Investigation regarding the presence of Trypanosoma cruzi in triatomines and humans in rural households in the State of Paraná, southern Brazil
DOI:
https://doi.org/10.33448/rsd-v10i10.18366Keywords:
Chagas disease; Epidemiological surveillance; Southern Brazil.Abstract
Trypanosoma cruzi, the etiologic agent of Chagas disease (CD), is transmitted by hematophagous insects belonging to the subfamily Triatominae. After elimination of Triatoma infestans, the infestation of human dwellings by secondary species of vectors continues to pose a risk of transmission of the parasite. Our aim was to investigate the T. cruzi presence in triatomines and humans in rural households in the State of Paraná, southern Brazil. The capture of the insects was carried out by technicians of the municipalities after residents reported the outbreak. Five residents and 27 triatomines captured in four municipalities in the North and Midwest of the state were evaluated. The research of T. cruzi was carried out using parasitological, serological, and molecular techniques, in human blood, excreta, intestinal contents and insect macerate. Panstrongylus megistus, P. geniculatus and Triatoma sp. were identified. Ten specimens of P. megistus were captured in a house in Mandaguari with five residents and presented an infection rate of 70% for T. cruzi like. All residents tested negative for T. cruzi infection. Another 15 P. megistus were captured in the peridomicile in Janiópolis and had 100.0% positivity. The only adult specimen of P. geniculatus captured in the intradomicile in Amaporã, as well as the nymph of Triatoma in the peridomicile in Paiçandu, were negative. The finding of P. megistus naturally infected by T. cruzi in households in rural area of Paraná demonstrates a potential risk of vector transmission of CD in these regions.
References
Abolis, N. G., Araújo, S. M. de, Toledo, M. J. de O., Fernandez, M. A., & Gomes, M. L. (2011). Trypanosoma cruzi I-III in southern Brazil causing individual and mixed infections in humans, sylvatic reservoirs and triatomines. Acta Tropica, 120(3), 167–172. https://doi.org/10.1016/j.actatropica.2011.08.001
Barbosa, G. L., Silva, R. A. Da, Rodrigues, V. L. C. C., Marli, D., & Wanderley, V. (2012). Busca ativa de triatomíneos em área com ausência de notificações como subsídio à estratégia de vigilância entomológica no Estado de São Paulo. Bepa, 9(102), 4–12.
Bisugo, M. da C., Araújo, M. de F. L. de, Nunes, E. V., Cunha, E. A., Junior, O. da C. O., Guilherme, C. do S., Ramirez, L. P., & Tolezano, J. E. (1998). Isolamento de Trypanosoma cruzi por xenocultura após aplicaçäo de xenodiagnóstico In vivo e/ou In vitro em pacientes na fase crônica da doença de Chagas e na co-infecçäo pelo HIV. Revista Do Instituto Adolfo Lutz, 57(2), 89–96.
Brasil, M. da S. (2013). Recomendações sobre o diagnóstico parasitológico, sorológico e molecular para confirmação da doença de Chagas aguda e crônica. Revista de Patologia Tropical, 42(4), 475–478.
Brasil, M. da S. (2017). Guia de vigilância em saúde. Secretaria de Vigilância Em Saúde Coordenação-Geral de Desenvolvimento Da Epidemiologia Em Serviços. https://portalarquivos.saude.gov.br/images/pdf/2017/outubro/06/Volume-Unico-2017.pdf
Brener, Z. (1962). Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi. Revista Do Instituto de Medicina Tropical de Sao Paulo, 4, 389–396. http://www.ncbi.nlm.nih.gov/pubmed/14015230
Bronfen, E., Rocha, F. S. de A., Machado, G. B. N., Perillo, M. M., Romanha, A. J., & Chiari, E. (1989). Isolamento de amostras do Trypanosoma cruzi por xenodiagnóstico e hemocultura de pacientes na fase crônica da doença de Chagas. Memórias Do Instituto Oswaldo Cruz, 84(2), 237–240. https://doi.org/10.1590/S0074-02761989000200012
Caldas, S., Caldas, I. S., Diniz, L. de F., Lima, W. G. de, Oliveira, R. de P., Cecílio, A. B., Ribeiro, I., Talvani, A., & Bahia, M. T. (2012). Real-time PCR strategy for parasite quantification in blood and tissue samples of experimental Trypanosoma cruzi infection. Acta Tropica, 123(3), 170–177. https://doi.org/10.1016/j.actatropica.2012.05.002
Candido, A. S., Arrais, F. M. de A., Pinto, L. C., Viana, M. W. C., Goes, M. I. L., & Ferreira, R. J. (2019). Ocorrência de triatomíneos em ambientes intra e peridomiciliares do Município de Campos Sales, Ceará. Biota Amazônia (Biote Amazonie, Biota Amazonia, Amazonian Biota), 9(1), 1–4.
Chagas, C. (1909). Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Memórias Do Instituto Oswaldo Cruz, 1(2), 159–218. https://doi.org/10.1590/S0074-02761909000200008
Chiari, E., Pinto Dias, J. C., Lana, M., & Andrade Chiari, C. (1989). Hemocultures for the parasitological diagnosis of human chronic Chagas’ disease. Revista Da Sociedade Brasileira de Medicina Tropical, 22(1), 19–23. https://doi.org/10.1590/S0037-86821989000100004
Cominetti, M. C., Almeida, R. F. C. de, Goncalves, G. M. do A., & Andreotti, R. (2013). Monitoring Trypanosoma cruzi infection in triatomines using PCR in Mato Grosso do Sul, Brazil. Revista Da Sociedade Brasileira de Medicina Tropical, 46(3), 277–280. https://doi.org/10.1590/0037-8682-0024-2013
Cordero-Montoya, G., Flores-Villegas, A. L., Salazar-Schettino, P. M., Vences-Blanco, M. O., Rocha-Ortega, M., Gutiérrez-Cabrera, A. E., Rojas-Ortega, E., & Córdoba-Aguilar, A. (2019). The cost of being a killer’s accomplice: Trypanosoma cruzi impairs the fitness of kissing bugs. Parasitology Research, 118(9), 2523–2529. https://doi.org/10.1007/s00436-019-06413-8
Coura, J. R., & Borges-Pereira, J. (2012). Chagas disease: What is known and what should be improved: a systemic review. Revista Da Sociedade Brasileira de Medicina Tropical, 45(3), 286–296. https://doi.org/10.1590/S0037-86822012000300002
Coura, J. R., & Dias, J. C. P. (2009). Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Memórias Do Instituto Oswaldo Cruz, 104(suppl 1), 31–40. https://doi.org/10.1590/S0074-02762009000900006
Cummings, K. L., & Tarleton, R. L. (2003). Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Molecular and Biochemical Parasitology, 129(1), 53–59. https://doi.org/10.1016/S0166-6851(03)00093-8
De Sá, Amanda Regina Nichi, Steindel, M., Demeu, L. M. K., Lückemeyer, D. D., Grisard, E. C., Neto, Q. A. D. L., De Araújo, S. M., Toledo, M. J. D. O., & Gomes, M. L. (2013). Cytochrome oxidase subunit 2 gene allows simultaneous detection and typing of Trypanosoma rangeli and Trypanosoma cruzi. Parasites and Vectors, 6(1), 1–9. https://doi.org/10.1186/1756-3305-6-363
Dias, J. C. P. (2007). Southern Cone Initiative for the elimination of domestic populations of Triatoma infestans and the interruption of transfusion Chagas disease: historical aspects, present situation, and perspectives. Memórias Do Instituto Oswaldo Cruz, 102(suppl 1), 11–18. https://doi.org/10.1590/S0074-02762007005000092
Dias, J. C. P., Ramos, A. N., Gontijo, E. D., Alejandro, L., Shikanai-Yasuda, M. A., Coura, J. R., Rosália Morais Torres, Melo, J. R. da C., Almeida, E. A. de, Jr, W. de O., Silveira, A. C., Rezende, J. M. de, Pinto, F. S., Ferreira, A. W., Rassi, A., Fragata Filho, A. A., Sousa, A. S. de, Correia Filho, D., Jansen, A. M., … Alves, R. V. (2016). II Consenso Brasileiro em Doença de Chagas, 2015. Epidemiologia e Serviços de Saúde, 25(21), 1–10. https://doi.org/10.5123/S1679-49742016000500002
Duffy, T., Cura, C. I., Ramirez, J. C., Abate, T., Cayo, N. M., & Parrado, R. (2013). Analytical performance of a multiplex Real-Time PCR assay using TaqMan probes for quantification of Trypanosoma cruzi satellite DNA in blood samples. PLoS Negl Trop Dis, 7. https://doi.org/10.1371/journal.pntd.0002000
Farias, A. D. S. C. de, Alves, Z. F., Silva, M. B. A., Coutinho, C. B. D., & Rocha, D. da S. (2019). Pesquisa entomológica das espécies de triatomíneos encontradas na zona rural do município de Caruaru, estado de Pernambuco, Brasil, de 2011 a 2012. Revista Pan-Amazônica de Saúde, 10(0), 1–6. https://doi.org/10.5123/S2176-6223201901593
Ferro e Silva, A. M., Sobral-Souza, T., Vancine, M. H., Muylaert, R. L., de Abreu, A. P., Pelloso, S. M., de Barros Carvalho, M. D., de Andrade, L., Ribeiro, M. C., & Toledo, M. J. de O. (2018). Spatial prediction of risk areas for vector transmission of Trypanosoma cruzi in the State of Paraná, southern Brazil. PLoS Neglected Tropical Diseases, 12(10), 1–17. https://doi.org/10.1371/journal.pntd.0006907
Filardi, L. S., & Brener, Z. (1987). Susceptibility and natural resistance of Trypanosoma cruzi strains to drugs used clinically in Chagas disease. Transactions of the Royal Society of Tropical Medicine and Hygiene, 81(5), 755–759. https://doi.org/10.1016/0035-9203(87)90020-4
Galvão, C., & Dale, C. (2014). Chaves de identificação para adultos. In Vetores da doença de Chagas no Brasil. https://doi.org/10.7476/9788598203096.0009
Gasparim, A. Z., Fontes, C. E. R., Rossoni, D. F., & Toledo, M. J. de O. (2018). Epidemiological and clinical profile of patients with chagas disease in the central-north area of Paraná, Southern Brazil. Revista Da Sociedade Brasileira de Medicina Tropical, 51(2), 225–230. https://doi.org/10.1590/0037-8682-0173-2017
Gomes, M L, Galvao, L. M., Macedo, A. M., Pena, S. D., & Chiari, E. (1999). Chagas’ disease diagnosis: comparative analysis of parasitologic, molecular, and serologic methods. The American Journal of Tropical Medicine and Hygiene, 60(2), 205–210. https://doi.org/10.4269/ajtmh.1999.60.205
Gomes, Mônica L., Macedo, A. M., Vago, A. R., Pena, S. D. J., Galvão, L. M. C., & Chiari, E. (1998). Trypanosoma cruzi:Optimization of Polymerase Chain Reaction for Detection in Human Blood. Experimental Parasitology, 88(1), 28–33. https://doi.org/10.1006/expr.1998.4191
IBGE — Instituto Brasileiro de Geografia e Estatística. (2017). História do Município de Janiopólis, Paraná, Brasil. https://cidades.ibge.gov.br/brasil/pr/janiopolis/historico
IBGE — Instituto Brasileiro de Geografia e Estatística. (2019). Censo demográfico do Paraná 2010.
Junqueira, A. C. V., Degrave, W., & Brandão, A. (2005). Minicircle organization and diversity in Trypanosoma cruzi populations. Trends in Parasitology, 21(6), 270–272. https://doi.org/10.1016/j.pt.2005.04.001
Jurberg, J., Rodrigues, J. M. S., Moreira, F. F. F., Dale, C., Cordeiro, I. R. S., Lamas Jr, V. D., Galvão, C., & Rocha, D. da S. (2014). Atlas Iconográfico dos Triatomíneos do Brasil (Vetores da Doença de Chagas). 58.
Justi, S. A., & Galvão, C. (2017). The Evolutionary Origin of Diversity in Chagas Disease Vectors. Trends in Parasitology, 33(1), 42–52. https://doi.org/10.1016/j.pt.2016.11.002
Léo Ramos Chaves. (2019). Focos de barbeiro na cidade de São Paulo. https://revistapesquisa.fapesp.br/focos-de-barbeiro-na-cidade-de-sao-paulo/
Macedo, A. M., Martins, M. S., Chiari, E., & Pena, S. D. J. (1992). DNA fingerprinting of Trypanosoma cruzi: A new tool for characterization of strains and clones. Molecular and Biochemical Parasitology, 55(1–2), 147–153. https://doi.org/10.1016/0166-6851(92)90135-7
Mendes-Sousa, A. F., Filho, E. de A. R., Macêdo, M. A., & Barros, V. C. (2019). Anti-complement activity in salivary glands and midgut of chagas disease vector, Panstrongylus megistus (Hemiptera, triatominae). Revista Do Instituto de Medicina Tropical de Sao Paulo, 61, 1–7. https://doi.org/10.1590/s1678-9946201961038
Ministério da Saúde. (2019). Doença de Chagas Aguda e distribuição espacial dos triatomíneos de importância epidemiológica, Brasil 2012 a 2016. Ministério Da Saúde. Boletim Epidemiológico, 50, 10. http://portalarquivos2.saude.gov.br/images/pdf/2019/janeiro/23/2018-025.pdf
Miyamoto, C. T., Gomes, M. L., Marangon, A. V., Araújo, S. M., Bahia, M. T., Lana, M., & Toledo, M. J. O. (2006). Trypanosoma cruzi: Sensitivity of the polymerase chain reaction for detecting the parasite in the blood of mice infected with different clonal genotypes. Experimental Parasitology, 112(3), 198–201. https://doi.org/10.1016/j.exppara.2005.10.006
Nascimento, J. D., da Rosa, J. A., Salgado-Roa, F. C., Hernández, C., Pardo-Diaz, C., Alevi, K. C. C., Ravazi, A., de Oliveira, J., de Azeredo Oliveira, M. T. V., Salazar, C., & Ramírez, J. D. (2019). Taxonomical over splitting in the Rhodnius prolixus (Insecta: Hemiptera: Reduviidae) clade: Are R. taquarussuensis (da Rosa et al., 2017) and R. neglectus (Lent, 1954) the same species? PLOS ONE, 14(2), e0211285. https://doi.org/10.1371/journal.pone.0211285
Peixoto, S. R., Rocha, D. da S., Dale, C., & Galvão, C. (2020). Panstrongylus geniculatus (Latreille, 1811) (Hemiptera, Reduviidae, Triatominae): First record on Ilha Grande, Rio de Janeiro, Brazil. Check List, 16(2), 391–394. https://doi.org/10.15560/16.2.391
Rassi, A., & Junior, A. (2013). Doença de Chagas aguda. In Programa de Atualização em Medicina de Urgência e Emergência (PROURGEM) (pp. 41–85). https://www.researchgate.net/publication/269985225_Doenca_de_Chagas_aguda
Ravazi, A., Alevi, K. C. C., Oliveira, J., Rosa, J. A., & Azeredo-Oliveira, M. T. V. (2017). Cytogenetic analysis in different populations of Rhodnius prolixus and R. nasutus from different countries of South America. Brazilian Journal of Biology, 78(1), 183–185. https://doi.org/10.1590/1519-6984.167196
Sá, Amanda R.N., Dias, G. B. M., Kimoto, K. Y., Steindel, M., Grisard, E. C., Toledo, M. J. O., & Gomes, M. L. (2016). Genotyping of Trypanosoma cruzi DTUs and Trypanosoma rangeli genetic groups in experimentally infected Rhodnius prolixus by PCR-RFLP. Acta Tropica, 156, 115–121. https://doi.org/10.1016/j.actatropica.2016.01.006
Silveira, A. C., & Dias, J. C. P. (2011). O controle da transmissão vetorial. Revista Da Sociedade Brasileira de Medicina Tropical, 44(suppl 2), 52–63. https://doi.org/10.1590/S0037-86822011000800009
Souto, R. P., Fernandes, O., Macedo, A. M., Campbell, D. A., & Zingales, B. (1996). DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Molecular and Biochemical Parasitology, 83(2), 141–152. https://doi.org/10.1016/S0166-6851(96)02755-7
Souza, E. dos S., Von Atzingen, N. C. B., Furtado, M. B., De Oliveira, J., Nascimento, J. D., Vendrami, D. P., Gardim, S., & Rosa, J. A. Da. (2016). Description of Rhodnius marabaensis sp. N. (Hemiptera, Reduviidade, Triatominae) from Pará State, Brazil. ZooKeys, 2016(621), 45–62. https://doi.org/10.3897/zookeys.621.9662
Sperandio da Silva, G. M., Mediano, M. F. F., Alvarenga Americano do Brasil, P. E., da Costa Chambela, M., da Silva, J. A., de Sousa, A. S., Xavier, S. S., Rodrigues da Costa, A., Magalhães Saraiva, R., & Hasslocher-Moreno, A. M. (2014). A Clinical Adverse Drug Reaction Prediction Model for Patients with Chagas Disease Treated with Benznidazole. Antimicrobial Agents and Chemotherapy, 58(11), 6371–6377. https://doi.org/10.1128/AAC.02842-14
Spitzner, F. L., De Freitas, J. M., Macedo, A. M., De Ornelas Toledo, M. J., De Araújo, S. M., Prioli, A. J., & Gomes, M. L. (2007). Trypanosoma cruzi-triatomine associations and the presence of mixed infections in single triatomine bugs in Paraná state, Brazil. Acta Parasitologica, 52(1), 74–81. https://doi.org/10.2478/s11686-007-0005-4
Valdez, R. H., Tonin, L. T. D., Ueda-Nakamura, T., Silva, S. O., Dias Filho, B. P., Kaneshima, E. N., Yamada-Ogatta, S. F., Yamauchi, L. M., Sarragiotto, M. H., & Nakamura, C. V. (2012). In vitro and in vivo trypanocidal synergistic activity of N-butyl-1- (4-dimethylamino)phenyl-1,2,3,4-tetrahydro-β-carboline-3- carboxamide associated with benznidazole. Antimicrobial Agents and Chemotherapy, 56(1), 507–512. https://doi.org/10.1128/AAC.05575-11
Vivas, R. J., García, J. E., Guhl, F., Hernández, C., Velásquez, N., Ramírez, J. D., Carranza, J. C., & Vallejo, G. A. (2021). Systematic review on the biology, ecology, genetic diversity and parasite transmission potential of Panstrongylus geniculatus (Latreille 1811) in Latin America. Memorias Do Instituto Oswaldo Cruz, 116(1), 1–18. https://doi.org/10.1590/0074-02760200528
WHO, W. H. O. (2021). Chagas disease (American trypanosomiasis). https://www.who.int/health-topics/chagas-disease#tab=tab_1
Zingales, B, Andrade, S. G., Briones, M. R. S., Campbell, D. A., Chiari, E., Fernandes, O., Guhl, F., Lages-Silva, E., Macedo, A. M., Machado, C. R., Miles, M. A., Romanha, A. J., Sturm, N. R., Tibayrenc, M., Schijman, A. G., & Second Satellite Meeting. (2009). A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Memorias Do Instituto Oswaldo Cruz, 104(7), 1051–1054. https://doi.org/10.1590/S0074-02762009000700021
Zingales, Bianca, Miles, M. A., Campbell, D. A., Tibayrenc, M., Macedo, A. M., Teixeira, M. M. G., Schijman, A. G., Llewellyn, M. S., Lages-Silva, E., Machado, C. R., Andrade, S. G., & Sturm, N. R. (2012). The revised Trypanosoma cruzi subspecific nomenclature: Rationale, epidemiological relevance and research applications. In Infection, Genetics and Evolution. https://doi.org/10.1016/j.meegid.2011.12.009
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Copyright (c) 2021 Ana Paula de Abreu; Hevillyn Fernanda Lucas da Silva; Marcella Paula Mansano Sarto; Giullia Ferreira Iunklaus; João Vitor Trovo ; Nilma de Souza Fernandes; Amanda Regina Nichi de Sá; Mônica Lucia Gomes; Max Jean de Ornelas Toledo
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