199 p.. Pirajá da Silva identified Conorhinus megistus triatomines - syn. Panstrongylus megistus (Burmeister, 1835) - in the city of Mata de São João, near Salvador, the capital city of Bahia. Pirajá da Silva also identified triatomines among the cities of Feira de Santana, Candeias, São Francisco do Conde, and Salvador1818. Brumpt E, Pirajá da Silva MA. Existence du Schizotrypanum cruzi Chagas 1909, à Bahia. (Mata de São João): Biologie du Conorhinus megistus. Bull Soc Pathol Exot. 1912;5:22-6.. Almost 40 years after Pirajá's initial research description, Chagas disease was recognized as a serious health problem in the state of Bahia, where triatomines were captured simultaneously to the record of autochthonous cases of Chagas heart disease in Salvador1919. Pondé AA. A Doença de Chagas na Bahia (Chagas disease in Bahia). Arq Univ Bahia Fac Med. 1946;1:333-456.. P. megistus and Triatoma rubrofasciata (De Geer, 1773) naturally infected by T. cruzi were found at the historic center of Salvador city, associated with human cases, which motivated a chemical control campaign2020. Leal JM, Sherlock IA, Serafim EM. Observações Sobre o Combate aos Triatomíneos Domiciliários com BHC, em Salvador, Bahia. Revista Brasileira de Malariologia e Doencas Tropicais . 1965;17(1):65-73. Available from: https://www.arca.fiocruz.br/handle/icict/33038
https://www.arca.fiocruz.br/handle/icict...
. Nevertheless, some foci of P. megistus maintained T. cruzi transmission to families in the neighborhoods of Salvador2020. Leal JM, Sherlock IA, Serafim EM. Observações Sobre o Combate aos Triatomíneos Domiciliários com BHC, em Salvador, Bahia. Revista Brasileira de Malariologia e Doencas Tropicais . 1965;17(1):65-73. Available from: https://www.arca.fiocruz.br/handle/icict/33038
https://www.arca.fiocruz.br/handle/icict...
. In the early 1970s, more than 600 specimens of P. megistus and T. rubrofasciata were examined in Salvador, of which 16% were infected with T. cruzi2121. Sherlock IA, Serafim EM. Fauna Triatominae do Estado da Bahia, Brasil. VI - Prevalência Geográfica da Infecção dos Triatomíneos por T. cruzi. Rev Soc Bras Med Trop . 1974;8(3):129-141. Available from: https://doi.org/10.1590/S0037-86821974000300001
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. During this period, efforts were made to identify and better understand the ecology of triatomines in Bahia, and 18 triatomine species were cataloged2222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
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.

National campaigns focused on active vector surveillance for the identification of household infestation areas in Brazil and strategies of triatomine vector-control using chemical insecticides (BHC and pyrethroids). The 1983 Brazilian campaign was executed by the Superintendence of Public Health Campaigns (SUCAM) of Brazil’s Health Ministry. During this period, new triatomines were recorded, and new species were described2222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
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.

Recent epidemiological studies indicate that Bahia had a high prevalence of human T. cruzi infection (0.77% to 2.22%) compared to the Northeast region of Brazil (0.69% to 0.88%) between 1987 and 19941515. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. General situation and perspectives of Chagas disease in Northeastern Region, Brazil. Cad Saude Publica. 2000;16(2):13-34. Available from: https://doi.org/10.1590/S0102-311X2000000800003
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. Data between 2008 and 2017 indicate that Chagas disease mortality rates in the state of Bahia (3.8 to 4.8 deaths/100,000 habitants) are the highest among the northeastern states and the fourth highest among all Brazilian states. Moreover, two deaths were registered in children younger than one year old, indicating acute cases and risk of domestic T. cruzi transmission2727. Silveira A, Feitosa V, Borges R. Distribuição de triatomíneos no ambiente domiciliar, no período de 1975/84, Brasil. Rev Bras Malariol Doencas Trop. 1984;36:5-312..

Currently, 26 triatomine species have been recognized in Bahia2525. Galvão C. Vetores da doença de Chagas no Brasil. Curitiba, Paraná: Soc Bras Zoo. 2014. 289 p. Available from: http://books.scielo.org/id/mw58j
http://books.scielo.org/id/mw58j...
-2626. Santos CGS, Ribeiro-Jr G, Sousa OMF. Diagnose e distribuição das espécies dos triatomíneos da Bahia. In: Sousa OMF, Santos CGS, Santos RF, Fonseca EOL, Lima AGD, editors. Triatomíneos da Bahia: Manual de identificação e orientações para o serviço. Vol. 1: Salvador, Bahia: Editora Oxente; 2020. p. 208. Available from: http://www.saude.ba.gov.br/wp-content/uploads/2020/04/Livro-triatom%C3%ADneos-da-Bahia-E-BOOK.pdf
http://www.saude.ba.gov.br/wp-content/up...
. Several factors can modify the spatial distribution and abundance of synanthropic triatomines. To understand the changes in T. cruzi vector occurrence, the use of retrospective epidemiological and entomological data has become a relevant strategy. In this study, we describe the relative abundance and proportional spatial distribution of synanthropic triatomines at the municipal level before (1957 to 1971) and after (2006 to 2019) the vector-control program implementation in the state of Bahia, which is one of the states with the greatest diversity of triatomines and highest rates of epidemiological information related to Chagas disease in northeastern Brazil.

METHODS

The state of Bahia has 417 municipalities and is located in the southern region of northeastern Brazil, bordering eight other Brazilian states and the Atlantic Ocean in the east (Figure 1). Descriptive analyses of both the spatial and temporal distribution of the synanthropic triatomine species data from Bahia was performed during two periods: (A) from 1957 to 1971, and (B) from 2006 to 2019. Data regarding period A present information on the Chagas disease vector surveillance program of Bahia between 1957 and 19712222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
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, which represents the period before the standardized implementation of systematic vector surveillance programs in Brazil2727. Silveira A, Feitosa V, Borges R. Distribuição de triatomíneos no ambiente domiciliar, no período de 1975/84, Brasil. Rev Bras Malariol Doencas Trop. 1984;36:5-312..

FIGURE 1:
Study area. Biomes of Brazil and geolocation of Bahia (a). Municipalities of Bahia (b); the inset shows the city of Salvador (in detail).

Information regarding period B was obtained from the following state government databases after the certification of interruption of Chagas disease transmission by T. infestans: Epidemiologic Surveillance team of the State of Bahia’s Health Service (SESAB), Epidemiological Surveillance Office (DIVEP), and Central Public Health Laboratory of Bahia (LACEN/BA) 2929. Abad-Franch F, Diotaiuti L, Gurgel-Goncalves R, Gurtler RE. Certifying the interruption of Chagas disease transmission by native vectors: cui bono? Mem Inst Oswaldo Cruz . 2013;108(2):251-4. Available from: https://doi.org/10.1590/0074-0276108022013022
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.

Entomological data were obtained in three different ways: (a) notification of triatomines (surveillance and community participation) performed by the population itself by taking suspicious insects to health agents; (b) notification attendance (active surveillance) performed by the health agents of each municipality, dependent on (a); and (c) active search (active surveillance), in which vectors were searched among household units around the area, regardless of any notification performed by the population.

To compare T. cruzi vector species information from both periods of the study, we evaluated: (1) the relative abundance, calculated as the proportion of each triatomine species divided by the total number of triatomines for each period; and (2) proportional spatial distribution, calculated as the proportion of municipalities that recorded a triatomine species divided by the number of sampled municipalities.

Spreadsheets were used to collect the following data: species, municipality, date, geographic information system (GIS) coordinates, sampling environment (intradomestic, peridomestic), and data reference. Graphs and descriptive statistics were computed using SPSS 24. In the absence of specific GIS information, the coordinates of the city's headquarters from the Brazilian Institute of Geography and Statistics (IBGE) were used3030. Censo 2010. Ministério da Economia (ME), Instituto Brasileiro de Geografia Estatística - IBGE [Internet]. 2012 [updated 2010 Jan 22; cited 2020 Nov 28] Available from: Available from: http://www.censo2010.ibge.gov.br
http://www.censo2010.ibge.gov.br...
. Data processing was performed using the ArcGis® Software 10.53131. Shaner J, Wrightsell J. Editing in ArcMap: Esri. 2000. 229 p..

RESULTS

In this study, information regarding 315 municipalities and 215597 triatomines collected during the two periods was evaluated, among which 35588 were from period A (1957-1971) and 180020 were from period B (2006-2019). During period A, data were gathered from 202/290 (71%) municipalities2222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
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, and in period B, 258/417 (61.8%) municipalities were evaluated. Regarding the number of triatomine species, 18 and 21 species were sampled during periods A and B, respectively, and 16 of them were sampled during both periods (Table 1).

TABLE 1:
Synanthropic triatomine species from the state of Bahia, Brazil, recorded between 1957-1971 and between 2006-2019.

Figure 2 shows the spatial distribution of triatomines in the municipalities during periods A and B. During period A, P. megistus was present in 122 (60.4%) of the sampled municipalities, followed by T. sordida (37.1%), T. pseudomaculata (19.8%), and T. infestans (12.8%). During period B, T. pseudomaculata was widely distributed, being recorded in 176 of 258 (68.2%) sampled municipalities, followed by T. sordida (61.6%), and T. brasiliensis (36.4%) (Figure 3).

FIGURE 2:
Municipalities with the occurrence of triatomines and species richness in the state of Bahia during periods A (1957-1971), in blue, and B (2006-2019), in red, and the spatial distribution of the synanthropic triatomines. Legend: Color gradients represent the species richness at each period of the study. “X” axis shows the name of the triatomine species evaluated, while “Y” axis shows the proportional (%) spatial distribution of them.

In period A, P. megistus was the most abundant species (n=22032), representing 61.9% of triatomines, followed by T. sordida (23.3%), T. brasiliensis species complex (4.3%), and T. infestans (3.6%). Conversely, in period B, T. sordida represented 81.6% of all collected triatomines, followed by T. pseudomaculata (9.2%) and T. brasiliensis species complex (6.3%).

By analyzing the spatial distribution of the main triatomine species before and after T. cruzi vector-control actions, we observed a reduction in the municipal occurrence of synanthropic populations of T. infestans and P. megistus. T. infestans was no longer detected in some municipalities in the west (e.g., Santa Maria Vitória, Barreiras) and north (e.g., Juazeiro, Curaçá) of Bahia (Figure 3) and had been first detected among other municipalities in the Caatinga (e.g., Itaguaçu da Bahia, Novo Horizonte) and Atlantic Forest biomes (e.g., Tremedal and Presidente Tancredo Neves). During period B, T. infestans was found only at residual foci and was last recorded in 2015 in the municipality of Novo Horizonte (Figure 3).

FIGURE 3:
Geographic distribution of Panstrongylus megistus, Triatoma infestans, T. pseudomaculata, T. sordida, *T. brasiliensis species complex in the municipalities of the state of Bahia during periods A (1957-1971), in blue, and B (2006-2019), in crosshatch.

During period B, we observed a higher occurrence of T. sordida in western Bahia, where the Cerrado biome predominates, in south-central Bahia, and in some municipalities of Recôncavo Baiano, eastern Bahia. However, we observed a remarkable change in the spatial distribution of T. pseudomaculata, which expanded its area of occurrence among western municipalities (Cerrado biome) and the central region (Caatinga biome) of Bahia (Figure 3).

A comparison of the total number of individuals (n) and the relative abundance (%) of species in periods A and B showed a reduction for P. megistus (A: n=22032, 61.9%; B: n=1804, 1.0%) and T. infestans (A: n=1310, 3.6%; B: n=763, 0.4%), as well as an increase in the relative abundance of T. sordida (A: n=8314, 23.3%, B: n=146901, 81.6%) and T. pseudomaculata (A: n=894, 2.5%, B: n=16717, 9.2%). During period B, most triatomines were captured in peridomestic habitats, with a predominance of T. sordida (Table 2).

TABLE 2:
Synanthropic triatomines collected in the state of Bahia, Brazil, by species and collection environment between 2006 and 2019.

DISCUSSION

This study indicated changes in the spatial distribution and relative abundance of synanthropic triatomines in the state of Bahia, Northeast Brazil, before and after 44 years of structured control actions of T. cruzi vectors, initiated in 1975. Our results indicate a clear reduction in the occurrence of P. megistus and T. infestans (last record in 2015) and an increase in the relative abundance and geographical distribution of T. sordida and T. pseudomaculata after the Brazilian vector-control program.

Panstrongylus megistus was the predominant species between 1957 and 1971; it was found in 60% of municipalities, with a relative abundance of 62% of collected triatomines2222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
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. Its proportional spatial distribution has been greatly reduced in the state of Bahia, especially in the areas of Recôncavo Baiano and the metropolitan region of Salvador. P. megistus spatial distribution has also been reduced in other Brazilian states1111. Silveira AC. Entomological survey (1975-1983). Rev Soc Bras Med Trop. 2011;44(2):26-32. Available from: https://doi.org/10.1590/s0037-86822011000800005
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,3636. Oliveira AWW, Silva IG. Geographical distribution and indicators entomologic of synanthropic triatomines captured in the State of Goiás. Rev Soc Bras Med Trop . 2007;40(2):204-8. Available from: https://doi.org/10.1590/s0037-86822007000200011
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37. Almeida PS, Ceretti-Junior W, Obara MT, Santos HR, Barata JM, Faccenda O. Survey of Triatominae (Hemiptera: Reduviidae) fauna in domestic environments and natural infection by Trypanosomatidae in the State of Mato Grosso do Sul. Rev Soc Bras Med Trop . 2008;41(4):374-80. Available from: https://doi.org/10.1590/s0037-86822008000400010
-3838. Passos AD, Silveira AC. Summary of results from the national surveys. Rev Soc Bras Med Trop . 2011;44(2):47-50. Available from: https://doi.org/10.1590/s0037-86822011000800008
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. Three hypotheses could explain this reduction in the metropolitan region of Salvador: (a) chemical control was successfully performed over four decades, resulting in the elimination of domestic populations of P. megistus; (b) intense urbanization in these municipalities resulted in deforestation and fragmentation of the Atlantic Forest biome areas, which is the natural habitat of this species2222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
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; and (c) housing improvement, with progressive depletion of adobe houses3939. Rodrigues TA, Salvador E. As implicações do Programa de Aceleração do Crescimento (PAC) nas políticas sociais. Ser Social. 2011;13(28):129-56. Available from: https://doi.org/10.26512/ser_social.v13i28.12685
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,4040. Pereira AS. Uma avaliação do Programa de Aceleração do Crescimento (PAC) no estado da Bahia (2007-10). Rev Adm Publ. 2013;47(1):177-203. Available from: https://doi.org/10.1590/S0034-76122013000100008
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, a favorable environment for P. megistus colonization. P. megistus is a native Brazilian species with a wide spatial distribution and high epidemiological and entomological relevance due to the high rates of T. cruzi infection and its proximity to human dwellings, as it can colonize intra-and/or peridomicile areas. In 2021, P. megistus foci were described in the metropolitan region of São Paulo, with T. cruzi-infected triatomines associated with marsupials, revealing the importance of continued surveillance of synanthropic P. megistus4646. Silva RA, Virgínio F, Estevão VAO, Martins ML, Duarte AN, Silva GP, et al. First report of colonization by Panstrongylus megistus (Burmeister, 1835) (Hemiptera, Reduviidae, Triatominae) in the Metropolitan Region of São Paulo, Brazil. Braz J Biol. 2021;81(1):178-82. Available from: https://doi.org/10.1590/1519-6984.225562
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.

During period A, T. infestans were found in 12.8% of the sampled municipalities and represented 3.7% of the sampled triatomines. During period B, T. infestans was identified in only seven municipalities with residual colonies3434. Araujo RF, Mendonca JV, Rosa JA, Matos JF, Lima SC, Figueiredo MAA. Description of a newly discovered Triatoma infestans (Hemiptera: Reduviidae) Foci in Ibipeba, State of Bahia, Brazil. Rev Soc Bras Med Trop . 2014;47(4):513-6. Available from: https://doi.org/10.1590/0037-8682-0219-2013
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-3535. Brandão H, Fonseca E, Santos R, Ribeiro-Jr G, Santos C, Cova B, et al. Descrição de focos residuais de Triatoma infestans (klug, 1834) no município de Novo Horizonte, Bahia. Rev Baiana Saude Publica. 2015;39(1):91-104. Available from: http://dx.doi.org/10.5327/Z0100-0233-201539S100009
https://doi.org/http://dx.doi.org/10.532...
. Bahia was the last Brazilian state to receive PAHO certification, possibly because of specific T. infestans identification errors and the appearance of new records of this species in the study area3232. Malafaia G, Rodrigues A. Centenário do descobrimento da doença de Chagas: desafios e perspectivas. Rev Soc Bras Med Trop . 2010;43(5):483-5. Available from: http://dx.doi.org/10.1590/S0037-86822010000500001
https://doi.org/http://dx.doi.org/10.159...
. The elimination of T. infestans in several municipalities in western and central Bahia can be explained by the T. infestans elimination plan. This plan was intensified in 2004 and included spraying households with insecticides, followed by research and capture of triatomines, surveying approximately 500000 households2626. Santos CGS, Ribeiro-Jr G, Sousa OMF. Diagnose e distribuição das espécies dos triatomíneos da Bahia. In: Sousa OMF, Santos CGS, Santos RF, Fonseca EOL, Lima AGD, editors. Triatomíneos da Bahia: Manual de identificação e orientações para o serviço. Vol. 1: Salvador, Bahia: Editora Oxente; 2020. p. 208. Available from: http://www.saude.ba.gov.br/wp-content/uploads/2020/04/Livro-triatom%C3%ADneos-da-Bahia-E-BOOK.pdf
http://www.saude.ba.gov.br/wp-content/up...
. However, residual colonies of this species have been detected in a few municipalities2828. Dias JC. Chagas disease: successes and challenges. Cad Saude Publica . 2006;22(10):2020-1. Available from: https://doi.org/10.1590/s0102-311x2006001000001
https://doi.org/https://doi.org/10.1590/...
,2929. Abad-Franch F, Diotaiuti L, Gurgel-Goncalves R, Gurtler RE. Certifying the interruption of Chagas disease transmission by native vectors: cui bono? Mem Inst Oswaldo Cruz . 2013;108(2):251-4. Available from: https://doi.org/10.1590/0074-0276108022013022
https://doi.org/https://doi.org/10.1590/...
, requiring constant monitoring to eliminate residual foci from the state of Bahia. In addition to the chemical control performed in Bahia since 1975, intensified in 1991, which aimed to eliminate T. infestans1111. Silveira AC. Entomological survey (1975-1983). Rev Soc Bras Med Trop. 2011;44(2):26-32. Available from: https://doi.org/10.1590/s0037-86822011000800005
https://doi.org/https://doi.org/10.1590/...
,1515. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. General situation and perspectives of Chagas disease in Northeastern Region, Brazil. Cad Saude Publica. 2000;16(2):13-34. Available from: https://doi.org/10.1590/S0102-311X2000000800003
https://doi.org/https://doi.org/10.1590/...
, other social actions were implemented by the federal government. These included the growth acceleration program, intended to improve housing quality, with the replacement of mud houses with brick houses and health education actions on Chagas disease. This may also have influenced the reduction in household colonization by T. infestans and other household species3939. Rodrigues TA, Salvador E. As implicações do Programa de Aceleração do Crescimento (PAC) nas políticas sociais. Ser Social. 2011;13(28):129-56. Available from: https://doi.org/10.26512/ser_social.v13i28.12685
https://doi.org/https://doi.org/10.26512...
,4040. Pereira AS. Uma avaliação do Programa de Aceleração do Crescimento (PAC) no estado da Bahia (2007-10). Rev Adm Publ. 2013;47(1):177-203. Available from: https://doi.org/10.1590/S0034-76122013000100008
https://doi.org/https://doi.org/10.1590/...
.

Although successful in controlling T. infestans, several native species have been recorded in a large number of municipalities. They were captured in households and frequently colonized peri domestic areas. Among them, some were infected by T. cruzi and many of them fed on domestic animals and human blood4242. Carbajal de la Fuente AL, Porcasi X, Noireau F, Diotaiuti L, Gorla DE. The association between the geographic distribution of Triatoma pseudomaculata and Triatoma wygodzinskyi (Hemiptera: Reduviidae) with environmental variables recorded by remote sensors. Infect Genet Evol. 2009;9(1):54-61. Available from: https://doi.org/10.1016/j.meegid.2008.09.008
https://doi.org/https://doi.org/10.1016/...
. In period A, T. sordida was recorded in 37% of the municipalities, representing 23% of the collected triatomines, while T. pseudomaculata was recorded in 19% of the municipalities, with a relative abundance of 2.5% of the gathered triatomines2323. Dias JCP. Control of Chagas disease in Brazil. Parasitol today. 1987;3(11):336-41. Available from: https://doi.org/10.1016/0169-4758(87)90117-7
https://doi.org/https://doi.org/10.1016/...
. In period B, T. sordida was recorded in 60% of the municipalities, representing approximately 81% of the triatomines. T. sordida is the most common species in different regions of Bahia. Similarly, T. pseudomaculata was identified in the largest number of municipalities during period B (67.4%). Systematic vector-control actions had a low impact on the spatial distribution of T. sordida and T. pseudomaculata in Bahia. There was a higher occurrence of T. sordida in western and south-central Bahia, where there are areas of Cerrado, which is the original biome of the species’ natural populations11. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas' disease. Bull Am Mus Nat Hist. 1979;163(3):123-520.,22. Galvao C, Justi SA. An overview of the ecology of Triatominae (Hemiptera: Reduviidae). Acta Trop. 2015;151:116-25. Available from: https://doi.org/10.1016/j.actatropica.2015.06.006
https://doi.org/https://doi.org/10.1016/...
,2525. Galvão C. Vetores da doença de Chagas no Brasil. Curitiba, Paraná: Soc Bras Zoo. 2014. 289 p. Available from: http://books.scielo.org/id/mw58j
http://books.scielo.org/id/mw58j...
. The highest occurrence of T. pseudomaculata in western and central Bahia followed the occurrence predictions of the species based on environmental variables4242. Carbajal de la Fuente AL, Porcasi X, Noireau F, Diotaiuti L, Gorla DE. The association between the geographic distribution of Triatoma pseudomaculata and Triatoma wygodzinskyi (Hemiptera: Reduviidae) with environmental variables recorded by remote sensors. Infect Genet Evol. 2009;9(1):54-61. Available from: https://doi.org/10.1016/j.meegid.2008.09.008
https://doi.org/https://doi.org/10.1016/...
. The number of specimens of T. sordida and T. pseudomaculata exceeded 90% of all triatomines collected in the state between 2006 and 2019.

We observed a higher occurrence of T. brasiliensis and similar species in Bahia, thus expanding the observations of Ribeiro-Jr et. al.4141. Ribeiro-Jr G, Santos CGS, Lanza F, Reis J, Vaccarezza F, Diniz C, et al. Wide distribution of Trypanosoma cruzi infected triatomines in the State of Bahia, Brazil. Parasit Vectors. 2019;12(1):604. Available from the following: https://doi.org/10.1186/s13071-019-3849-1
https://doi.org/https://doi.org/10.1186/...
. Before systematized control actions, the T. brasiliensis species complex was registered in 10% of the municipalities of Bahia, and between 2006 and 2019, at least 94 municipalities (36%) registered this species. In the last few years, other species of the T. brasiliensis complex have been described in the state of Bahia, including T. juazeirensis, T. melanica, T. sherlocki, and T. petrocchiae4343. Dale C, Almeida CE, Mendonça VJ, Oliveira J, Osa JA, Galvão C, et al. An updated and illustrated dichotomous key for the Chagas disease vectors of Triatoma brasiliensis species complex and their epidemiologic importance. Zookeys. 2018;805:33-43. Available from: https://doi.org/10.3897/zookeys.805.25559
https://doi.org/https://doi.org/10.3897/...
. Among these species, T. juazeirensis is noteworthy because it was predominantly collected inside household units. Other species, such as T. tibiamaculata, P. geniculatus, T. melanocephala, and P. lutzi, were intrusively detected inside the houses, mainly adult specimens.

There was a significant difference in the occurrence of T. tibiamaculata between the two periods. In period A, it was recorded in approximately 1% of the municipalities with a relative abundance of 0.01%2323. Dias JCP. Control of Chagas disease in Brazil. Parasitol today. 1987;3(11):336-41. Available from: https://doi.org/10.1016/0169-4758(87)90117-7
https://doi.org/https://doi.org/10.1016/...
. In period B, it was recorded in 7% of the municipalities with a relative abundance of 0.55%. In recent decades, even though T. tibiamaculata has been naturally found inside nests of marsupials, rodents, and epiphytes in forests11. Lent H, Wygodzinsky P. Revision of the Triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas' disease. Bull Am Mus Nat Hist. 1979;163(3):123-520.,2222. Sherlock IA, Serafim EM. Fauna Triatominae no Estado da Bahia, Brasil: as espécies e distribuição geográfica. Rev Soc Bras Med Trop . 1972;6(5):265-76. Available from: https://doi.org/10.1590/S0037-86821972000500005
https://doi.org/https://doi.org/10.1590/...
, it has been recorded in peri domestic palms and inside households. Therefore, T. cruzi-infected T. tibiamaculata generates a transmission risk in Salvador, probably in the entire metropolitan region, and in the Atlantic Forest areas4444. Ribeiro-Jr G, Gurgel-Goncalves R, Reis RB, Santos CG, Amorim A, Andrade SG, et al. Frequent house invasion of Trypanosoma cruzi infected triatomines in a suburban area of Brazil. PLoS Negl Trop Dis . 2015;9(4):e0003678. Available from: https://doi.org/10.1371/journal.pntd.0003678
https://doi.org/https://doi.org/10.1371/...
.

Triatomine vectors of T. cruzi can be classified as native/non native, wild/non wild, domestic/peridomestic to enable the definition of effective vector-control strategies4545. Ribeiro-Jr G, Abad-Franch F, Sousa OMF, Santos CGS, Fonseca EOL, Santos RF, et al. TriatoScore: an entomological-risk score for Chagas disease vector control-surveillance. Parasit Vectors . 2021;14:492. Available from: https://doi.org/10.1186/s13071-021-04954-5
https://doi.org/10.1186/s13071-021-04954...
. While domestic and peridomestic populations of species of triatomines are subject to spraying of chemical pesticides, which is the main strategy of vector control, native-wild species can persistently invade or colonize the household (peri-and intradomicile). Thus, this may represent a challenge for controlling T. cruzi transmission in the domestic environment.

This study has several limitations. Since the use of reference databases does not allow a broad analysis of data, it was impossible to obtain data on triatomines within habitats (intra-and peridomicile) in period A (1957-1971). The effects of passive dispersion and seasonal changes on vector behavior were impossible to measure. In addition, the database does not allow descriptive evaluations of nymph occurrence. Moreover, not all municipalities collected data regularly during the evaluated periods, and the health surveillance service classifies municipalities among the high, medium, and low risk of transmission, emphasizing that there is no obligation to conduct regular entomological research among low-risk municipalities based on the classification presented by Brazil’s Health Ministry2626. Santos CGS, Ribeiro-Jr G, Sousa OMF. Diagnose e distribuição das espécies dos triatomíneos da Bahia. In: Sousa OMF, Santos CGS, Santos RF, Fonseca EOL, Lima AGD, editors. Triatomíneos da Bahia: Manual de identificação e orientações para o serviço. Vol. 1: Salvador, Bahia: Editora Oxente; 2020. p. 208. Available from: http://www.saude.ba.gov.br/wp-content/uploads/2020/04/Livro-triatom%C3%ADneos-da-Bahia-E-BOOK.pdf
http://www.saude.ba.gov.br/wp-content/up...
. Future studies reassessing risk classification at the municipal level are urgently needed for the redefinition of areas and risk of transmission. Further studies should analyze the situation of these areas to explain whether the absence of triatomines is due to the functioning of the service or biogeographic issues related to triatomines. In periods A and B, T. brasiliensis complex species were considered as one, and to avoid misinterpretations, data obtained in this study were evaluated at stricto sensu level4444. Ribeiro-Jr G, Gurgel-Goncalves R, Reis RB, Santos CG, Amorim A, Andrade SG, et al. Frequent house invasion of Trypanosoma cruzi infected triatomines in a suburban area of Brazil. PLoS Negl Trop Dis . 2015;9(4):e0003678. Available from: https://doi.org/10.1371/journal.pntd.0003678
https://doi.org/https://doi.org/10.1371/...
. In Bahia, nine species that are unlikely to be found within households2424. Vinhaes MC, Oliveira SV, Reis PO, Sousa ACL, Silva RA, Obara MT, et al. Assessing the vulnerability of Brazilian municipalities to the vectorial transmission of Trypanosoma cruzi using multi-criteria decision analysis. Acta Trop. 2014;137:105-10. Available from: https://doi.org/10.1016/j.actatropica.2014.05.007
https://doi.org/https://doi.org/10.1016/...
,2525. Galvão C. Vetores da doença de Chagas no Brasil. Curitiba, Paraná: Soc Bras Zoo. 2014. 289 p. Available from: http://books.scielo.org/id/mw58j
http://books.scielo.org/id/mw58j...
,3333. Gurgel-Gonçalves R, Galvão C, Mendonça J, Neto E. Guia de triatomíneos da Bahia. Feira de Santana, Bahia: UEFS Editora. 2012. 112 p. Available from: http://dx.doi.org/10.13140/2.1.1347.2000
https://doi.org/http://dx.doi.org/10.131...
were recorded by the surveillance services. These included Belminus laportei, Eratyrus mucronatus, Microtriatoma trinidadensis, Panstrongylus tupynambai, P. lignarius, Rhodnius prolixus, Triatoma maculata, T. circummaculata, and T. rubrovaria. To reduce taxonomic identification errors, a guide was developed3333. Gurgel-Gonçalves R, Galvão C, Mendonça J, Neto E. Guia de triatomíneos da Bahia. Feira de Santana, Bahia: UEFS Editora. 2012. 112 p. Available from: http://dx.doi.org/10.13140/2.1.1347.2000
https://doi.org/http://dx.doi.org/10.131...
and, more recently, a guidance manual for the surveillance of triatomines in Bahia, with identification keys, diagnosis, and distribution of vector species2626. Santos CGS, Ribeiro-Jr G, Sousa OMF. Diagnose e distribuição das espécies dos triatomíneos da Bahia. In: Sousa OMF, Santos CGS, Santos RF, Fonseca EOL, Lima AGD, editors. Triatomíneos da Bahia: Manual de identificação e orientações para o serviço. Vol. 1: Salvador, Bahia: Editora Oxente; 2020. p. 208. Available from: http://www.saude.ba.gov.br/wp-content/uploads/2020/04/Livro-triatom%C3%ADneos-da-Bahia-E-BOOK.pdf
http://www.saude.ba.gov.br/wp-content/up...
.

This study describes changes in the triatomine fauna of Bahia between the analyzed periods more than 40 years after the implementation of the vector-control program in the state. During this period, we observed changes in the Chagas disease surveillance policies in Brazil due to decentralization. The centralized Brazilian control program was transferred to municipalities without corresponding training. The decentralization policy of the Chagas disease vector-control program aimed to bring the actions of the government closer to the communities, but true engagement by local communities has not been achieved. After decentralization, the efficacy of some municipalities in detecting triatomines has been reduced. We observed a reduction in the relative abundance and proportional spatial distribution of domestic and domesticated species of T. cruzi vectors P. megistus and T. infestans, respectively. In addition, we described an increase in the native species T. sordida, T. pseudomaculata, and T. brasiliensis species subcomplex and highlighted the important role of native triatomine species in T. cruzi transmission in the domiciliary environment. The observed changes in T. cruzi main vectors between the evaluated periods demonstrate the importance of reinforcing entomological surveillance actions. Furthermore, promoting and disseminating community-based scientific knowledge and health education actions on Chagas disease at a local scale will help mitigate surveillance challenges and control native triatomines.

Ethics

The procedures followed the ethical standards of the Research Ethics Committee of the Gonçalo Moniz Institute (IGM - FIOCRUZ, Bahia, Brazil). The consent form was waived since the analysis was performed using a database. However, to provide full anonymity to participants, no personal identification data were used. The research did not cause any physical, psychological, moral, intellectual, social, cultural, or religious risks to the residents or animals in the study areas. In addition, this study did not include endangered or protected species.

ACKNOWLEDGMENTS

We are grateful to the Epidemiologic Surveillance team of Bahia’s State Health Service (SESAB-DIVEP) for the databases and all support with the triatomines and vectors information. We are also grateful to Rafaella Albuquerque Silva and César Augusto Cuba Cuba for their suggestions and comments. Also, we would like to thank Natalie Jennifer Hurrell for the help with the English language proofreading.

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  • Financial Support: Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB).

Publication Dates

  • Publication in this collection
    25 July 2022
  • Date of issue
    2022

History

  • Received
    04 Jan 2022
  • Accepted
    20 Apr 2022
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