Entomological triatomine indicators in the State of Rio Grande do Norte, Brazil

Márcio Adriano Fernandes Barreto Marília Abrantes Fernandes Cavalcanti Cléber de Mesquita Andrade Ellany Gurgel Cosme do Nascimento Wogelsanger Oliveira Pereira About the authors

Abstract

This study aimed to describe the main entomological triatomine-related indicators in the western mesoregion of Rio Grande do Norte. This is a descriptive cross-sectional retrospective study developed on a historical analysis of information on the triatomine capture carried out by the Chagas Disease Control Program, from 2008 to 2013. Five species were captured, of which the Triatoma brasiliensis and Triatoma pseudomaculata, by occupying the domestic and peridomestic environment, sequentially, and Panstrongylus lutzi by the highest rate of natural infection. A prevalence of nymphs among the captured specimens, a higher triatominal density in the peridomicile, infestation, colonization and natural infection rates of 5.6%, 49.6% and 0.8%, respectively, a significant difference in the distribution of specimens between the municipalities investigated and lack of declining infestation and colonization rates between 2009 and 2012 was observed. Findings suggest the need for continuous surveillance, facilitated by the association between field teams and communities, with emphasis on the proposal of health education for the recognition and notification of triatomines by the population.

Chagas disease; Entomology; Vector control

Introduction

Chagas disease still represents an important public health problem, given the current prevalence of Trypanosoma cruzi infection of approximately 5.7 million individuals in Latin America, with the highest number of infected in Argentina, Mexico and Brazil. In the latter, specifically, it is estimated that 1.2 million people are affected by the disease11. World Health Organization (WHO). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly epidemiological record. 2015; 90(6):33-44..

Vector transmission, which occurs through the penetration of parasites into the bloodstream through the gateway created in the skin by the bite of the hematophagous insect, still is the most important route of human infection by T. cruzi11. World Health Organization (WHO). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly epidemiological record. 2015; 90(6):33-44., and is facilitated by the great variety of triatomines in Brazil, which houses sixty-two species, of which thirty are in the domestic environment and ten are epidemiologically important22. Gurgel-Gonçalves RC, Galvão C, Costa J, Peterson AT. Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med 2012; 2012:705326..

In relation to the Brazilian Northeast, the same stands out for the dispersion rates, domestic infestation, colonization and natural infection, anthropophilia and number of captures of species Triatoma brasiliensis, Triatoma pseudomaculata and Panstrongylus megistus. In addition, species Triatoma brasiliensis and Triatoma pseudomaculata are found in all northeastern states and are a concern due to their great dispersion and difficult control33. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34..

In the state of Rio Grande do Norte, the first scientific description of T. cruzi infection was carried out in a seroprevalence study, which showed a positivity of 15.5% of the population44. Lucena DT, Lima ET. Epidemiologia da doença de Chagas no Rio Grande do Norte, III - A infecção humana determinada pela reação de Guerreiro Machado. Revista Brasileira de Malariologia e Doenças Tropicais 1962; 15:361-366. and, in spite of vector control programs adopted since that time, the presence of nine species of triatomines are recorded, among which are Triatoma brasiliensis, Triatoma pseudomaculata, Panstrongylus megistus, Panstrongylus lutzi, Panstrongylus diasi, Rhodnius nasutus, Triatoma melanocephala, Triatoma petrochiae and Triatoma rubrofasciata33. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34.. Recent data have shown the estimated T. cruzi seroprevalence at 6.5% in the rural population of the Western Potiguar mesoregion, without, however, describing natural triatomine infection, infestation and domestic colonization rates55. Brito CRN, Sampaio GHF, Câmara ACJ, Nunes DF, Azevedo PR, Chiari E, Galvão LMC. Seroepidemiology of Trypanosoma cruzi infection in the semiarid rural zone of the State of Rio Grande do Norte, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(3):346-352..

This study aimed to describe the species captured in the peridomestic and intradomestic environment, the occurrence of infestation and domestic colonization, and the natural infection rates of the different triatomine species to understand the challenges in controlling vector transmission control in an endemic rural area for Chagas’ disease.

Methodology

Study design

This is a descriptive, cross-sectional and retrospective study developed through an analysis of the historical series of information on triatomine capture provided by the Chagas Disease Control Program (PCDCh), corresponding to the period 2008-2013.

Study location

Rio Grande do Norte is located in the northeastern region of Brazil, bordering to the north and east with the Atlantic Ocean, to the south with Paraíba and to the west with Ceará (Figure 1) and has a population of 3,168,027 inhabitants66. Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados. Rio de Janeiro: IBGE; 2010.. It has one of the lowest HDIs in the Brazilian Northeast, with a large ruralized area and high index of low quality human dwellings, which are characterized as favorable for the triatomine shelter.

Figure 1
Map of Brazil demarcating the State of Rio Grande do Norte, the Western Mesoregion and the municipalities evaluated.

The area of this study is located to the west of the state and has 448,904 inhabitants, characterizing it as the second most populous region66. Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados. Rio de Janeiro: IBGE; 2010.. It has a predominance of semiarid climate, low rainfall index and the Caatinga as main vegetation. Despite housing programs, it still has houses of mud and masonry without plaster, besides peridomestic environment with the presence of animal breeding, heaps of straw, bricks, tiles and wood, conditions conducive to the emergence of the vector.For the study, we considered nine municipalities in the region with epidemiological relevance to Chagas disease, which include Apodi, Campo Grande, Caraúbas, Felipe Guerra, Governor Dix-Sept Rosado, Janduís, Messias Targino, Mossoró and Upanema (Figure 1).

Entomological indicators

The following entomological indicators were considered for analysis: number of triatomines captured (males, females, nymphs and infected), number of triatomines found in the domestic and peridomestic environment, intradomestic triatominal density (number of triatomines captured in intradomestic environment/number of intradomestic environments investigated); peridomestic triatominal density (number of triatomines captured in peridomestic environment/number of peridomestic environments investigated); colonization index (number of households with nymphs/total number of households with triatomines x 100), infestation index (number of infested households/number of households investigated x 100) and natural infection index (number of infected triatomines/number of triatomines examined x 100).

Triatomines captured

The capture of triatomines in the peridomestic and intradomestic environment occurred actively (manual capture) and was carried out by endemic agents of the municipalities in household visits programmed or directly by residents of the homes studied.

In the intradomestic environment, all household dependencies were verified, besides any possibilities of shelter for triatomines, such as cracks, holes, crevices in the floor, internal and external walls, furniture and objects. In the peridomestic environment, the search was performed in animal husbandry annexes (poultry, sheep, goats, pigs, cattle and horses), wooden piles, bricks, tiles, straws and warehouses or storehouses.

Metal tongs of different sizes and lanterns were used for the inspection of cracks and places lacking luminosity that could serve as shelter for triatomines, without any use of traps. All the captured triatomines were placed in polyethylene bottles with shredded or folded paper and sealed with a perforated lid for better preservation. Vials were duly labeled, identified and recorded on the Chagas Disease Control Program form.

Taxonomy

The records of triatomine species cases in the investigated municipalities were provided by the Regional Chagas Disease Control Coordination of the Second Regional Health Administration of Rio Grande do Norte.

Entomological indices: natural infection, home infestation and colonization

The study on natural triatomine infection by T. cruzi was carried out in the Laboratory of the II Regional Health Administration located in the municipality of Mossoró (RN).

The direct parasitological technique was adopted by abdominal compression of the insect to collect the fecal material in saline solution (NaCl 0.9%), which was deposited on a slide and examined in an optical microscope with a magnification of 400x. In the positive cases, slides were stained by the Giemsa technique and sent for confirmation at the Central Laboratory in Natal (RN). The natural infection index was obtained from the ratio between the number of infected triatomines and the number of triatomines examined.

Data review

Descriptive statistics were used to obtain the relative and absolute frequencies of triatomine data. The Kruskal Wallis test was used to verify the association between the distribution of the number of captured triatomines and the study sites. The ANOVA and Tukey tests (multiple comparisons) were used to identify significant differences in entomological indexes between study sites. The Student’s t test was selected to observe the difference of means between the intradomestic infestation index and the peridomestic infestation index in the study period. The simple linear regression test was performed to verify correlation between the entomological indices and the years of the study.

The analyses were performed through the Statistical Package for the Social Sciences (SPSS), version 20 (Chicago, IL, USA) and a significance level of 5% was established.

Results

According to a report provided by the Chagas Disease Control Program, 5,370 triatomines were captured, of which 50.6% (2,662/5,370) were in the form of nymphs and 75.5% (4,053/5,370) occupied the peridomestic environment (Table 1), so that statistical significance was detected between the intradomestic and peridomestic densities, with the latter being highlighted.

Table 1
Trypanosoma cruzi captured and positive synanthropic triatomines corresponding to the Western Mesoregion (RN), Brazil, from 2008 to 2013.

The general household triatominal density was 0.11. A statistical difference (p < 0.05) was observed between the number of triatomines captured and the locations included in the study, with a higher number of specimens in the rural area of Apodi.

The species captured were Triatoma brasiliensis, representing 56.9% (3,053/5,370), Triatoma pseudomaculata, with a percentage of 41.8% (2,247/ 5,370), Panstrongylus lutzi, corresponding to 0.7% (35/5,370), Rhodnius nasutus, with 0.5% of the total (25/5,370) and Panstrongylus megistus, indicated by 0.2% (10/5,370) (Table 1).

The species with the highest triatominal densities corresponded to T. brasiliensis and T. pseudomaculata (Table 2).

Table 2
Values of intra- and peridomestic triatominal densities and rate of natural infection by captured species, related to the municipalities of the Western Mesoregion (Brazil), from 2008 to 2013.

The overall natural infection rate among triatomines was 0.8%. Among the infected species found in intradomestic environment, T. brasiliensis and T. pseudomaculata, with 9 and 7 contaminated specimens, respectively, were highlighted (Table 1). While P. lutzi represented a lower triatomine concentration, it was responsible for the higher rate of natural infection among the captured triatomines (Table 2).

Of the 47,095 households investigated, 5.6% (2,630/47,095) evidenced triatomines, reflecting the overall household infestation index. The distribution of infested households among the studied sites showed statistical significance (p < 0.05), especially the municipality of Campo Grande, with the highest infestation rate seen in the analysis period, of 47.7% in 2012 (Table 3).

Table 3
Entomological indices of triatomines in the municipalities of the Western Mesoregion (NR), Brazil, from 2008 to 2013.

The overall colonization index corresponded to 49.6%, so that 17.3% (472/2,727) of the nymphs were located in the intradomestic space. Considering the species captured in the intradomestic environment, 71.3% (938/1,317) were T. brasiliensis. Of the species T. pseudomaculata, 85.4% (1,919/2,247) was found in the peridomestic environment (Table 1). Comparing the colonization coefficient between the locations considered in the study, a significant difference (p < 0.05) was observed, underlining the municipality of Caraúbas, with 100% domiciliation in 2013 (Table 3).

All municipalities in the study showed contaminated specimens during the analyzed period (Table 3).

The distribution of colonization rates and domestic infestation shows the progression of these values between the years 2009 and 2012, denoting the discontinuous control of entomological indicators throughout the analyzed period. There was a statistical difference (p < 0.05) between the rates of domestic and peridomestic infestation over the period analyzed, so that the peridomicile had a higher infestation rate in all years of the study (Graphic 1).

Graphic 1
Distribution of the entomological indices of the Western Mesoregion (RN), Brazil, from 2008 to 2013.

Discussion

After more than four decades of fighting Chagas’ disease vector transmission in Brazil, the setting investigated still has a wide distribution of triatomines and is among the regions originally at risk for vector transmission, along the states of Alagoas, Bahia, the Federal District, Goiás, among others, a condition explained by the number of autochthonous and potentially vector species77. Brasil. Secretaria de Vigilância em Saúde do Ministério da Saúde. Consenso Brasileiro em Doença de Chagas. Revista da Sociedade Brasileira de Medicina Tropical 2005; 38(Supl. 3):29., such as T. brasiliensis44. Lucena DT, Lima ET. Epidemiologia da doença de Chagas no Rio Grande do Norte, III - A infecção humana determinada pela reação de Guerreiro Machado. Revista Brasileira de Malariologia e Doenças Tropicais 1962; 15:361-366.

5. Brito CRN, Sampaio GHF, Câmara ACJ, Nunes DF, Azevedo PR, Chiari E, Galvão LMC. Seroepidemiology of Trypanosoma cruzi infection in the semiarid rural zone of the State of Rio Grande do Norte, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(3):346-352.

6. Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados. Rio de Janeiro: IBGE; 2010.

7. Brasil. Secretaria de Vigilância em Saúde do Ministério da Saúde. Consenso Brasileiro em Doença de Chagas. Revista da Sociedade Brasileira de Medicina Tropical 2005; 38(Supl. 3):29.
-88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147. and T. pseudomaculata99. Costa J, Almeida CE, Dotson EM, Lins A, Vinhaes M, Silveira AC, Beard CB. The epidemiologic importance of Triatoma brasiliensis as a Chagas disease vector in Brazil: a revision of domiciliary captures during 1993-1999. Memórias do Instituto Oswaldo Cruz 2003; 98(4):443-449. and the emergence of “new species”, such as P. lutzi1010. Sherlock IA, Guitton N. Fauna Triatominae do Estado da Bahia Brasil III: notas sobre ecótopos silvestres e o gênero Psammolestes. Memórias do Instituto Oswaldo Cruz. 1974; 72(1-2):91-101., all of which are found in the field of this study.

The prevalence of nymphs among the specimens captured in the region is the characteristic of the adaptive action of triatomines to the artificial ecotope, consolidated in the domestic process1111. Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias, JCP. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21(3):878-886.,1212. Brasil. Ministério da Saúde (MS). Manual de Normas Técnicas da Campanha de Controle da Doença de Chagas. Brasília: MS; 1980., which did not show a declining artificial ecotope in most of the years considered and may be related to the invasion of this environment by females in fertile period1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240..

The higher concentration of triatomines in the extradomestic space, reaffirmed by the significant difference between the means of the intradomestic and peridomestic densities was also a finding denoted in other studies1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240., and can be explained by the focus on measures to combat the domiciled vectors1414. Silva RA, Bonifácio PR, Wanderley DMV. Doença de Chagas no Estado de São Paulo: comparação entre pesquisa ativa de triatomíneos em domicílio e notificação de sua presença pela população em área sob vigilância entomológica. Revista da Sociedade Brasileira de Medicina Tropical 1999; 32(6):653-659. and by the appropriate conditions for agglomeration of colonies in the peridomicile promoted by careless cleaning of domestic annexes1515. Dias JCP. Problemas e possibilidades de participação comunitária no controle das grandes endemias. Cad Saude Publica 1999; 14(Supl. 2):19-37.. In addition, the occupation of this space can act as a defense mechanism for triatomines in response to the reduced species in the households through chemical control, which compose residues in the peridomestic space, where the insecticides do not perform satisfactorily1515. Dias JCP. Problemas e possibilidades de participação comunitária no controle das grandes endemias. Cad Saude Publica 1999; 14(Supl. 2):19-37.

16. Dias JCP, Diotaiuti LG. IWHO/TDR Technical report n. 811: small correction, proposal. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(6):582-583.
-1717. Brasil. Guia de Vigilância epidemiológica. Brasília: Ministério da Saúde; 2002. due to the effects of the climatic variations, of the direct incidence of solar rays and rainfall1818. Oliveira Filho AM. New alternatives for the control of triatomines in peridomestic buildings. Revista da Sociedade Brasileira de Medicina Tropical 1989; 22(Supl. 2):53-57..

The occupation of the domestic environment, while showing less representativeness compared to the number of specimens detected, should not be ignored, indicating the need for routine surveillance in residences of locations with high triatomine burden in the peridomicile1414. Silva RA, Bonifácio PR, Wanderley DMV. Doença de Chagas no Estado de São Paulo: comparação entre pesquisa ativa de triatomíneos em domicílio e notificação de sua presença pela população em área sob vigilância entomológica. Revista da Sociedade Brasileira de Medicina Tropical 1999; 32(6):653-659.. Studies indicate the risks of the transfer of insects from the extradomestic space to within households, related to the habits of individuals transporting wood and their own belongings from the wild environment to the household and its surroundings, which may contain triatomines, especially in the younger forms, and may cause passive dispersion of vectors1919. Freitas SPC, Freitas ALC, Prazeres SM, Gonçalves TCM. Influência de hábitos antrópicos na dispersão de Triatoma pseudomaculata Corrêa & Espínola, 1964 através de Mimosa tenuiflora (Willdenow) (Mimosaceae) no Estado do Ceará, Brasil. Cad Saude Publica 2004; 20(20):333-336.. In addition, the possibilities of transmission also go back to the development of activities such as cattle raising and the process of disorderly appropriation of the natural environment, followed by abrupt changes in vegetation and reducednumber of wild animals2020. Fernandes AJ, Diotaiuti L, Dias JCP, Romanha AJ, Chiari E. Inter-relações entre os ciclos de transmissão do Trypanosoma cruzi no município de Bambuí, Minas Gerais, Brasil. Cad Saude Publica 1994: 10(4):473-480..

The high prevalence of T. brasiliensis and T. pseudomaculata55. Brito CRN, Sampaio GHF, Câmara ACJ, Nunes DF, Azevedo PR, Chiari E, Galvão LMC. Seroepidemiology of Trypanosoma cruzi infection in the semiarid rural zone of the State of Rio Grande do Norte, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(3):346-352. was also a finding that was repeated in the states of Sergipe, Ceará33. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34., Piauí2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.

22. Carvalho DM, Gomes WS. Distribuição de triatomíneos hemíptera, reduviidae, triatominae nos municípios da mesorregião sul do estado do Ceará, no período de 2010 a 2012. Cadernos ESP 2014; 8(2):30-37.

23. Silveira AC, Vinhaes M. Doença de Chagas: Aspectos epidemiológicos e de controle. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(Sup. 2):15-60.
-2424. Diotaiuti L, Faria Filho OF, Carneiro FCF, Dias JCP, Pires HHR, Schofield CJ. Aspectos operacionais do controle do Triatoma brasiliensis. Cad Saude Publica 2000; 16(Supl. 2):61-67. and Pernambuco2525. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, Gurgel-Gonçalves R. Synanthropictriatomines (Hemiptera, Reduviidade) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45:60-65., confirming the general panorama of Chagas’ disease in the Northeast, with regard to P. megistus and T. brasiliensis,and P. megistus has decreased its occurrence practically throughout the Northeast, with T. brasiliensis being the main species, followed by T. pseudomaculata1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240..

In any of the analyzed years, the study showed infestation rates higher than those of the Northeast, in a survey conducted in the 1990s, similar to that of Ceará, in the same decade33. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34., and lower than the state of São Paulo2626. Silva RA, Rodrigues VLCC, Carvalho ME, Pauliquévis-Júnior C. Programa de Controle da Doença de Chagas no Estado de São Paulo: persistência de alta infestação por triatomíneos em localidades na década de 1990. Cad Saude Publica 2003; 19(4):965-971., data that is reaffirmed in the stagnated intradomestic and peridomestic colonization and infestation indices during the years studied, with emphasis on this last index, higher than intradomestic invasion throughout the analyzed period. In this perspective, the reduced entomological indices related to the peridomicile of the region under study is an important challenge, since the infestation of the domestic environment is not due to insecticide’s ineffectiveness, but elements such as the modification of natural areas, the use of material for the construction of annexes coming directly from the wild and without any specific treatment regarding the handling2525. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, Gurgel-Gonçalves R. Synanthropictriatomines (Hemiptera, Reduviidade) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45:60-65. and breeding of animals2727. Walter A, Rego IP, Ferreira AJ, Rogier C. Risk factors for reinvasion of humans dwellings by sylvatic triatomines in northern Bahia State, Brazil. Cad Saude Publica 2005; 21(3):974-978..

The region’s colonization index neared that reported in Piauí2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64. and exceeded the respective foci rates in the state of São Paulo1111. Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias, JCP. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21(3):878-886., Minas Gerais99. Costa J, Almeida CE, Dotson EM, Lins A, Vinhaes M, Silveira AC, Beard CB. The epidemiologic importance of Triatoma brasiliensis as a Chagas disease vector in Brazil: a revision of domiciliary captures during 1993-1999. Memórias do Instituto Oswaldo Cruz 2003; 98(4):443-449. and Rondônia2828. Massaro DC, Rezende DS, Camargo LMA. Estudo da fauna de triatomíneos e da ocorrência de doença de Chagas em Montenegro, Rondônia, Brasil. Revista Brasileira de Epidemiologia 2008; 11(2):228-240., a condition that may have been caused by reduced food demand2828. Massaro DC, Rezende DS, Camargo LMA. Estudo da fauna de triatomíneos e da ocorrência de doença de Chagas em Montenegro, Rondônia, Brasil. Revista Brasileira de Epidemiologia 2008; 11(2):228-240.,2929. Forattini OP. Biogeografia, origem e distribuição da domiciliação de triatomíneos no Brasil. Rev Saude Publica 1980; 14:265-299., modification of wild environments2929. Forattini OP. Biogeografia, origem e distribuição da domiciliação de triatomíneos no Brasil. Rev Saude Publica 1980; 14:265-299. through the deforestation or realization of fires and reduced fauna through predatory hunting, practices inherent to the field of study.

Although it represented the highest expression among the triatomines found in the intradomestic environment, since it resembles the reality of the state of Piauí2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64., the T. brasiliensis species had a peculiar behavior in the region evaluated, considering that the extradomestic space was its preferred environment. It persists as a concern and priority in Public Health in the areas of its occurrence2323. Silveira AC, Vinhaes M. Doença de Chagas: Aspectos epidemiológicos e de controle. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(Sup. 2):15-60. and is characterized by great capacity for infestation, colonization88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147.,1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240. and reinvasion of the home by wild foci2424. Diotaiuti L, Faria Filho OF, Carneiro FCF, Dias JCP, Pires HHR, Schofield CJ. Aspectos operacionais do controle do Triatoma brasiliensis. Cad Saude Publica 2000; 16(Supl. 2):61-67., establishing itself as a priority target of vector control campaigns among municipalities of states such as Piauí2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.. In this setting, considering the classification of this species as the main species1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240. and considering the high seroprevalence of Chagas’ disease, highlighting the Western mesoregion55. Brito CRN, Sampaio GHF, Câmara ACJ, Nunes DF, Azevedo PR, Chiari E, Galvão LMC. Seroepidemiology of Trypanosoma cruzi infection in the semiarid rural zone of the State of Rio Grande do Norte, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(3):346-352., the role of T. brasiliensis as a vector disseminator of T. cruzi infection is reaffirmed.

The species T. pseudomaculata, characteristic of the extradomestic space3030. Freitas SPC, Lorosa ES, Rodrigues DCS, Freitas ALC, Gonçalves TCM. Feeding patterns of Triatoma pseudomaculata in the state of Ceará, Brazil. Rev Saude Publica 2005; 39(1):27-32.,3131. Marcondes CB, Dias JCP, Guedes L A, Filho ANF, Vera LCC, Rodrigues e Mendonça DD. Estudo epidemiológico de fontes de alimentação sanguínea dos triatomíneos da fazenda aroeira (Catolé do Rocha, Paraíba) e circunvizinhanças. Revista da Sociedade Brasileira de Medicina Tropical 1991; 24(3):137-140., as in other settings investigated, was predominant in the peridomicile1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.,2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.,2222. Carvalho DM, Gomes WS. Distribuição de triatomíneos hemíptera, reduviidae, triatominae nos municípios da mesorregião sul do estado do Ceará, no período de 2010 a 2012. Cadernos ESP 2014; 8(2):30-37.,3131. Marcondes CB, Dias JCP, Guedes L A, Filho ANF, Vera LCC, Rodrigues e Mendonça DD. Estudo epidemiológico de fontes de alimentação sanguínea dos triatomíneos da fazenda aroeira (Catolé do Rocha, Paraíba) e circunvizinhanças. Revista da Sociedade Brasileira de Medicina Tropical 1991; 24(3):137-140.

32. Costa J, Lorenzo M. Biologia, diversidade e estratégias para o monitoramento e controle vetorial de triatomíneos da doença de chagas. Memórias do Instituto Oswaldo Cruz 2009; 104:46-51.
-3333. Alencar JE, Sherlock VA. Triatomíneos capturados em domicílios no Estado do Ceará, Brasil. Boletim da Sociedade Cearense de Agronomia 1962; 3:49-54., although the number of nymphs captured in the intradomestic environment surpassed that of Ceará3131. Marcondes CB, Dias JCP, Guedes L A, Filho ANF, Vera LCC, Rodrigues e Mendonça DD. Estudo epidemiológico de fontes de alimentação sanguínea dos triatomíneos da fazenda aroeira (Catolé do Rocha, Paraíba) e circunvizinhanças. Revista da Sociedade Brasileira de Medicina Tropical 1991; 24(3):137-140., Piauí and Paraíba2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.,3131. Marcondes CB, Dias JCP, Guedes L A, Filho ANF, Vera LCC, Rodrigues e Mendonça DD. Estudo epidemiológico de fontes de alimentação sanguínea dos triatomíneos da fazenda aroeira (Catolé do Rocha, Paraíba) e circunvizinhanças. Revista da Sociedade Brasileira de Medicina Tropical 1991; 24(3):137-140.. The condition of occupation of T. pseudomaculata restricted to the peridomicile determines the difficulty for the traditional chemical control, since the insecticides demonstrate a transient effect in a situation in which the habitat corresponds to the extradomestic space, so that reinfestation becomes a common process2424. Diotaiuti L, Faria Filho OF, Carneiro FCF, Dias JCP, Pires HHR, Schofield CJ. Aspectos operacionais do controle do Triatoma brasiliensis. Cad Saude Publica 2000; 16(Supl. 2):61-67.,3434. Barbu C, Dumonteil E, Gourbiere S. Optimization of control strategies for non-domiciliated Triatoma dimidata, Chagas disease vector in the Yucatán peninsula, Mexico. Public Library of Science Neglected Tropical Diseases 2009; 3:e416., attributed to the great pressure of recolonization by this species2424. Diotaiuti L, Faria Filho OF, Carneiro FCF, Dias JCP, Pires HHR, Schofield CJ. Aspectos operacionais do controle do Triatoma brasiliensis. Cad Saude Publica 2000; 16(Supl. 2):61-67.. However, its classification as a second species in intradomestic space triatominal density, right after T. brasiliensis, reinforces its progressive adaptation to the artificial ecotope, as reported in other studies33. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34.,3535. Dias JCP. Vigilância epidemiológica em doença de Chagas. Cad Saude Publica 2000; 16(2):S43-S59.. Habits such as passive firewood management for daily use and timber transportation are considered as possible facilitating factors for the residence of T. pseudomaculata2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64., in addition to, in the situation of a larger number of specimens, this species colonizing the interior of households and take over the spot of T. brasiliensis. In addition, it was found that certain man-made structures were occupied by both species, indicating that T. pseudomaculata is gradually becoming dominant1616. Dias JCP, Diotaiuti LG. IWHO/TDR Technical report n. 811: small correction, proposal. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(6):582-583., maintaining infestation and colonization levels both in the household and in the peridomicile, with great invasive potential and is difficult to control1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.. Therefore, the adaptation of T. pseudomaculata to the intradomestic behavior raises the need for further investigation, given that the approximation of vectors with human living spaces increases the risk of transmission of Chagas disease2222. Carvalho DM, Gomes WS. Distribuição de triatomíneos hemíptera, reduviidae, triatominae nos municípios da mesorregião sul do estado do Ceará, no período de 2010 a 2012. Cadernos ESP 2014; 8(2):30-37..

The study shows the persistence of triatomines capable of transmitting T. cruzi in the region, so that the natural infection index was similar to that found in the same state in the 1980s33. Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34., although the proportion of infected triatomines has been low, as shown in another study3636. Silva RA, Barbosa GL, Rodrigues VLCC. Epidemiological Surveillance of Chagas disease in the State of São Paulo, Brazil, 2010-2012. Revista Epidemiologia e Serviços de Saúde 2014; 23(2):259-267., and is lower than that observed in the state of Piauí66. Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados. Rio de Janeiro: IBGE; 2010. and in Minas Gerais1111. Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias, JCP. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21(3):878-886.,3737. Fernandes HM, Costa C. Índice de triatomíneos positivos para Trypanosoma Cruzi, em Monte Carmelo (MG), no período de 2005 a 2009. GETEC 2012; 1(1):59-69..

Among the infected species detected in the intradomestic environment, it is worth noting that, although it evidenced lower intradomestic and peridomestic density than T. brasiliensis, P. lutzi showed the highest rate of natural infection among the species considered and was distributed in almost all of the locations of the study, deserving attention for the increased number of captures in Brazil3838. Silveira AC, Dias JCP. O controle da transmissão vetorial. Revista da Sociedade Brasileira de Medicina Tropical 2011; 44(2):52-63., as it can easily form colonies inside the households1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240. and has one of the highest rates of natural infection in other locations2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.,3838. Silveira AC, Dias JCP. O controle da transmissão vetorial. Revista da Sociedade Brasileira de Medicina Tropical 2011; 44(2):52-63..

T. brasiliensis also showed representativeness and is the main vector in the transmission of T. cruzi in Northeast Brazil88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147.,99. Costa J, Almeida CE, Dotson EM, Lins A, Vinhaes M, Silveira AC, Beard CB. The epidemiologic importance of Triatoma brasiliensis as a Chagas disease vector in Brazil: a revision of domiciliary captures during 1993-1999. Memórias do Instituto Oswaldo Cruz 2003; 98(4):443-449.,2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64. and greater power of synanthropy88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147.,3939. Dias DM, Dantas LNA, Dantas JO. Distribuição geográfica dos vetores de chagas em Sergipe. Revista Multidisciplinar da UNIESP 2010; 10:50-56.,4040. Alencar JE. História natural da doença de Chagas no Estado do Ceará. Fortaleza: Imprensa Universitária da Universidade Federal do Ceará; 1987..

The T. pseudomaculata species also showed infected captured specimens, although some studies consider that the risk for vector transmission through this species is low when compared to T. brasiliensis4141. Forattini OP, Barata JMS, Santos JLF, Silveira AC. Hábitos alimentares, infecção natural e distribuição de triatomíneos domiciliados na Região Nordeste do Brasil. Rev Saude Publica 1981; 15(2):113-164. due to its low conversion rate for metacyclic trypomastigotes3232. Costa J, Lorenzo M. Biologia, diversidade e estratégias para o monitoramento e controle vetorial de triatomíneos da doença de chagas. Memórias do Instituto Oswaldo Cruz 2009; 104:46-51.,4040. Alencar JE. História natural da doença de Chagas no Estado do Ceará. Fortaleza: Imprensa Universitária da Universidade Federal do Ceará; 1987.,4242. Perlowagora-Szumlewicz A, Moreira CJC. In vivo differentiation of Trypanosoma cruzi-1. Experimental evidence of the influence of vector species on metacyclogenesis. Memórias do Instituto Oswaldo Cruz 1994; 89(4):603-618., the infecting form of vertebrates3232. Costa J, Lorenzo M. Biologia, diversidade e estratégias para o monitoramento e controle vetorial de triatomíneos da doença de chagas. Memórias do Instituto Oswaldo Cruz 2009; 104:46-51.. On the other hand, while some studies show a low natural rate of infection1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.,4343. Silveira EA, Ribeiro IS, Amorim MS, Rocha DV, Coutinho HS, Freitas LM, Tomazi L, Silva RAA. Correlation between infection rate of triatominies and Chagas Disease in Southwest of Bahia, Brazil: a warning sign? Anais da Academia Brasileira de Ciências 2016; 11p., a survey carried out in the state of Bahia showed that all samples of T. pseudomaculata collected for seroprevalence responded positively to the T. cruzi test, which denotes the representativeness of this species in the transmission in regions where the presence of the vector is clear1010. Sherlock IA, Guitton N. Fauna Triatominae do Estado da Bahia Brasil III: notas sobre ecótopos silvestres e o gênero Psammolestes. Memórias do Instituto Oswaldo Cruz. 1974; 72(1-2):91-101..

The P. megistus species, despite being a highly dispersed agent in the Brazilian territory, with a recognized potential for infestation and colonization of households2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64. and high levels of infection2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.,4444. Ferraz Filho AN, Rodrigues VLCC. Distribuição e índice de infecção natural de triatomíneos capturados na região de Campinas, São Paulo, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 1987; 20(1):25-30.,4545. Dias JCP. Doença de Chagas, ambiente, participação e Estado. Cad Saude Publica 2001; 17(Supl.):165-169., showed low density in the evaluated region, besides not having evidenced no positive species for T. cruzi1010. Sherlock IA, Guitton N. Fauna Triatominae do Estado da Bahia Brasil III: notas sobre ecótopos silvestres e o gênero Psammolestes. Memórias do Instituto Oswaldo Cruz. 1974; 72(1-2):91-101.,2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64., differently from the State of Ceará and Bahia in the 1990s and the Federal District1010. Sherlock IA, Guitton N. Fauna Triatominae do Estado da Bahia Brasil III: notas sobre ecótopos silvestres e o gênero Psammolestes. Memórias do Instituto Oswaldo Cruz. 1974; 72(1-2):91-101.,1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.,4646. Maeda MH, Knox MB, Gurgel-Gonçalves R. Ocorrência de triatomíneos sinantrópicos (Hemiptera: Reduviidae) no Distrito Federal, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(1):71-76.. We would like to add that this was the only species among the ones found that did not have any nymph captured in the intradomestic environment. However, this finding does not disqualify the epidemiological importance of the species for the area, since the presence of adults in the peridomestic environment can trigger the establishment of colonies in the intradomestic space and maintenance of the parasite’s transmission cycle1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240..

Similarly, the R. nasutus species had a reduced number of specimens captured and none of the triatomines evaluated were contaminated, as also shown by the literature2323. Silveira AC, Vinhaes M. Doença de Chagas: Aspectos epidemiológicos e de controle. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(Sup. 2):15-60.. However, it is worth mentioning that two-thirds of the numbers detected were in the intradomestic environment, a finding that diverged from other reported realities88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147.,1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.,2121. Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64., showing that, although this species does not frequently colonize households, a possible household invasion may occur from wild environments, increasing the risk of household vector transmission without actual colonization4747. Falavigna-Guilherme AL, Costa AL, Batista O, Pavanelli GC, Araújo SM. Atividades educativas para o controle de triatomíneos em área de vigilância epidemiológica do Estado do Paraná, Brasil. Cad Saude Publica 2002; 18(6):1543-1550.

48. Silva RA, Wanderley DMV, Domingos MF, Yasumaro S, Scandar SAS, Pauliquévis-Júnior C, Sampaio SMP, Takaku L, Rodrigues VLCC. Doença de Chagas: notificação de triatomíneos no Estado de São Paulo na década de 1990. Revista da Sociedade Brasileira de Medicina Tropical 2006; 39(5):488-494.
-4949. Dias JCP, Dias RB. Participação da comunidade no controle da doença de Chagas. Anales de la Societè Belge de Medicine Tropicale 1985; 65(Supl. 1):127-135..

A significant statistical association between triatomine distribution and study sites was found, similar to the findings in the Federal District4747. Falavigna-Guilherme AL, Costa AL, Batista O, Pavanelli GC, Araújo SM. Atividades educativas para o controle de triatomíneos em área de vigilância epidemiológica do Estado do Paraná, Brasil. Cad Saude Publica 2002; 18(6):1543-1550. and in Piauí88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147.. Several factors may explain this situation, from the assiduity of the surveillance actions of the endemic agents in the municipalities99. Costa J, Almeida CE, Dotson EM, Lins A, Vinhaes M, Silveira AC, Beard CB. The epidemiologic importance of Triatoma brasiliensis as a Chagas disease vector in Brazil: a revision of domiciliary captures during 1993-1999. Memórias do Instituto Oswaldo Cruz 2003; 98(4):443-449., encompassing the whole rural area characteristic of each location, the environmental conditions, the state and organization of households and the community’s commitment to surveillance of triatomines88. Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147..

The lack of declining infestation and colonization rates in most of the years addressed in the study can be explained by the appearance of other diseases, such as dengue2626. Silva RA, Rodrigues VLCC, Carvalho ME, Pauliquévis-Júnior C. Programa de Controle da Doença de Chagas no Estado de São Paulo: persistência de alta infestação por triatomíneos em localidades na década de 1990. Cad Saude Publica 2003; 19(4):965-971.,5050. Wanderley DMV. Perspectivas de controle da doença de Chagas no Estado de São Paulo [tese]. São Paulo: Faculdade de Saúde Pública; 1994. and American visceral leishmaniasis2626. Silva RA, Rodrigues VLCC, Carvalho ME, Pauliquévis-Júnior C. Programa de Controle da Doença de Chagas no Estado de São Paulo: persistência de alta infestação por triatomíneos em localidades na década de 1990. Cad Saude Publica 2003; 19(4):965-971., which triggered the redirection of activities in the area of education in health and interfered with the actions of notification of triatomines by populations5151. Dias JVL, Queiroz DRM, Diotaiuti L, Pires HHR. Conhecimentos sobre triatomíneos e sobre a doença de Chagas em localidades com diferentes níveis de infestação vetorial. Cien Saude Colet 2016; 21(7):2293-2303.. In addition, low prevalence rates of Chagas’ disease in some regions and political-administrative issues related to systematic control programs4646. Maeda MH, Knox MB, Gurgel-Gonçalves R. Ocorrência de triatomíneos sinantrópicos (Hemiptera: Reduviidae) no Distrito Federal, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(1):71-76. have contributed to the disrupted follow-up of entomological surveys over the years2626. Silva RA, Rodrigues VLCC, Carvalho ME, Pauliquévis-Júnior C. Programa de Controle da Doença de Chagas no Estado de São Paulo: persistência de alta infestação por triatomíneos em localidades na década de 1990. Cad Saude Publica 2003; 19(4):965-971.,4646. Maeda MH, Knox MB, Gurgel-Gonçalves R. Ocorrência de triatomíneos sinantrópicos (Hemiptera: Reduviidae) no Distrito Federal, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(1):71-76..

Findings of the study demonstrate that the main obstacle to be overcome in the Chagas disease vector transmission control is continuous surveillance, assuming that household invasions from the extradomestic environment will always be possible1111. Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias, JCP. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21(3):878-886.. In this context, community participation in the triatomine detection process is required4747. Falavigna-Guilherme AL, Costa AL, Batista O, Pavanelli GC, Araújo SM. Atividades educativas para o controle de triatomíneos em área de vigilância epidemiológica do Estado do Paraná, Brasil. Cad Saude Publica 2002; 18(6):1543-1550. in order to decentralize of entomological surveillance actions by the field teams4848. Silva RA, Wanderley DMV, Domingos MF, Yasumaro S, Scandar SAS, Pauliquévis-Júnior C, Sampaio SMP, Takaku L, Rodrigues VLCC. Doença de Chagas: notificação de triatomíneos no Estado de São Paulo na década de 1990. Revista da Sociedade Brasileira de Medicina Tropical 2006; 39(5):488-494., a measure with a significant impact, as demonstrated in some regions1111. Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias, JCP. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21(3):878-886.,1313. Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.,4747. Falavigna-Guilherme AL, Costa AL, Batista O, Pavanelli GC, Araújo SM. Atividades educativas para o controle de triatomíneos em área de vigilância epidemiológica do Estado do Paraná, Brasil. Cad Saude Publica 2002; 18(6):1543-1550.,4949. Dias JCP, Dias RB. Participação da comunidade no controle da doença de Chagas. Anales de la Societè Belge de Medicine Tropicale 1985; 65(Supl. 1):127-135.

50. Wanderley DMV. Perspectivas de controle da doença de Chagas no Estado de São Paulo [tese]. São Paulo: Faculdade de Saúde Pública; 1994.
-5151. Dias JVL, Queiroz DRM, Diotaiuti L, Pires HHR. Conhecimentos sobre triatomíneos e sobre a doença de Chagas em localidades com diferentes níveis de infestação vetorial. Cien Saude Colet 2016; 21(7):2293-2303..

Final considerations

The focus setting demonstrated a still critical area for the proliferation of Chagas’ disease, given the numbers of captured triatomines and the potential vectors detected in the region, such as T. brasiliensis, representing the highest intradomestic density among captured triatomines; P. lutzi, characterizing the highest rate of natural infection; and T. pseudomaculata, which has entered households, translating its adaptive action to the various ecotopes of human experience. It is also worth noting that this study faxed some limitations, which started from the lack of data referring to some locations, a factor that may have underestimated the actual indexes analyzed.

The recognition of the entomological triatomine-related indicators in the region facilitated the approximation with the distribution of vectors and the vulnerability of communities to the T. cruzi infection, and was a relevant tool for the design of control and surveillance actions that avoid the possibility of propagation of the most popular species and prevent the recrudescence of the extirpated species.

We suggested the systematic follow-up of entomological surveillance by field teams, as well as the involvement of local communities in the detection, recognition and consequent notification of vectors in the intradomestic and peridomestic spaces and in the reorganization of the surroundings of households, highlighting the appropriation of measures that promote popular education in health as the strengthening element of this process.

References

  • 1
    World Health Organization (WHO). Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly epidemiological record 2015; 90(6):33-44.
  • 2
    Gurgel-Gonçalves RC, Galvão C, Costa J, Peterson AT. Geographic distribution of Chagas disease vectors in Brazil based on ecological niche modeling. J Trop Med 2012; 2012:705326.
  • 3
    Dias JCP, Machado EMM, Fernandes AL, Vinhaes MC. Esboço geral e perspectivas da doença de Chagas no Nordeste do Brasil. Cad Saude Publica 2000; 16(2):13-34.
  • 4
    Lucena DT, Lima ET. Epidemiologia da doença de Chagas no Rio Grande do Norte, III - A infecção humana determinada pela reação de Guerreiro Machado. Revista Brasileira de Malariologia e Doenças Tropicais 1962; 15:361-366.
  • 5
    Brito CRN, Sampaio GHF, Câmara ACJ, Nunes DF, Azevedo PR, Chiari E, Galvão LMC. Seroepidemiology of Trypanosoma cruzi infection in the semiarid rural zone of the State of Rio Grande do Norte, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(3):346-352.
  • 6
    Instituto Brasileiro de Geografia e Estatística (IBGE). Cidades e Estados Rio de Janeiro: IBGE; 2010.
  • 7
    Brasil. Secretaria de Vigilância em Saúde do Ministério da Saúde. Consenso Brasileiro em Doença de Chagas. Revista da Sociedade Brasileira de Medicina Tropical 2005; 38(Supl. 3):29.
  • 8
    Sarquis O, Sposina R, Oliveira TG, MacCord JR, Cabello PH, Borges-Pereira J, Lima MM. Aspects of peridomiciliar ecotopes in rural areas of Northeastern Brazil associated to triatomine (Hemiptera, Reduviidae) infestation, vectors of Chagas disease. Memórias do Instituto Oswaldo Cruz 2006; 101(2):143-147.
  • 9
    Costa J, Almeida CE, Dotson EM, Lins A, Vinhaes M, Silveira AC, Beard CB. The epidemiologic importance of Triatoma brasiliensis as a Chagas disease vector in Brazil: a revision of domiciliary captures during 1993-1999. Memórias do Instituto Oswaldo Cruz 2003; 98(4):443-449.
  • 10
    Sherlock IA, Guitton N. Fauna Triatominae do Estado da Bahia Brasil III: notas sobre ecótopos silvestres e o gênero Psammolestes. Memórias do Instituto Oswaldo Cruz 1974; 72(1-2):91-101.
  • 11
    Villela MM, Souza JB, Mello VP, Azeredo BVM, Dias, JCP. Vigilância entomológica da doença de Chagas na região centro-oeste de Minas Gerais, Brasil, entre os anos de 2000 e 2003. Cad Saude Publica 2005; 21(3):878-886.
  • 12
    Brasil. Ministério da Saúde (MS). Manual de Normas Técnicas da Campanha de Controle da Doença de Chagas Brasília: MS; 1980.
  • 13
    Freitas ALC, Freitas SPC, Gonçalves TCM, Lima Neto AS. Vigilância Entomológica dos Vetores da Doença de Chagas no Município de Farias Brito, Estado do Ceará-Brasil. Cadernos de Saúde Coletiva 2007; 15(2):231-240.
  • 14
    Silva RA, Bonifácio PR, Wanderley DMV. Doença de Chagas no Estado de São Paulo: comparação entre pesquisa ativa de triatomíneos em domicílio e notificação de sua presença pela população em área sob vigilância entomológica. Revista da Sociedade Brasileira de Medicina Tropical 1999; 32(6):653-659.
  • 15
    Dias JCP. Problemas e possibilidades de participação comunitária no controle das grandes endemias. Cad Saude Publica 1999; 14(Supl. 2):19-37.
  • 16
    Dias JCP, Diotaiuti LG. IWHO/TDR Technical report n. 811: small correction, proposal. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(6):582-583.
  • 17
    Brasil. Guia de Vigilância epidemiológica Brasília: Ministério da Saúde; 2002.
  • 18
    Oliveira Filho AM. New alternatives for the control of triatomines in peridomestic buildings. Revista da Sociedade Brasileira de Medicina Tropical 1989; 22(Supl. 2):53-57.
  • 19
    Freitas SPC, Freitas ALC, Prazeres SM, Gonçalves TCM. Influência de hábitos antrópicos na dispersão de Triatoma pseudomaculata Corrêa & Espínola, 1964 através de Mimosa tenuiflora (Willdenow) (Mimosaceae) no Estado do Ceará, Brasil. Cad Saude Publica 2004; 20(20):333-336.
  • 20
    Fernandes AJ, Diotaiuti L, Dias JCP, Romanha AJ, Chiari E. Inter-relações entre os ciclos de transmissão do Trypanosoma cruzi no município de Bambuí, Minas Gerais, Brasil. Cad Saude Publica 1994: 10(4):473-480.
  • 21
    Gurgel-Gonçalves R, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Revista Pan-Amaz Saúde 2008; 1(4):57-64.
  • 22
    Carvalho DM, Gomes WS. Distribuição de triatomíneos hemíptera, reduviidae, triatominae nos municípios da mesorregião sul do estado do Ceará, no período de 2010 a 2012. Cadernos ESP 2014; 8(2):30-37.
  • 23
    Silveira AC, Vinhaes M. Doença de Chagas: Aspectos epidemiológicos e de controle. Revista da Sociedade Brasileira de Medicina Tropical 1998; 31(Sup. 2):15-60.
  • 24
    Diotaiuti L, Faria Filho OF, Carneiro FCF, Dias JCP, Pires HHR, Schofield CJ. Aspectos operacionais do controle do Triatoma brasiliensis. Cad Saude Publica 2000; 16(Supl. 2):61-67.
  • 25
    Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, Gurgel-Gonçalves R. Synanthropictriatomines (Hemiptera, Reduviidade) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45:60-65.
  • 26
    Silva RA, Rodrigues VLCC, Carvalho ME, Pauliquévis-Júnior C. Programa de Controle da Doença de Chagas no Estado de São Paulo: persistência de alta infestação por triatomíneos em localidades na década de 1990. Cad Saude Publica 2003; 19(4):965-971.
  • 27
    Walter A, Rego IP, Ferreira AJ, Rogier C. Risk factors for reinvasion of humans dwellings by sylvatic triatomines in northern Bahia State, Brazil. Cad Saude Publica 2005; 21(3):974-978.
  • 28
    Massaro DC, Rezende DS, Camargo LMA. Estudo da fauna de triatomíneos e da ocorrência de doença de Chagas em Montenegro, Rondônia, Brasil. Revista Brasileira de Epidemiologia 2008; 11(2):228-240.
  • 29
    Forattini OP. Biogeografia, origem e distribuição da domiciliação de triatomíneos no Brasil. Rev Saude Publica 1980; 14:265-299.
  • 30
    Freitas SPC, Lorosa ES, Rodrigues DCS, Freitas ALC, Gonçalves TCM. Feeding patterns of Triatoma pseudomaculata in the state of Ceará, Brazil. Rev Saude Publica 2005; 39(1):27-32.
  • 31
    Marcondes CB, Dias JCP, Guedes L A, Filho ANF, Vera LCC, Rodrigues e Mendonça DD. Estudo epidemiológico de fontes de alimentação sanguínea dos triatomíneos da fazenda aroeira (Catolé do Rocha, Paraíba) e circunvizinhanças. Revista da Sociedade Brasileira de Medicina Tropical 1991; 24(3):137-140.
  • 32
    Costa J, Lorenzo M. Biologia, diversidade e estratégias para o monitoramento e controle vetorial de triatomíneos da doença de chagas. Memórias do Instituto Oswaldo Cruz 2009; 104:46-51.
  • 33
    Alencar JE, Sherlock VA. Triatomíneos capturados em domicílios no Estado do Ceará, Brasil. Boletim da Sociedade Cearense de Agronomia 1962; 3:49-54.
  • 34
    Barbu C, Dumonteil E, Gourbiere S. Optimization of control strategies for non-domiciliated Triatoma dimidata, Chagas disease vector in the Yucatán peninsula, Mexico. Public Library of Science Neglected Tropical Diseases 2009; 3:e416.
  • 35
    Dias JCP. Vigilância epidemiológica em doença de Chagas. Cad Saude Publica 2000; 16(2):S43-S59.
  • 36
    Silva RA, Barbosa GL, Rodrigues VLCC. Epidemiological Surveillance of Chagas disease in the State of São Paulo, Brazil, 2010-2012. Revista Epidemiologia e Serviços de Saúde 2014; 23(2):259-267.
  • 37
    Fernandes HM, Costa C. Índice de triatomíneos positivos para Trypanosoma Cruzi, em Monte Carmelo (MG), no período de 2005 a 2009. GETEC 2012; 1(1):59-69.
  • 38
    Silveira AC, Dias JCP. O controle da transmissão vetorial. Revista da Sociedade Brasileira de Medicina Tropical 2011; 44(2):52-63.
  • 39
    Dias DM, Dantas LNA, Dantas JO. Distribuição geográfica dos vetores de chagas em Sergipe. Revista Multidisciplinar da UNIESP 2010; 10:50-56.
  • 40
    Alencar JE. História natural da doença de Chagas no Estado do Ceará Fortaleza: Imprensa Universitária da Universidade Federal do Ceará; 1987.
  • 41
    Forattini OP, Barata JMS, Santos JLF, Silveira AC. Hábitos alimentares, infecção natural e distribuição de triatomíneos domiciliados na Região Nordeste do Brasil. Rev Saude Publica 1981; 15(2):113-164.
  • 42
    Perlowagora-Szumlewicz A, Moreira CJC. In vivo differentiation of Trypanosoma cruzi-1. Experimental evidence of the influence of vector species on metacyclogenesis. Memórias do Instituto Oswaldo Cruz 1994; 89(4):603-618.
  • 43
    Silveira EA, Ribeiro IS, Amorim MS, Rocha DV, Coutinho HS, Freitas LM, Tomazi L, Silva RAA. Correlation between infection rate of triatominies and Chagas Disease in Southwest of Bahia, Brazil: a warning sign? Anais da Academia Brasileira de Ciências 2016; 11p.
  • 44
    Ferraz Filho AN, Rodrigues VLCC. Distribuição e índice de infecção natural de triatomíneos capturados na região de Campinas, São Paulo, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 1987; 20(1):25-30.
  • 45
    Dias JCP. Doença de Chagas, ambiente, participação e Estado. Cad Saude Publica 2001; 17(Supl.):165-169.
  • 46
    Maeda MH, Knox MB, Gurgel-Gonçalves R. Ocorrência de triatomíneos sinantrópicos (Hemiptera: Reduviidae) no Distrito Federal, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 2012; 45(1):71-76.
  • 47
    Falavigna-Guilherme AL, Costa AL, Batista O, Pavanelli GC, Araújo SM. Atividades educativas para o controle de triatomíneos em área de vigilância epidemiológica do Estado do Paraná, Brasil. Cad Saude Publica 2002; 18(6):1543-1550.
  • 48
    Silva RA, Wanderley DMV, Domingos MF, Yasumaro S, Scandar SAS, Pauliquévis-Júnior C, Sampaio SMP, Takaku L, Rodrigues VLCC. Doença de Chagas: notificação de triatomíneos no Estado de São Paulo na década de 1990. Revista da Sociedade Brasileira de Medicina Tropical 2006; 39(5):488-494.
  • 49
    Dias JCP, Dias RB. Participação da comunidade no controle da doença de Chagas. Anales de la Societè Belge de Medicine Tropicale 1985; 65(Supl. 1):127-135.
  • 50
    Wanderley DMV. Perspectivas de controle da doença de Chagas no Estado de São Paulo [tese]. São Paulo: Faculdade de Saúde Pública; 1994.
  • 51
    Dias JVL, Queiroz DRM, Diotaiuti L, Pires HHR. Conhecimentos sobre triatomíneos e sobre a doença de Chagas em localidades com diferentes níveis de infestação vetorial. Cien Saude Colet 2016; 21(7):2293-2303.

Publication Dates

  • Publication in this collection
    02 May 2019
  • Date of issue
    Apr 2019

History

  • Received
    07 Dec 2016
  • Reviewed
    06 July 2017
  • Accepted
    08 July 2017
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