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Entomological indicators and food sources of triatomines in the Brazilian semi-arid region

ABSTRACT

Background:

Triatomines are biological vectors of Trypanosoma cruzi, the etiological agent of Chagas Disease (CD) and have various mammalian hosts. This study evaluated the entomological indicators and food sources of triatomines in Petrolina in the semi-arid region of Brazil, where CD is endemic.

Methods:

Triatomines were captured indoors and outdoors through an active search and entomological indices (household and natural infections) were calculated. Parasitological analyses were performed through microscopic visualization using Giemsa-stained insect feces, and DNA sequencing was employed to identify food sources from the gut contents of 82 insects (9.05%) that were better preserved.

Results:

We captured triatomines (906) in peridomicile (807) and intradomicile (99): Triatoma brasiliensis (84.7%, 767 specimens), Triatoma spp. (8.2%, 74 specimens), T. pseudomaculata (6.5%, 59 specimens), Rhodnius spp. (0.4%, four specimens), R. nasutus (0.1%, one specimen), and T. sordida (0.1%, one specimen). The household infestation index is 11.8%. Thirty-five triatomines were infected (33 T. brasiliensis and two T. pseudomaculata), corresponding to a natural infection index of 3.8%. The identified food sources were human T. pseudomaculata and T. brasiliensis, dogs for T. brasiliensis and rodents (Mus musculus) for T. brasiliensis.

Conclusions:

The results reinforce the need to intensify CD diagnosis, surveillance, and control actions, as an increase in entomological indices was recorded. Blood from humans and domestic and synanthropic animals was detected in the infected triatomines, suggesting a risk of CD vector transmission in Petrolina. As CD is a zoonosis, multidisciplinary and intersectoral CD surveillance must be conducted in the context of the One Health.

Keywords:
Vectors; Household infestation index; Natural infection index; Disease ecology; Epidemiology; One Health

INTRODUCTION

Triatomines (Hemiptera, Triatominae) are vectors of Trypanosoma cruzi (Chagas, 1909) (Kinetoplastida, Trypanosomatidae), a protozoan that causes Chagas Disease (CD)11. Organização Pan Americana de Saúde (OPAS). Dia Mundial da Doença de Chagas: trazendo uma doença esquecida à atenção mundial [Internet]. Washington D.C.: 2020 [updated 2020 Apr 14; cited 2024 Feb 26]. Available from: Available from: https://www.paho.org/pt/noticias/14-4-2020-dia-mundial-da-doenca-chagas-trazendo-uma-doenca-esquecida-atencao-mundial
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. Neglected tropical diseases are endemic in 21 countries in Latin America, with approximately 6-8 million infected individuals, 30,000 cases per year and 10,000 deaths22. Organização Pan Americana de Saúde (OPAS). Menos de 10 % dos infectados com doença de Chagas recebem diagnóstico e tratamento oportunos [Internet]. Washington D.C.: 2022 [updated 2022 Apr 13; cited 2023 Sep 29]. Available from: Available from: https://www.paho.org/pt/noticias/13-4-2022-menos-10-dos-infectados-com-doenca-chagas-recebem-diagnostico-e-tratamento
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. Transmission also occurs through ingestion of food contaminated with T. cruzi33. Santos AMS, Almeida JC, Villa-Verde DMS. Doença de Chagas transmitida por via oral no Brasil. Rev Episteme Transversalis 2021;12(2):246-75..

Triatomines are found in domestic, peridomestic, and wild environments44. Argolo AM, Felix M, Pacheco R, Costa J. Doença de Chagas e seus principais vetores no Brasil. Rio de Janeiro: Imperial Novo Milênio; 2008. 63 p., and 64 species of Hemiptera have been identified in Brazil55. Bittinelli IF, Oliveira J, Reis YV, Ravazi A, Madeira FF, Oliveira ABB, et al. Do not judge a book by its cover: would Triatoma tibiamaculata (Pinto, 1926) belong to Triatoma Laporte, 1832, or to Panstrongylus Berg, 1879, with misleading homoplasies? Parasit Vectors 2022;15(1):184. Available from: https://doi.org/10.1186/s13071-022-05314-7
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-66. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Boletim epidemiológico - Territorialização e vulnerabilidade para doença de Chagas crônica. Edição especial. Brasília: 2022. 53 p.. In Pernambuco, 14 species have already been recorded77. Silva MBA, Rocha DS, Borba RFB. Triatomíneos Sinantrópicos de Pernambuco: Biogeografia, técnicas laboratoriais e controle da qualidade. Recife: EDUPE; 2019. 170 p., namely: Panstrongylus geniculatus (Latreille, 1811), Panstrongylus megistus (Burmeister, 1835), Panstrongylus lutzi (Neiva & Pinto, 1923), Panstrongylus tibiamaculatus (Pinto, 1926), Rhodnius nasutus Stål, 1859, Rhodnius neglectus Lent, 1954, Triatoma brasiliensis Neiva, 1911, Triatoma infestans (Klug, 1834), Triatoma melanocephala Neiva & Pinto, 1923, Triatoma pseudomaculata Corrêa & Espínola, 1964, Triatoma petrocchiae Pinto & Barreto, 1925, Triatoma rubrofasciata (De Geer, 1773), Triatoma sordida (Stål, 1859), and Psammolestes tertius Lent & Jurberg, 196588. Galvão C, Gurgel-Gonçalves RG. Vetores conhecidos no Brasil. In: Galvão C, editor. Vetores da doença de chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia - Série Zoologia: guias e manuais de identificação; 2014. p. 88-70.

9. Jurberg J, Rodrigues JMS, Moreira FFF, Dale C, Cordeiro IRS, Lamas Jr VD, et al. Atlas Iconográfico dos Triatomíneos do Brasil (Vetores da Doença de Chagas). Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos. Rio de Janeiro: Instituto Oswaldo Cruz; 2014. 52 p.

10. Silva TRM, Barros GMMR, Lima TARF, Giannelli A, Silva GM, Alves KML, et al. Spatial distribution of triatomine bugs in a Chagas disease endemic region in Brazil. Rev Soc Bras Med Trop 2019;52:1-5. Available from: https://doi.org/10.1590/0037-8682-0278-2019
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-1111. Ministério da Saúde (MS). Secretaria de vigilância em Saúde. Boletim Epidemiológico - Doença de Chagas Aguda e distribuição espacial dos triatomíneos de importância epidemiológica, Brasil 2012 a 2016. Brasília:2019;50(2):1-10.. T. brasiliensis and T. pseudomaculata are the most relevant species throughout northeastern Brazil66. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde. Boletim epidemiológico - Territorialização e vulnerabilidade para doença de Chagas crônica. Edição especial. Brasília: 2022. 53 p.,1212. Costa J, Dale C, Galvão C, Almeida CE, Dujardin JP. Do the new triatomine species pose new challenges or strategies for monitoring Chagas disease? An overview from 1979-2021. Mem Inst Oswaldo Cruz 2021;116:1-10. Available from: https://doi.org/10.1590/0074-02760210015
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as they have a high capacity for adaptation to intra-domestic, peridomestic, and wild environments, although T. brasiliensis presents superior vector capacity and competence1313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
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The transmission of T. cruzi occurs in three cycles: (i) wild, which involves triatomines and wild mammals; (ii) peridomestic animals, including domestic animals (dogs, cats, pigs, and goats), synanthropic animals (such as marsupials and rodents), and wild triatomines, which are attracted to food sources inside homes; and (iii) domestic animals, which are related to transmission between humans, domestic animals, and triatomines1414. Coura JR, Dias JCP. Epidemiology, control and surveillance of Chagas disease - 100 years after its discovery. Mem Inst Oswaldo Cruz 2009;104(1):31-40. Available from: https://doi.org/10.1590/S0074-02762009000900006
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15. Zetun CB, Lucheis SB, Troncarelli MZ, Langoni H. Infecção por Trypanosoma cruzi em animais silvestres procedentes de zoológicos do estado de São Paulo. Vet Zootec 2014;21(1):139-47.
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Mammals from different orders act as hosts for T. cruzi and those that stand out in the morphoclimatic domain of the Caatingas, in the Brazilian semi-arid region1717. Bezerra CM, Cavalcanti LPG, Souza RCM, Barbosa SE, Xavier SCC, Jansen AM, et al. Domestic, Peridomestic and wild hosts in the transmission of Trypanosoma cruzi in the Caatinga area colonised by Triatoma brasiliensis. Mem Inst Oswaldo Cruz 2014;109(7):887-98. Available from: https://doi.org/10.1590/0074-0276140048
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. Dogs act as sentinels to identify areas at risk of CD emergence, as highlighted in studies in Argentina1919. Gürtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE. Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 2007;134(1):69-82. Available from: https://doi.org/10.1017/S0031182006001259
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, Brazil2020. Roque ALR, Jansen AM. Importância dos animais domésticos sentinelas na identificação de áreas de risco de emergência de doença de Chagas. Rev Soc Bras Med Trop 2008;41(3):191-3., and the United States2121. Kjos SA, Marcet PL, Yabsley MJ, Kitron U, Snowden KF, Logan KS, et al. Identification of bloodmeal sources and Trypanosoma cruzi infection in triatomine bugs (Hemiptera: Reduviidae) from residential settings in Texas, the United States. J Med Entomol 2013;50(5):1126-39. Available from: https://doi.org/10.1603/me12242
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. These mammals are considered one of the primary elements of transmission within the home, serving as a bridge between wild and domestic cycle1616. Jansen AM, Xavier SCDC, Roque ALR. Landmarks of the Knowledge and Trypanosoma cruzi Biology in the Wild Environment. Front Cell Infect Microbiol. 2020;10(2):1-15. Available from: https://doi.org/10.3389/fcimb.2020.00010
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,2222. Garcia MN, O’Day S, Fisher-Hoch S, Gorchakov R, Patino R, Arroyo TPF, et al. One Health Interactions of Chagas Disease Vectors, Canid Hosts, and Human Residents along the Texas-Mexico Border. PLoS Negl Trop Dis 2016;10(11):1-0. Available from: https://doi.org/10.1371/journal.pntd.0005074
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, in addition to being susceptible to manifesting the disease1919. Gürtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE. Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 2007;134(1):69-82. Available from: https://doi.org/10.1017/S0031182006001259
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,2121. Kjos SA, Marcet PL, Yabsley MJ, Kitron U, Snowden KF, Logan KS, et al. Identification of bloodmeal sources and Trypanosoma cruzi infection in triatomine bugs (Hemiptera: Reduviidae) from residential settings in Texas, the United States. J Med Entomol 2013;50(5):1126-39. Available from: https://doi.org/10.1603/me12242
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,2323. Souza AI, Paulino-Junior D, Sousa MG, Camacho AA. Aspectos clínico-laboratoriais da infecção natural por Trypanosoma cruzi em cães de Mato Grosso do Sul. Cienc Rural 2008;38(5):1351-6. Available from: https://doi.org/10.1590/S0103-84782008000500024
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.

Among CD surveillance and control strategies, some entomological indicators stand out, such as the household infestation index, related to the index of household units with the occurrence of triatomines, and the natural infection index, associated with the percentage of triatomines positive for trypanosomatids2424. Organização Pan Americana de Saúde (OPAS). Guía para muestreo en actividades de vigilancia y control vectorial de la enfermedad de Chagas. Washington D.C.: OPAS; 2003. 46 p..

Pernambuco is at risk vector transmission of CD2525. Secretaria Estadual de Saúde de Pernambuco. Secretaria Executiva de Vigilância em Saúde. Plano Integrado de Ações para o Enfrentamento às Doenças Negligenciadas no Estado de Pernambuco/ SANAR - 2015 - 2018. Recife: Secretaria Estadual de Saúde - Série A. Normas e Manuais Técnicos; 2015. 46 p.. From 2012 to 2017, Petrolina was the municipality in the Sertão region of the São Francisco River that had the largest number of triatomines captured as well as the largest number of insects infected by T. cruzi2626. Coordenação Municipal de Controle da Doença de Chagas de Petrolina (CMCDCP). 2023. Relatório das ações do Programa Municipal de Doença de Chagas no ano de 2022.. The study of triatomine food sources can significantly support the knowledge about their natural hosts and their role in the transmission of T. cruzi, effectively contributing to the epidemiological surveillance of the disease. According to the Coordenação Municipal de Controle da Doença de Chagas de Petrolina, in the last 4 years, 39 cases of chronic CD have been diagnosed in the municipality of Petrolina due to vector transmission2626. Coordenação Municipal de Controle da Doença de Chagas de Petrolina (CMCDCP). 2023. Relatório das ações do Programa Municipal de Doença de Chagas no ano de 2022.. Therefore, this study aimed to understand the entomological indicators and identify the hosts that act as food sources for triatomines in the municipality of Petrolina, to contribute to CD surveillance and control actions in Pernambuco from the perspective of the One Health.

METHODS

● Study area

The municipality of Petrolina (9º 23' 55'' S, 40º 30' 3'' W) is in the morphoclimatic domain of the Caatingas2727. Base Nacional de Dados do Estado de Pernambuco (BDEPE). Posição geográfica das sedes dos municípios [Internet]. Recife: 2005 [updated 2005 Nov; cited 2023 Oct 01]. Available from: Available from: http://www.bde.pe.gov.br/visualizacao/Visualizacao_formato2.aspx?CodInformacao=280&Cod=1
http://www.bde.pe.gov.br/visualizacao/Vi...
, in the semi-arid region of Pernambuco, in the Sertão of São Francisco River region2828. Base Nacional de Dados do Estado de Pernambuco (BDEPE). Relação dos municípios, por Região de Desenvolvimento [Internet]. Recife: 2000 [updated 2000; cited 2023 Oct 01]. Available from: Available from: http://www.bde.pe.gov.br/visualizacao/Visualizacao_formato2.aspx?CodInformacao=798&Cod=1
http://www.bde.pe.gov.br/visualizacao/Vi...
,2929. Base Nacional de Dados do Estado de Pernambuco (BDEPE). Tipologia climática [Internet]. Recife: 2017 [updated 2017 Nov; cited 2023 Oct 01]. Available from: Available from: http://www.bde.pe.gov.br/visualizacao/Visualizacao_formato2.aspx?CodInformacao=633&Cod=1
http://www.bde.pe.gov.br/visualizacao/Vi...
(Figure 1). It has the third largest population in the state of Pernambuco: 386,786 inhabitants, with a demographic density of 84.79 inhabitants/km2, an area of 4,561.870 km2; 72.7% of households with adequate sanitation, 91.9% of urban homes on tree-lined public roads, and 8.7% of homes with adequate urbanization3030. Instituto Brasileiro de Geografia e Estatística (IBGE). Panorama: Petrolina [Internet]. Brasília: 2022 [updated 2022; cited 2023 Oct 01]. Available from: Available from: https://cidades.ibge.gov.br/brasil/pe/petrolina/panorama
https://cidades.ibge.gov.br/brasil/pe/pe...
. The average annual rainfall is 560 mm, temperature with average variations between 24 ºC and 28 ºC and average relative humidity between 66% and 72% in the wettest months3131. Sistema de Organização Nacional de Dados Ambientais (SONDA). Estação de Petrolina - Climatologia Local [Internet]. São José dos Campos: 2023 [cited 2023 Oct 01]. Available from: Available from: http://sonda.ccst.inpe.br/estacoes/petrolina_clima.html
http://sonda.ccst.inpe.br/estacoes/petro...
.

FIGURE 1:
Map of study area, Petrolina, Pernambuco state, Brazil.

● Ethical considerations, collection, and processing of triatomines

The insects were captured from January to December 2022, during entomological research carried out by health agent of the municipality, following the routine of the State Chagas Disease Surveillance and Control Program (PCDCh), in accordance with the “Manual of Surveillance, Prevention and Control of Zoonoses: technical and operational standards” of the Ministry of Health3232. Ministério da Saúde (MS). Secretaria de Vigilância em Saúde - Departamento de Vigilância das Doenças Transmissíveis. Manual de vigilância, prevenção e controle de zoonoses: normas técnicas e operacionais. Brasília: MS; 2016. 121 p. and the guidelines of Technical Note 36/2012 of July 25, 2012, of the Ministry of Health. This is the standard procedure used in entomological research to control CD in Pernambuco. Therefore, it was not necessary to submit this research to the Human Research Ethics Committee.

Insects were collected using entomological tweezers and flashlights to inspect crevices and places without lighting, and all rooms in the household units were inspected. Entomological research began in houses/intradomiciles (walls, furniture, and mattresses). Subsequently, inspections were conducted in the vicinity/peridomicile (grain and tool storage areas, chicken coops, animal pens, stone walls, fences, and rubble).

All the activities and pertinent data were recorded in a specific form and used for routine entomological research. The presence of a single triatomine specimen was sufficient for the household unit to be considered positive in entomological research, intra-domicile, and/or peridomicile. The triatomines were sent to the Regional Entomology Laboratory of VIII GERES and the Pernambuco Central Laboratory Dr. Milton Bezerra Sobral - LACEN/Central Laboratory of Endemics (LABEND) for taxonomic identification and parasitological research. Specimens with incomplete data on their origin, those without specific identification, and those without conditions for examination were excluded. The specimens were identified to the species level according to Galvão and Gurgel-Gonçalves1010. Silva TRM, Barros GMMR, Lima TARF, Giannelli A, Silva GM, Alves KML, et al. Spatial distribution of triatomine bugs in a Chagas disease endemic region in Brazil. Rev Soc Bras Med Trop 2019;52:1-5. Available from: https://doi.org/10.1590/0037-8682-0278-2019
https://doi.org/10.1590/0037-8682-0278-2...
, Lent and Wygodzinsky3333. Lent H, Wygodzinsky P. Revision of triatominae (Hemiptera, Reduviidae), and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist 1979;163(3):123-520., and Gurgel-Gonçalves et al.3434. Gurgel-Gonçalves RG, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Rev Panamazonica Saude 2010;1(4):57-4.. The identification of Triatoma brasiliensis nymphs was based on the following morphological characteristics: tibiae with a subapical ring, a pronotum design that looks like two question marks, and the dorsal surface of the abdomen without a defined design3535. Rocha DS, Santos CM. Morfologia dos ovos e ninfas. In: Galvão C, org. Vetores da doença de Chagas no Brasil [online]. Curitiba: Sociedade Brasileira de Zoologia, 2014, pp. 40-63. Zoologia: guias e manuais de identificação series. ISBN 978-85-98203-09-6. Available from SciELO Books (https://books.scielo.org/).
https://books.scielo.org/...
.

The household infestation index was calculated using the following formula2424. Organização Pan Americana de Saúde (OPAS). Guía para muestreo en actividades de vigilancia y control vectorial de la enfermedad de Chagas. Washington D.C.: OPAS; 2003. 46 p.: household infestation index = (total number of household units with triatomines/total number of household units surveyed) × 100.

For parasitological analyses using the conventional method in triatomines, fresh intestinal contents of the insects were examined by abdominal compression. All captured insects were examined and confirmed through visualization of the parasites by direct examination of triatomine feces and subsequent confirmation of the stained slides using GIEMSA3636. Medeiros CA, Silva MBA, Oliveira ALS, Alves SMM, Oliveira Júnior W, Medeiros ZM. Spatial analysis of the natural infection index for Triatomines and the risk of Chagas disease transmission in Northeastern Brazil. Rev Inst Med Trop São Paulo 2023;65(32):1-10. Available from: https://doi.org/10.1590/S1678-9946202365032
https://doi.org/10.1590/S1678-9946202365...
. The natural infection index was calculated using the following formula2424. Organização Pan Americana de Saúde (OPAS). Guía para muestreo en actividades de vigilancia y control vectorial de la enfermedad de Chagas. Washington D.C.: OPAS; 2003. 46 p.: natural infection index = (total number of infected triatomines/total number of insects examined) × 100.

● Identification of triatomine food sources

Not all captured triatomines were processed to identify the food sources. The best preserved triatomines infected with T. cruzi were used, from which intestinal contents were used for DNA extraction. Intestinal content samples were processed at the National and International Reference Laboratory for Triatomine Taxonomy of the Oswaldo Cruz Institute Foundation to identify food sources.

Genomic DNA was extracted using a DNeasy Blood & Tissue kit (Qiagen) following the manufacturer's protocol. DNA concentration was estimated using the Quantus TM Fluorometer (Promega). The PCR mix without DNA was used as a negative control, and triatomine specimens from the National and International Reference Laboratory for Triatomine Taxonomy Insectary (with controlled feeding) were used as positive controls.

To identify the food source, PCR was performed using the Platinum II Hot-Star Master Mix Kit (Thermo Fisher Scientific) and the 12S rDNA marker3737. Kitano T, Umetsu K, Tian W, Osawa M. Two universal primer sets for species identification among vertebrates. Int J Legal Med 2007;121(5):423-7. Available from: https://doi.org/10.1007/s00414-006-0113-y
https://doi.org/10.1007/s00414-006-0113-...
-3838. Stevens L, Dorn PL, Hobson J, de la Rua NM, Lucero DE, Klotz JH, et al. Vector blood meals and Chagas disease transmission potential, United States. Emerg Infect Dis 2012;18(4):646-9.. The PCR products were electrophoresed on an agarose gel (2%), stained with Gel Red (Biotium, Inc., California, USA), and observed under UV light. The amplicons were purified using EXOSAP (Affymetrix, USA).

DNA fragments were sequenced by Sanger sequencing. Sequences were visualized, edited, and aligned using Bioedit v. 7.0.5 (Department of Microbiology, North Carolina State University) and Lasergene SeqMan TM v. 7 (DNStar, Madison, Wisconsin, USA) and compared using Blast (Basic Local Alignment Search Tool) in the National Center for Biotechnology Information database (http://blast.ncbi.nim.nih.gov/Blast.cgi). Only sequences with a coverage above 95% were considered for species identification.

● Data analysis

Data were analyzed using descriptive statistics. The chi-square test (χ²) was used to analyze the number of triatomines captured at the intradomicile and peridomicile, and the G-test was used to compare triatomine species with the capture environment (intradomicile or peridomicile). Statistical significance was set at 5%. The BioEstat software version 5.3 was used.

RESULTS

According to secondary data provided by the Petrolina Municipal Health Department, 906 triatomines will be captured in the municipality in 2022. Triatoma brasiliensis accounted for 84.7% (767/906) of the total (419 nymphs and 348 adults), Triatoma spp. accounted for 8.2% (74/906 nymphs), and T. pseudomaculata 6.5% (59/906 adults). Rhodnius spp. constituted 0.4% (4/906 nymphs) of the total, R. nasutus represented 0.1% (1/906 adults), and T. sordida 0.1% (1/906 adults) (Table 1).

TABLE 1:
Triatomine species and natural infection index by Trypanosoma cruzi in the municipality of Petrolina, an endemic area of Chagas Disease in Brazilian semi-arid region.

Overall, 2,717 household units were visited, with a household infestation index of 11.04% (300/2717).

Of the 906 triatomines captured, 807 (89.1%) were captured in peridomicile and 99 (10.9%) in intradomicile (χ² = 313.39, df = 4, p = 1.40 E-66). The predominant species in the peridomicile area was T. brasiliensis (676), followed by Triatoma spp. (70), T. pseudomaculata (56), Rhodnius spp. (4), and R. nasutus (1). In the intradomicile period, this scenario was also repeated, with T. brasiliensis being the most frequent (91), followed by Triatoma spp. (4), T. pseudomaculata (3), and T. sordida (1) (G-test = 7.1319; p = 0.0283) (Table 1).

Of the 906 captured insects, 35 were infected, corresponding to a natural infection index of 3.8%. Regarding T. brasiliensis, 33 specimens were infected, with a natural infection index of 4.3%, whereas two specimens of T. pseudomaculata were infected, representing a natural infection index of 3.4%.

To identify food sources, 82 triatomine specimens were used: T. brasiliensis (72 specimens: 41 adults and 31 nymphs) and T. pseudomaculata (10 adult specimens). Regarding the location of capture, 60 (51 T. brasiliensis and nine T. pseudomaculata) were in the peridomicile (animal pens, chicken coops, stone walls, fences, and rubble) and 22 (21 T. brasiliensis and one T. pseudomaculata). Of the 82 triatomines analyzed, 11 were infected: nine with T. brasiliensis and two with T. pseudomaculata, which corresponded to a natural infection index of 13.4% (Table 1).

Of the 82 specimens, in five (one nymph and four adults), it was possible to identify the food source: human blood in T. pseudomaculata (two) and T. brasiliensis (one), dog blood in T. brasiliensis (one), and rodent (Mus musculus) blood in T. brasiliensis (one) (Table 2). All five specimens whose food sources were identified were infected. Of the three triatomines in which human blood was identified, two were intra-domicile and one was peridomicile, whereas the two triatomines infected with dog and rodent blood were captured in the peridomicile (Table 2).

TABLE 2:
Species of infected triatomines captured in the municipality of Petrolina, an endemic area of Chagas Disease in Brazilian semi-arid, according to the stage of development and identified food source.

DISCUSSION

According to Jansen et al.1616. Jansen AM, Xavier SCDC, Roque ALR. Landmarks of the Knowledge and Trypanosoma cruzi Biology in the Wild Environment. Front Cell Infect Microbiol. 2020;10(2):1-15. Available from: https://doi.org/10.3389/fcimb.2020.00010
https://doi.org/10.3389/fcimb.2020.00010...
, the assessment of infection risks for humans in each location must jointly consider the triatomine fauna, mammalian hosts, and reservoirs. In this regard, identification of the food sources of triatomines is an important contribution to the knowledge of their natural hosts and their respective roles in the transmission of T. cruzi, effectively contributing to the epidemiological surveillance of the disease, mainly using molecular techniques. This study is pioneering in Pernambuco in terms of the molecular identification of food sources for infected triatomines.

T. brasiliensis and T. pseudomaculata are triatomines adapted to the morphoclimatic domain of the Caatingas, and a semi-arid climate has been identified in previous studies conducted in Petrolina from 2012 to 20171313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
,3939. Silva MBA, Menezes KR, Siqueira AM, Balbino VQ, Lorosa ES, Farias MCG, et al. Importância da distribuição geográfica dos vetores da Doença de Chagas em Pernambuco, Brasil, em 2012. Rev Patol Trop 2015;44(2):195-06. Available from: https://doi.org/10.5216/rpt.v44i2.36650
https://doi.org/10.5216/rpt.v44i2.36650...
. Both are of epidemiological importance because of their high capacity to adapt to intradomicile, peridomicile, and wild environments, although T. brasiliensis has superior vector capacity and competence1111. Ministério da Saúde (MS). Secretaria de vigilância em Saúde. Boletim Epidemiológico - Doença de Chagas Aguda e distribuição espacial dos triatomíneos de importância epidemiológica, Brasil 2012 a 2016. Brasília:2019;50(2):1-10..

According to the Coordenação Municipal de Controle da Doença de Chagas de Petrolina2626. Coordenação Municipal de Controle da Doença de Chagas de Petrolina (CMCDCP). 2023. Relatório das ações do Programa Municipal de Doença de Chagas no ano de 2022., the household infestation index in the present study (11.04%) was higher than that in 2018 (5.5%). The increase in this rate may have occurred because of the suspension of visits by Endemic Disease Control Agents (ACE) during the COVID-19 pandemic. Therefore, spraying aimed at eliminating triatomines from the home environment was not performed in this study. Alpha-cypermethrin has been used in Pernambuco for two decades4040. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, et al. Synanthropic triatomines (Hemiptera, Reduviidae) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Rev Patol Trop 2012;45(1):60-5. Available from: https://doi.org/10.1590/S0037-86822012000100012
https://doi.org/10.1590/S0037-8682201200...
.

The household infestation index in Petrolina was higher than that of the entire state of Pernambuco in recent years: 2007 (9.45%), 2008 (8.9%), 2009 (8.8%), 2010 (9, 0%), 2011 (7.1%), 2012 (6.9%), 2013 (8.6%), 2014 (7.7%), 2015 (8.3%), 2016 (8.5%), 2017 (6.7%)4141. Secretaria Estadual de Saúde de Pernambuco. Secretaria Executiva de Vigilância em Saúde. Programa de Enfrentamento das Doenças Negligenciadas no Estado de Pernambuco SANAR - 2011 / 2014. Recife: Secretaria Estadual de Saúde - Série A. Normas e Manuais Técnicos; 2013. 39 p.-4242. Secretaria Estadual de Saúde de Pernambuco. Secretaria Executiva de Vigilância em Saúde. Plano de Ações para o enfrentamento às Doenças Negligenciadas. Recife: Secretaria Estadual de Saúde - Série A. Normais e manuais técnicos; 2019.48 p.. From 2011 onward, surveillance actions were implemented in the state through the Program to Combat Neglected Diseases (SANAR), which were directly reflected in the household infestation index. The state no longer had numbers higher than before the implementation of the SANAR, which established the goal of maintaining the household infestation index in municipalities below 10%4141. Secretaria Estadual de Saúde de Pernambuco. Secretaria Executiva de Vigilância em Saúde. Programa de Enfrentamento das Doenças Negligenciadas no Estado de Pernambuco SANAR - 2011 / 2014. Recife: Secretaria Estadual de Saúde - Série A. Normas e Manuais Técnicos; 2013. 39 p.-4242. Secretaria Estadual de Saúde de Pernambuco. Secretaria Executiva de Vigilância em Saúde. Plano de Ações para o enfrentamento às Doenças Negligenciadas. Recife: Secretaria Estadual de Saúde - Série A. Normais e manuais técnicos; 2019.48 p..

The natural infection index of Petrolina in the present study (3.8%) was higher than that in the period 2012-2017 (2.4%)1313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
. T. brasiliensis had a natural infection index (4.3%) higher than that in 2018 in the municipality (3.8%); in 2017, the natural infection index of T. brasiliensis was also lower (2%)1313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
, while in 2016, no infected triatomines were found in the municipality2323. Souza AI, Paulino-Junior D, Sousa MG, Camacho AA. Aspectos clínico-laboratoriais da infecção natural por Trypanosoma cruzi em cães de Mato Grosso do Sul. Cienc Rural 2008;38(5):1351-6. Available from: https://doi.org/10.1590/S0103-84782008000500024
https://doi.org/10.1590/S0103-8478200800...
. The natural infection rate of this species exhibited a potentially unstable pattern: 5.5% in 2012, 2.1% in 2013, 1.6% in 2014, and 6% in 20151313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
. No statistical tests were performed to validate the observed fluctuations.

The results of the present study are in line with those of other studies conducted in Pernambuco regarding the natural infection index of T. cruzi in T. brasiliensis: 6.5%4040. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, et al. Synanthropic triatomines (Hemiptera, Reduviidae) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Rev Patol Trop 2012;45(1):60-5. Available from: https://doi.org/10.1590/S0037-86822012000100012
https://doi.org/10.1590/S0037-8682201200...
, 19.2%3939. Silva MBA, Menezes KR, Siqueira AM, Balbino VQ, Lorosa ES, Farias MCG, et al. Importância da distribuição geográfica dos vetores da Doença de Chagas em Pernambuco, Brasil, em 2012. Rev Patol Trop 2015;44(2):195-06. Available from: https://doi.org/10.5216/rpt.v44i2.36650
https://doi.org/10.5216/rpt.v44i2.36650...
, 7.41%4343. Silva TRM, Rios TG, Ramos CAN, Scofield A, Lima TARF, Alves LC, et al. Molecular characterization of Trypanosoma cruzi DTUs of the triatomine species in a Chagas disease endemic area. J Parasit Dis 2022;46(1):64-1. Available from: https://doi.org/10.1007/s12639-021-01418-6
https://doi.org/10.1007/s12639-021-01418...
, 10.50%3636. Medeiros CA, Silva MBA, Oliveira ALS, Alves SMM, Oliveira Júnior W, Medeiros ZM. Spatial analysis of the natural infection index for Triatomines and the risk of Chagas disease transmission in Northeastern Brazil. Rev Inst Med Trop São Paulo 2023;65(32):1-10. Available from: https://doi.org/10.1590/S1678-9946202365032
https://doi.org/10.1590/S1678-9946202365...
, and 12,2%4444. Oliveira Neto JA, Anastácio DB, Silva TRM, Silva SS, Carvalho GA, Ramos RAN. Triatomine vectors of Trypanosoma cruzi in an endemic área for Chagas disease in Northeast Brazil. Rev Soc Bras Med Trop 2024;57:1-5. Available from: https://doi.org/10.1590/0037-8682-0413-2024
https://doi.org/10.1590/0037-8682-0413-2...
. In other studies, carried out in the northeastern region, T. brasiliensis was also found infected in Piauí (7.18%)3434. Gurgel-Gonçalves RG, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Rev Panamazonica Saude 2010;1(4):57-4. and in Rio Grande do Norte (1.2%)4545. Barreto AF, Cavalcanti MAF, Andrade CM, Nascimento EGC, Pereira WO. Indicadores entomológicos de triatomíneos no Estado do Rio Grande do Norte, Brasil. Cien Saude Colet 2019;24(4):1483-94. Available from: https://doi.org/10.1590/1413-81232018244.06062017
https://doi.org/10.1590/1413-81232018244...
(2.8%)4646. Sampaio GHF, Silva ANB, Negreiros CCA, Honorato NRM, Martins RR, Aguiar LMA et al. Temporal assessment of entomological surveillance of Trypanosoma cruzi vectors in an endemic area of northeastern Brazil. PLoS One 2023;18(6):1-14. Available from: https://doi.org/10.1371/journal.pone.0287260
https://doi.org/10.1371/journal.pone.028...
.

Triatoma pseudomaculata had a lower natural infection rate (3.4%) than in 2017 in the municipality (1.4%)1313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
. Notably, no infected specimens were observed between 2013 and 20161010. Silva TRM, Barros GMMR, Lima TARF, Giannelli A, Silva GM, Alves KML, et al. Spatial distribution of triatomine bugs in a Chagas disease endemic region in Brazil. Rev Soc Bras Med Trop 2019;52:1-5. Available from: https://doi.org/10.1590/0037-8682-0278-2019
https://doi.org/10.1590/0037-8682-0278-2...
. In 2012, the infection rate of natural T. pseudomaculata was 7.7%2626. Coordenação Municipal de Controle da Doença de Chagas de Petrolina (CMCDCP). 2023. Relatório das ações do Programa Municipal de Doença de Chagas no ano de 2022.. Similar to the present study, T. pseudomaculata presented with infection in other studies conducted in Pernambuco: 8%4040. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, et al. Synanthropic triatomines (Hemiptera, Reduviidae) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Rev Patol Trop 2012;45(1):60-5. Available from: https://doi.org/10.1590/S0037-86822012000100012
https://doi.org/10.1590/S0037-8682201200...
, 13.1%3939. Silva MBA, Menezes KR, Siqueira AM, Balbino VQ, Lorosa ES, Farias MCG, et al. Importância da distribuição geográfica dos vetores da Doença de Chagas em Pernambuco, Brasil, em 2012. Rev Patol Trop 2015;44(2):195-06. Available from: https://doi.org/10.5216/rpt.v44i2.36650
https://doi.org/10.5216/rpt.v44i2.36650...
, 8.70%3636. Medeiros CA, Silva MBA, Oliveira ALS, Alves SMM, Oliveira Júnior W, Medeiros ZM. Spatial analysis of the natural infection index for Triatomines and the risk of Chagas disease transmission in Northeastern Brazil. Rev Inst Med Trop São Paulo 2023;65(32):1-10. Available from: https://doi.org/10.1590/S1678-9946202365032
https://doi.org/10.1590/S1678-9946202365...
, and 12.90%4343. Silva TRM, Rios TG, Ramos CAN, Scofield A, Lima TARF, Alves LC, et al. Molecular characterization of Trypanosoma cruzi DTUs of the triatomine species in a Chagas disease endemic area. J Parasit Dis 2022;46(1):64-1. Available from: https://doi.org/10.1007/s12639-021-01418-6
https://doi.org/10.1007/s12639-021-01418...
. Research carried out in northeastern Brazil confirms T. cruzi infection in T. pseudomaculata: Piauí (2.28%)3434. Gurgel-Gonçalves RG, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Rev Panamazonica Saude 2010;1(4):57-4., Rio Grande do Norte (0.1%)4444. Oliveira Neto JA, Anastácio DB, Silva TRM, Silva SS, Carvalho GA, Ramos RAN. Triatomine vectors of Trypanosoma cruzi in an endemic área for Chagas disease in Northeast Brazil. Rev Soc Bras Med Trop 2024;57:1-5. Available from: https://doi.org/10.1590/0037-8682-0413-2024
https://doi.org/10.1590/0037-8682-0413-2...
and Bahia (4%)4747. Santos JSS, Pauda AD, Novais JMCB, Magalhães Junior JT, Carneiro IO, Santos F et al. Retrospective study of triatomines in an endemic region for Chagas disease in the state of Bahia, Brazil. Acta Vet Brasilica 2022;16(2):117-5. Available from: https://doi.org/10.21708/avb.2022.16.2.10473
https://doi.org/10.21708/avb.2022.16.2.1...
. Outside the northeastern region, infection was detected in T. pseudomaculata in Goiás in a study that did not record the infection rate4747. Santos JSS, Pauda AD, Novais JMCB, Magalhães Junior JT, Carneiro IO, Santos F et al. Retrospective study of triatomines in an endemic region for Chagas disease in the state of Bahia, Brazil. Acta Vet Brasilica 2022;16(2):117-5. Available from: https://doi.org/10.21708/avb.2022.16.2.10473
https://doi.org/10.21708/avb.2022.16.2.1...
.

In the present study, infection by T. cruzi was not detected in T. sordida, which was also recorded by Silva et al.1313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
not only in Petrolina, but also in all municipalities in the Sertão of the São Francisco River region from 2012 to 2017. Silva et al.4040. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, et al. Synanthropic triatomines (Hemiptera, Reduviidae) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Rev Patol Trop 2012;45(1):60-5. Available from: https://doi.org/10.1590/S0037-86822012000100012
https://doi.org/10.1590/S0037-8682201200...
, Silva et al.4343. Silva TRM, Rios TG, Ramos CAN, Scofield A, Lima TARF, Alves LC, et al. Molecular characterization of Trypanosoma cruzi DTUs of the triatomine species in a Chagas disease endemic area. J Parasit Dis 2022;46(1):64-1. Available from: https://doi.org/10.1007/s12639-021-01418-6
https://doi.org/10.1007/s12639-021-01418...
, and Medeiros et al.3636. Medeiros CA, Silva MBA, Oliveira ALS, Alves SMM, Oliveira Júnior W, Medeiros ZM. Spatial analysis of the natural infection index for Triatomines and the risk of Chagas disease transmission in Northeastern Brazil. Rev Inst Med Trop São Paulo 2023;65(32):1-10. Available from: https://doi.org/10.1590/S1678-9946202365032
https://doi.org/10.1590/S1678-9946202365...
also did not record infections in this species of triatomine in Pernambuco. In contrast, in Goiás4848. Oliveira AWS, Silva IG. Geographical distribution and indicators entomologic of sinantropic 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
https://doi.org/10.1590/s0037-8682200700...
, Paraná4949. Ferro e Silva AM, Sobral-Souza T, Vancine MH, Muylaert RL, Abreu AP, Pelloso SM, et al. Spatial prediction of risk areas for vector transmission of Trypanosoma cruzi in the State of Paraná, southern Brazil. PLoS Negl Trop Dis 2018;12(10):1-17. Available from: https://doi.org/10.1371/journal.pntd.0006907
https://doi.org/10.1371/journal.pntd.000...
, and Bahia4747. Santos JSS, Pauda AD, Novais JMCB, Magalhães Junior JT, Carneiro IO, Santos F et al. Retrospective study of triatomines in an endemic region for Chagas disease in the state of Bahia, Brazil. Acta Vet Brasilica 2022;16(2):117-5. Available from: https://doi.org/10.21708/avb.2022.16.2.10473
https://doi.org/10.21708/avb.2022.16.2.1...
T. cruzi infection was recorded in T. sordida.

Infection with R. nasutus was also not detected in the present study, which has also been reported in the state4040. Silva MBA, Barreto AVMS, Silva HA, Galvão C, Rocha D, Jurberg J, et al. Synanthropic triatomines (Hemiptera, Reduviidae) in the state of Pernambuco, Brazil: geographical distribution and natural Trypanosoma infection rates between 2006 and 2007. Rev Patol Trop 2012;45(1):60-5. Available from: https://doi.org/10.1590/S0037-86822012000100012
https://doi.org/10.1590/S0037-8682201200...
and Rio Grande do Norte4545. Barreto AF, Cavalcanti MAF, Andrade CM, Nascimento EGC, Pereira WO. Indicadores entomológicos de triatomíneos no Estado do Rio Grande do Norte, Brasil. Cien Saude Colet 2019;24(4):1483-94. Available from: https://doi.org/10.1590/1413-81232018244.06062017
https://doi.org/10.1590/1413-81232018244...
. This result differed from those obtained by Piauí3434. Gurgel-Gonçalves RG, Pereira FCA, Lima IP, Cavalcante RR. Distribuição geográfica, infestação domiciliar e infecção natural de triatomíneos (Hemiptera: Reduviidae) no Estado do Piauí, Brasil, 2008. Rev Panamazonica Saude 2010;1(4):57-4. and Pernambuco3636. Medeiros CA, Silva MBA, Oliveira ALS, Alves SMM, Oliveira Júnior W, Medeiros ZM. Spatial analysis of the natural infection index for Triatomines and the risk of Chagas disease transmission in Northeastern Brazil. Rev Inst Med Trop São Paulo 2023;65(32):1-10. Available from: https://doi.org/10.1590/S1678-9946202365032
https://doi.org/10.1590/S1678-9946202365...
.

The municipality of Petrolina demonstrates a certain seasonality of species, except T. brasiliensis and T. pseudomaculata, which were frequently recorded. From 2012 to 2017, T. sordida was recorded from 2013 to 20171313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
, while R. nasutus was recorded only in 20181313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
.

In the present study, it was possible to identify food sources for only 6% of the triatomines studied. One factor that may have prevented DNA amplification was the preservation of the captured material before DNA extraction. It is also important to consider that among the Brazilian morphoclimatic domains, the Caatinga has one of the highest temperatures, especially during the dry period, which accelerates the digestion of blood consumed by triatomines5050. Lilioso M, Reigada C, Pires-Silva D, Fontes FVHM, Limeira C, Monsalve-Lara J, et al. Dynamics of food sources, ecotypic distribution and Trypanosoma cruzi infection in Triatoma brasiliensis from the northeast of Brazil. PLoS Negl Trop Dis 2020;14(9):1-17. Available from: https://doi.org/10.1371/journal.pntd.0008735
https://doi.org/10.1371/journal.pntd.000...
.

In a study carried out in Pernambuco, using the precipitin technique, Silva et al.5151. Silva MBA, Menezes KR, Farias MCG, Andrade MS, Victor CCA, Lorosa ES, et al. Description of the feeding preferences of triatominae in the chagas disease surveillance study for the state of Pernambuco, Brazil (Hemiptera: Reduviidae). Rev Soc Bras Med Trop 2017;50(4):543-6. Available from: https://doi.org/10.1590/0037-8682-0334-2016
https://doi.org/10.1590/0037-8682-0334-2...
identified the eclectic eating behavior of T. brasiliensis and T. pseudomaculata when recording birds, rodents, dogs, opossums, lizards, cattle, goats, cockroaches, pigs, and humans as food sources. Using PCR, rodents from four families were identified as the most frequent food sources of T. brasiliensis in the municipality of Tauá, Ceará5252. Bezerra CM, Barbosa SE, Souza RCM, Barezani CP, Gürtler RE, Ramos Jr AN et al. Triatoma brasiliensis Neiva, 1911: Food sources and diversity of Trypanosoma cruzi in wild and artificial environments of the semiarid region of Ceará, northeastern Brazil. Parasit Vectors 2018;11(1):642. Available from: https://doi.org/10.1186/s13071-018-3235-4
https://doi.org/10.1186/s13071-018-3235-...
.

In the present study, T. brasiliensis and T. pseudomaculata were the most common triatomines, and hematophagy was observed in humans, dogs, and rodents. Similar PCR results were obtained in the states of Paraíba and Rio Grande do Norte5353. Honorato NRM, Silva ANB, Negreiros CCA, Aguiar LMA, Marliére NP, Souza RCM, et al. Triatomine and Trypanosoma cruzi discrete typing units distribution in a semi-arid area of northeastern Brazil. Acta Trop 2021;220(5). Available from: https://doi.org/10.1016/j.actatropica.2021.105950
https://doi.org/10.1016/j.actatropica.20...
. However, unlike the present study, in which human blood was the most frequent food source, dog blood was the main food source for triatomines, followed by humans and rodents such as Mus musculus5353. Honorato NRM, Silva ANB, Negreiros CCA, Aguiar LMA, Marliére NP, Souza RCM, et al. Triatomine and Trypanosoma cruzi discrete typing units distribution in a semi-arid area of northeastern Brazil. Acta Trop 2021;220(5). Available from: https://doi.org/10.1016/j.actatropica.2021.105950
https://doi.org/10.1016/j.actatropica.20...
.

Similar to other rodents1717. Bezerra CM, Cavalcanti LPG, Souza RCM, Barbosa SE, Xavier SCC, Jansen AM, et al. Domestic, Peridomestic and wild hosts in the transmission of Trypanosoma cruzi in the Caatinga area colonised by Triatoma brasiliensis. Mem Inst Oswaldo Cruz 2014;109(7):887-98. Available from: https://doi.org/10.1590/0074-0276140048
https://doi.org/10.1590/0074-0276140048...
, in the present study, the house mouse (M. musculus) was identified as a food source for T. brasiliensis, which was also reported by Honorato et al.5353. Honorato NRM, Silva ANB, Negreiros CCA, Aguiar LMA, Marliére NP, Souza RCM, et al. Triatomine and Trypanosoma cruzi discrete typing units distribution in a semi-arid area of northeastern Brazil. Acta Trop 2021;220(5). Available from: https://doi.org/10.1016/j.actatropica.2021.105950
https://doi.org/10.1016/j.actatropica.20...
using PCR. This rodent species, which was introduced in Brazil, may have a relevant epidemiological role, either as a host for triatomines or as a reservoir for T. cruzi. This rodent is generally associated with human habitation and is considered a generalist synanthropic species5454. Rozental T, Ferreira MS, Guterres A, Mares-Guia MA, Teixeira BR, Gonçalves J, et al. Zoonotic pathogens in Atlantic Forest wild rodents in Brazil: Bartonella and Coxiella infections. Acta Trop 2017;168:64-73. Available from: https://doi.org/10.1016/j.actatropica.2017.01.003
https://doi.org/10.1016/j.actatropica.20...
, presenting a cosmopolitan distribution and being responsible for most of the damage caused to the economy and public health5555. Guimarães AO, Valença FM, Sousa JBS, Souza SA, Madi RR, Melo CM. Parasitic and fungal infections in synanthropic rodents in an area of urban expansion, Aracaju, Sergipe State, Brazil. Acta Sci Biol Sci 2014;36(1):113-120. Available from: https://doi.org/10.4025/actascibiolsci.v36i1.19760
https://doi.org/10.4025/actascibiolsci.v...
. When these animals access their homes, infected triatomines can feed on them, facilitating the transmission of T. cruzi to both humans and domestic animals.

Similar to the results of the present study, Ribeiro et al.5656. Ribeiro Jr G, Santos CGS, Lanza F, Reis J, Vaccareza 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: https://doi.org/10.1186/s13071-019-3849-1
https://doi.org/10.1186/s13071-019-3849-...
used PCR to identify human and dog blood in T. brasiliensis and T. pseudomaculata in the dog blood in Bahia. Similar to the present study, the vast majority of triatomines have been captured in an intradomicile environment.

The detection of human blood as a food source in triatomines of T. brasiliensis and T. pseudomaculata captured intradomiciles is of epidemiological importance. It is important to highlight that T. brasiliensis is more anthropophilic than T. pseudomaculata77. Silva MBA, Rocha DS, Borba RFB. Triatomíneos Sinantrópicos de Pernambuco: Biogeografia, técnicas laboratoriais e controle da qualidade. Recife: EDUPE; 2019. 170 p..

Pernambuco State is at risk for vector transmission of CD, and Petrolina was the municipality in the Sertão of the São Francisco River that, from 2012 to 2017, had the largest number of triatomines captured, as well as the largest quantity of infected insects1313. Silva LRS, Silva MBA, Oliveira GMA, Medeiros CA, Oliveira JB. Vigilância entomológica dos vetores da doença de Chagas nos municípios da VIII Gerência Regional de Saúde do estado de Pernambuco, Brasil, de 2012 a 2017. Rev Panamazonica Saude 2021;12:1-9. Available from: https://doi.org/10.5123/S2176-6223202100858
https://doi.org/10.5123/S2176-6223202100...
. According to the Coordenação Municipal de Controle da Doença de Chagas de Petrolina2626. Coordenação Municipal de Controle da Doença de Chagas de Petrolina (CMCDCP). 2023. Relatório das ações do Programa Municipal de Doença de Chagas no ano de 2022., 39 cases of chronic CD. All cases were related to vector transmission.

The presence of nymphs of T. brasiliensis and Triatoma spp. in the intra-domicile region is traditionally used as a parameter for vector control. This is a sign of adaptation of the species to the artificial ecotope, as nymphs do not have wings4545. Barreto AF, Cavalcanti MAF, Andrade CM, Nascimento EGC, Pereira WO. Indicadores entomológicos de triatomíneos no Estado do Rio Grande do Norte, Brasil. Cien Saude Colet 2019;24(4):1483-94. Available from: https://doi.org/10.1590/1413-81232018244.06062017
https://doi.org/10.1590/1413-81232018244...
,5757. Valença-Barbosa C, Fernandes FA, Santos HLC, Sarquis O, Harry M, Almeida CE, et al. Molecular identification of food sources in triatomines in the brazilian northeast: Roles of goats and rodents in Chagas disease epidemiology. Am J Trop Med Hyg 2015;93(5):994-7. Available from: https://doi.org/10.4269/ajtmh.15-0156
https://doi.org/10.4269/ajtmh.15-0156...
.

The majority of insects were captured in the peridomicile because of the presence of domestic animals such as dogs, cats, pigs, sheep, cattle, horses, goats, and birds, as well as synanthropic animals such as rodents1717. Bezerra CM, Cavalcanti LPG, Souza RCM, Barbosa SE, Xavier SCC, Jansen AM, et al. Domestic, Peridomestic and wild hosts in the transmission of Trypanosoma cruzi in the Caatinga area colonised by Triatoma brasiliensis. Mem Inst Oswaldo Cruz 2014;109(7):887-98. Available from: https://doi.org/10.1590/0074-0276140048
https://doi.org/10.1590/0074-0276140048...
-1818. Jansen AM, Xavier SCDC, Roque ALR. Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil. Parasit Vectors 2018;11(9):502. Available from: https://doi.org/10.1186/s13071-018-3067-2
https://doi.org/10.1186/s13071-018-3067-...
. The peridomicile is considered a link between wild and domestic cycles1515. Zetun CB, Lucheis SB, Troncarelli MZ, Langoni H. Infecção por Trypanosoma cruzi em animais silvestres procedentes de zoológicos do estado de São Paulo. Vet Zootec 2014;21(1):139-47.,5252. Bezerra CM, Barbosa SE, Souza RCM, Barezani CP, Gürtler RE, Ramos Jr AN et al. Triatoma brasiliensis Neiva, 1911: Food sources and diversity of Trypanosoma cruzi in wild and artificial environments of the semiarid region of Ceará, northeastern Brazil. Parasit Vectors 2018;11(1):642. Available from: https://doi.org/10.1186/s13071-018-3235-4
https://doi.org/10.1186/s13071-018-3235-...
,5757. Valença-Barbosa C, Fernandes FA, Santos HLC, Sarquis O, Harry M, Almeida CE, et al. Molecular identification of food sources in triatomines in the brazilian northeast: Roles of goats and rodents in Chagas disease epidemiology. Am J Trop Med Hyg 2015;93(5):994-7. Available from: https://doi.org/10.4269/ajtmh.15-0156
https://doi.org/10.4269/ajtmh.15-0156...
, in which dogs play a prominent role1515. Zetun CB, Lucheis SB, Troncarelli MZ, Langoni H. Infecção por Trypanosoma cruzi em animais silvestres procedentes de zoológicos do estado de São Paulo. Vet Zootec 2014;21(1):139-47.-1616. Jansen AM, Xavier SCDC, Roque ALR. Landmarks of the Knowledge and Trypanosoma cruzi Biology in the Wild Environment. Front Cell Infect Microbiol. 2020;10(2):1-15. Available from: https://doi.org/10.3389/fcimb.2020.00010
https://doi.org/10.3389/fcimb.2020.00010...
. Dogs can act as sentinels to identify areas at risk of CD emergence, in addition to being susceptible to manifesting the disease1919. Gürtler RE, Cecere MC, Lauricella MA, Cardinal MV, Kitron U, Cohen JE. Domestic dogs and cats as sources of Trypanosoma cruzi infection in rural northwestern Argentina. Parasitology 2007;134(1):69-82. Available from: https://doi.org/10.1017/S0031182006001259
https://doi.org/10.1017/S003118200600125...

20. Roque ALR, Jansen AM. Importância dos animais domésticos sentinelas na identificação de áreas de risco de emergência de doença de Chagas. Rev Soc Bras Med Trop 2008;41(3):191-3.
-2121. Kjos SA, Marcet PL, Yabsley MJ, Kitron U, Snowden KF, Logan KS, et al. Identification of bloodmeal sources and Trypanosoma cruzi infection in triatomine bugs (Hemiptera: Reduviidae) from residential settings in Texas, the United States. J Med Entomol 2013;50(5):1126-39. Available from: https://doi.org/10.1603/me12242
https://doi.org/10.1603/me12242...
,2323. Souza AI, Paulino-Junior D, Sousa MG, Camacho AA. Aspectos clínico-laboratoriais da infecção natural por Trypanosoma cruzi em cães de Mato Grosso do Sul. Cienc Rural 2008;38(5):1351-6. Available from: https://doi.org/10.1590/S0103-84782008000500024
https://doi.org/10.1590/S0103-8478200800...
. Studies conducted in dogs have demonstrated a high seroprevalence of anti-T. cruzi, which demonstrates the exposure of these animals to the protozoan and confirms their status as sentinel host2020. Roque ALR, Jansen AM. Importância dos animais domésticos sentinelas na identificação de áreas de risco de emergência de doença de Chagas. Rev Soc Bras Med Trop 2008;41(3):191-3.,5858. Dario MA, Furtado C, Lisboa CV, Oliveira F, Santos FM, D’Andrea PS, et al. Trypanosomatid Richness Among Rats, Opossums, and Dogs in the Caatinga Biome, Northeast Brazil, a Former Endemic Area of Chagas Disease. Front Cell Infect Microbiol 2022;12(85):1903. Available from: https://doi.org/10.3389/fcimb.2022.851903
https://doi.org/10.3389/fcimb.2022.85190...
. Furthermore, compared to humans, dogs are more susceptible as hosts of triatomines and are consequently infected with T. cruzi5959. Travi BL. Considering Dogs as Complementary Targets of Chagas Disease Control. Vector Borne Zoonotic Dis 2019;19(2):90-4. Available from: https://doi.org/10.1089/vbz.2018.2325
https://doi.org/10.1089/vbz.2018.2325...
.

In Pernambuco and other states where CD is endemic, the role of dogs as hosts of T. cruzi and other animals susceptible to the disease must be investigated. In the present study, the detection of human, dog, and rodent blood in triatomines demonstrates the risk of vector transmission of T. cruzi in the studied region.

T. brasiliensis occurs exclusively in Brazil1818. Jansen AM, Xavier SCDC, Roque ALR. Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil. Parasit Vectors 2018;11(9):502. Available from: https://doi.org/10.1186/s13071-018-3067-2
https://doi.org/10.1186/s13071-018-3067-...
and is considered the most important vector in the northeastern region77. Silva MBA, Rocha DS, Borba RFB. Triatomíneos Sinantrópicos de Pernambuco: Biogeografia, técnicas laboratoriais e controle da qualidade. Recife: EDUPE; 2019. 170 p. because it presents some epidemiologically important characteristics, such as being the most frequent species, having a wider geographic distribution5151. Silva MBA, Menezes KR, Farias MCG, Andrade MS, Victor CCA, Lorosa ES, et al. Description of the feeding preferences of triatominae in the chagas disease surveillance study for the state of Pernambuco, Brazil (Hemiptera: Reduviidae). Rev Soc Bras Med Trop 2017;50(4):543-6. Available from: https://doi.org/10.1590/0037-8682-0334-2016
https://doi.org/10.1590/0037-8682-0334-2...
, a higher rate of natural infection by T. cruzi and a higher level of anthropophilia77. Silva MBA, Rocha DS, Borba RFB. Triatomíneos Sinantrópicos de Pernambuco: Biogeografia, técnicas laboratoriais e controle da qualidade. Recife: EDUPE; 2019. 170 p.. T. pseudomaculata stands out as the second most important species in the transmission of T. cruzi77. Silva MBA, Rocha DS, Borba RFB. Triatomíneos Sinantrópicos de Pernambuco: Biogeografia, técnicas laboratoriais e controle da qualidade. Recife: EDUPE; 2019. 170 p.,4343. Silva TRM, Rios TG, Ramos CAN, Scofield A, Lima TARF, Alves LC, et al. Molecular characterization of Trypanosoma cruzi DTUs of the triatomine species in a Chagas disease endemic area. J Parasit Dis 2022;46(1):64-1. Available from: https://doi.org/10.1007/s12639-021-01418-6
https://doi.org/10.1007/s12639-021-01418...
, as it is found both indoors and outdoors, in domestic animal breeding facilities, and in fences made of dry twigs associated with Cereus jamacaru (Mandacaru), in addition to wild environments, such as marsupial and rodent burrows88. Galvão C, Gurgel-Gonçalves RG. Vetores conhecidos no Brasil. In: Galvão C, editor. Vetores da doença de chagas no Brasil. Curitiba: Sociedade Brasileira de Zoologia - Série Zoologia: guias e manuais de identificação; 2014. p. 88-70.-99. Jurberg J, Rodrigues JMS, Moreira FFF, Dale C, Cordeiro IRS, Lamas Jr VD, et al. Atlas Iconográfico dos Triatomíneos do Brasil (Vetores da Doença de Chagas). Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos. Rio de Janeiro: Instituto Oswaldo Cruz; 2014. 52 p..

According to Jansen et al.1616. Jansen AM, Xavier SCDC, Roque ALR. Landmarks of the Knowledge and Trypanosoma cruzi Biology in the Wild Environment. Front Cell Infect Microbiol. 2020;10(2):1-15. Available from: https://doi.org/10.3389/fcimb.2020.00010
https://doi.org/10.3389/fcimb.2020.00010...
, “due to the multiplicity of T. cruzi vectors and hosts, CD should not be seen solely as a human parasitic disease”. Therefore, for the effective control of this neglected tropical disease, multi-professional, transdisciplinary, and intersectoral actions are necessary, as recommended by the One Health approach, as this disease is associated with ecological aspects inherent to the human-animal-vector-ecosystem interaction1616. Jansen AM, Xavier SCDC, Roque ALR. Landmarks of the Knowledge and Trypanosoma cruzi Biology in the Wild Environment. Front Cell Infect Microbiol. 2020;10(2):1-15. Available from: https://doi.org/10.3389/fcimb.2020.00010
https://doi.org/10.3389/fcimb.2020.00010...
,6060. Austen JM, Barbosa AD. Diversity and epidemiology of bat Trypanosomes: a One Health perspective. Pathogens 2021;10(9):1148. Available from: https://doi.org/10.3390/pathogens10091148
https://doi.org/10.3390/pathogens1009114...
.

These results reinforce the need to intensify CD diagnosis, surveillance, and control actions in Petrolina, as an increase in entomological indices was recorded in addition to the detection of the blood of humans and domestic and synanthropic animals as a food source for infected triatomines, suggesting the risk of vector transmission of CD in the municipality. Multidisciplinary and intersectoral actions must be performed in the context of the One Health approach.

ACKNOWLEDGMENTS

We thank the team of the Municipal Health Department of Petrolina, Regional Entomology Laboratory of VIII GERES, Central Laboratory of Pernambuco (LACEN).

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  • Financial Support: This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Publication Dates

  • Publication in this collection
    16 Aug 2024
  • Date of issue
    2024

History

  • Received
    04 Dec 2023
  • Accepted
    28 June 2024
Sociedade Brasileira de Medicina Tropical - SBMT Sociedade Brasileira de Medicina Tropical - SBMT, Núcleo de Medicina Tropical – UnB, Sala 43C – 70904-970, E-mails: rsbmt@uftm.edu.br | artes.rsbmt@gmail.com | sbmt@sbmt.org.br , WhatsApp: SBMT (61) 9.9192-6496, WhatsApp: RSBMT (34) 9.9996-5807 - Brasília - DF - Brazil
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