Skip to main content

Advertisement

Log in

Different infective forms trigger distinct lesions in the colon during experimental Chagas disease

  • Immunology and Host-Parasite Interactions - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

With the control of vectorial transmission of Chagas disease caused by metacyclic trypomastigotes (MT) in endemic countries, other pathways of infection have become important. The infection caused by blood trypomastigotes (BT) is relevant in places where the blood transfusion and organ transplantation are poorly controlled. This study aimed to evaluate immunopathogenic parameters in the colon during the acute and chronic phases of experimental infection in Swiss mice infected with BT or MT forms of VL-10 strain of Trypanosoma cruzi. We have found that animals infected with MT forms presented lower survival rate, and higher tissue parasitism in the acute phase of the disease, which may be associated with the exacerbated activation of the immune system with the production of pro-inflammatory cytokines even in the chronic phase of infection. Taken together, these results can also be associated to the maintenance of the inflammatory process in chronic phase and an earlier denervation of myenteric plexus in colon. These findings emphasized the importance of the inoculum source and the strain, once different forms of different strains seem to promote distinct diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Adad SJ, Cançado CG, Etchebehere RM, Teixeira VPA, Gomes UA, Chapadeiro E, Lopes ER (2001) Neuron count reevaluation in the myenteric plexus of chagasic megacolon after morphometric neuron analysis. Virchows Archiv 438(3):254–258

    Article  CAS  Google Scholar 

  • Adad, Sheila Jorge, Gisele Barbosa e Silva, and Alessandro Adad Jammal. 2013. The development of chagasic megacolon requires severe denervation and the reduction in interstitial cells of Cajal number might be a contributing factor. Virchows Archiv 462 (1): 127-127

  • Alcantara A, Brener Z (1978) The in vitro interaction of Trypanosoma cruzi bloodstream forms and mouse peritoneal macrophages. Acta Tropica 35(3):209–219

    CAS  PubMed  Google Scholar 

  • Andrade LO, Andrews NW (2005) Opinion: the Trypanosoma cruzi-host-cell interplay: location, invasion, retention. Nat Rev Microbiol 3(10):819

    Article  CAS  Google Scholar 

  • Arantes RME, Marche HHF, Bahia MT, Cunha FQ, Rossi MA, Silva JS (2004) Interferon-γ-induced nitric oxide causes intrinsic intestinal denervation in Trypanosoma cruzi-infected mice. Am J Pathol 164(4):1361–1368

    Article  CAS  Google Scholar 

  • Borges DC, Araújo NM, Cardoso CR, Lazo JE, Chica. (2013) Different parasite inocula determine the modulation of the immune response and outcome of experimental Trypanosoma cruzi infection. Immunology 138(2):145–156

    Article  CAS  Google Scholar 

  • Brener Z (1962) Therapeutic activity and criterion of cure on mice experimentally infected with Trypanosoma cruzi. Revista Do Instituto De Medicina Tropical De São Paulo 4(6):389–396

    CAS  PubMed  Google Scholar 

  • Brener Z, Gazzinelli RT (1997) Immnunological Control of Trypanosoma cruzi infection and pathogenesis of Chagas’ disease. Int Arch Allergy Immunol 114(2):103–110

    Article  CAS  Google Scholar 

  • Campos JV, Tafuri WL (1973) Chagas enteropathy. Gut 14(11):910

    Article  CAS  Google Scholar 

  • Cardillo F, Postol E, Nihei J, Aroeira LS, Nomizo A, Mengel J (2007) B cells modulate T cells so as to favour T helper type 1 and CD8+ T-cell responses in the acute phase of Trypanosoma cruzi infection. Immunology 122(4):584–595

    Article  CAS  Google Scholar 

  • Carneiro CM, Martins-Filho OA, Reis AB, Veloso VM, Araújo FMG, Bahia MT, de Lana M, Machado-Coelho GLL, Gazzinelli G, Correa-Oliveira R (2007) Differential impact of metacyclic and blood trypomastigotes on parasitological, serological and phenotypic features triggered during acute Trypanosoma cruzi infection in dogs. Acta Tropica 101(2):120–129

    Article  CAS  Google Scholar 

  • Chagas Carlos (1909) Nova tripanozomiaze humana: estudos sobre a morfologia 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

    Article  Google Scholar 

  • Corbett, Carlos EP, Ulysses Ribeiro, Maria das Graças Prianti, Angelita Habr-Gama, Masayuki Okumura, and Joaquim Gama-Rodrigues. 2001. Cell-mediated immune response in megacolon from patients with chronic Chagas’ disease. Diseases of the colon & rectum 44 (7): 993-998

  • Corrêa-Oliveira R, de Assis J, Gomes S, Lemos EM, Cardoso GM, Reis DD’Ávila, Adad S, Crema E, Martins-Filho OA, Costa MOR, Gazzinelli G (1999) The role of the immune response on the development of severe clinical forms of human Chagas disease. Memórias Do Instituto Oswaldo Cruz 94:253–255

    Article  Google Scholar 

  • Coura JR, Dias JCP (2009) Epidemiology, control and surveillance of Chagas disease: 100 years after its discovery. Memórias Do Instituto Oswaldo Cruz 104:31–40

    Article  Google Scholar 

  • Coura José Rodrigues, Viñas Pedro Albajar (2010) Chagas disease: a new worldwide challenge. Nature 465(7301):S6–S7

    Article  Google Scholar 

  • Cummings KL, Tarleton RL (2003) Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Mol Biochem Parasit 129(1):53–59

    Article  CAS  Google Scholar 

  • Da Silveira ABM, Arantes RME, Vago AR, Lemos EM, Adad SJ, Correa-Oliveira R, Avila Reis DD (2005) Comparative study of the presence of Trypanosoma cruzi kDNA, inflammation and denervation in chagasic patients with and without megaesophagus. Parasitology 131(5):627–634

    Article  Google Scholar 

  • da Silveira A, Morais B, Lemos EM, Adad SJ, Correa-Oliveira R, Furness JB, Reis DD (2007) Megacolon in Chagas disease: a study of inflammatory cells, enteric nerves, and glial cells. Human Pathology 38(8):1256–1264

    Article  Google Scholar 

  • de Abreu Vieira, Paula Melo, Amanda Fortes Francisco, Evandro Marques de Meneses Machado, Nívia Carolina Nogueira, Kátia da Silva Fonseca, Alexandre Barbosa Reis, Andrea Teixeira-Carvalho, Olindo Assis Martins-Filho, Washington Luiz Tafuri, and Cláudia Martins Carneiro. 2012. Different infective forms trigger distinct immune response in experimental Chagas disease. PloS one 7 (3): e32912

  • de Almeida-Leite, Camila Megale, Lúcia Maria da Cunha Galvão, Luis CC Afonso, Fernando de Queiróz Cunha, and Rosa Maria Esteves Arantes. 2007. Interferon-γ induced nitric oxide mediates in vitro neuronal damage by Trypanosoma cruzi-infected macrophages. Neurobiology of disease 25 (1): 170-178

  • DeFaria CR, De Rezende JM, Rassi A (1988) Peripheral denervation in the various clinical forms of Chagas’ disease. Arquivos De Neuro-Psiquiatria 46(3):225–237

    Article  CAS  Google Scholar 

  • Dorn PL, Perniciaro L, Yabsley MJ, Roellig DM, Balsamo G, Diaz J, Wesson D (2007) Autochthonous transmission of Trypanosoma cruzi, Louisiana. Emerg Infect Dis 13(4):605

    Article  Google Scholar 

  • Fernandes MC, Andrews NW (2012) Host cell invasion by Trypanosoma cruzi: a unique strategy that promotes persistence. FEMS Microbiol Rev 36(3):734–747

    Article  CAS  Google Scholar 

  • González CSM, Sanz OP, Muller LA, Molina HA, Fernandez J, Rimoldi MT, Sica REP (1987) Peripheral nervous system damage in experimental chronic Chagas’ disease. Am J Trop Med Hyg 36(1):41–45

    Article  Google Scholar 

  • Gürtler RE, Segura EL, Cohen JE (2003) Congenital transmission of Trypanosoma cruzi infection in Argentina. Emerg Infect Dis 9(1):29

    Article  Google Scholar 

  • Haberland A, Saravia SGM, Wallukat G, Ziebig R, Schimke I (2013) Chronic Chagas disease: from basics to laboratory medicine. Clin Chem Lab Med 51(2):271–294

    Article  CAS  Google Scholar 

  • Koberle F, de ALCANTARA F (1960) Mechanism of destruction of the neurons of the peripheral nervous system in Changas’ disease. Hospital (Rio de Janeiro, Brazil) 57:1057

    CAS  Google Scholar 

  • Köberle, Fritz. 1968. Chagas’ disease and Chagas’ syndromes: the pathology of American trypanosomiasis. In Advances in parasitology, 63–116. Elsevier.

  • Lages-Silva E, Crema E, Ramirez LE, Macedo AM, Pena SD, Chiari E (2001) Relationship between Trypanosoma cruzi and human chagasic megaesophagus: blood and tissue parasitism. Am J Trop Med Hyg 65(5):435–441

    Article  CAS  Google Scholar 

  • Leite MF, Moyer MS, Andrews NW (1998) Expression of the mammalian calcium signaling response to Trypanosoma cruzi in Xenopus laevis oocytes. Mol Biochem Parasit 92(1):1–13

    Article  CAS  Google Scholar 

  • Lemos, Juliana Regina Dias, Wellington Francisco Rodrigues, Camila Botelho Miguel, Ricardo Cambraia Parreira, Renata Botelho Miguel, Alexandre de Paula Rogerio, Carlo Jose Freire Oliveira, and Javier Emilio Lazo Chica. 2013. Influence of parasite load on renal function in mice acutely infected with Trypanosoma cruzi. PloS one 8 (8): e71772.

  • Lopes MF, Nunes MP, Henriques-Pons A, Giese N, Morse III HC, Davidson WF, Araújo-Jorge TC, Dosreis GA (1999) Increased susceptibility of Fas ligand-deficient gld mice to Trypanosoma cruzi infection due to a Th2-biased host immune response. Eur J Immunol 29(1):81–89

    Article  CAS  Google Scholar 

  • Machado, Fabiana S, Walderez O Dutra, Lisia Esper, Kenneth J Gollob, Mauro M Teixeira, Stephen M Factor, Louis M Weiss, Fnu Nagajyothi, Herbert B Tanowitz, and Nisha J Garg. 2012. Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Seminars in immunopathology.

  • Nascimento, Rodolfo Duarte, André de Souza Lisboa, Ricardo Toshio Fujiwara, Michelle Aparecida Ribeiro de Freitas, Sheila Jorge Adad, Rodrigo Correa Oliveira, Débora d’Ávila Reis, and Alexandre Barcelos Morais da Silveira. 2010. Characterization of enteroglial cells and denervation process in chagasic patients with and without megaesophagus. Human pathology 41 (4): 528-534

  • Neira I, Silva FA, Cortez M, Yoshida N (2003) Involvement of Trypanosoma cruzi metacyclic trypomastigote surface molecule gp82 in adhesion to gastric mucin and invasion of epithelial cells. Infect Immun 71(1):557–561

    Article  CAS  Google Scholar 

  • Organization, World Health (2000) Challenges of Chagas disease vector control in Central America: position paper. World Health Organization, Geneva

    Google Scholar 

  • Prevention, Centers for Disease Control and. 2006. Chagas disease after organ transplantation--Los Angeles, California, 2006. MMWR. Morbidity and mortality weekly report 55 (29): 798

  • Ramirez MARCEL, de C Ruiz IVAN R, Araya JORGE ENRIQUE, Da Silveira JFranco, Yoshida NOBUKO (1993) Involvement of the stage-specific 82-kilodalton adhesion molecule of Trypanosoma cruzi metacyclic trypomastigotes in host cell invasion. Infect Immun 61(9):3636–3641

    Article  CAS  Google Scholar 

  • Anis Rassi Jr, Anis Rassi, Marin-Neto José Antonio (2010) Chagas disease. Lancet 375(9723):1388–1402

    Article  Google Scholar 

  • Reis DD, Jones EM, Sebastiao T Jr, Lopes ER, Gazzinelli G, Colley DG, McCurley TL (1993) Characterization of inflammatory infiltrates in chronic chagasic myocardial lesions: presence of tumor necrosis factor-α+ cells and dominance of granzyme A+, CD8+ lymphocytes. Am J Trop Med Hyg 48(5):637–644

    Article  CAS  Google Scholar 

  • Ricci, Mayra Fernanda, Samantha Ribeiro Béla, Michele Macedo Moraes, Maria Terezinha Bahia, Ana Lia Mazzeti, Anny Carolline Silva Oliveira, Luciana Oliveira Andrade, Rafael Radí, Lucía Piacenza, and Rosa Maria Esteves Arantes. 2020. Neuronal parasitism, early myenteric neurons depopulation and continuous axonal networking damage as underlying mechanisms of the experimental intestinal Chagas’ disease. Frontiers in Cellular and Infection Microbiology 10.

  • Schmunis GA (2007) Epidemiology of Chagas disease in non-endemic countries: the role of international migration. Memórias Do Instituto Oswaldo Cruz 102:75–86

    Article  Google Scholar 

  • Tanowitz HB, Kirchhoff LV, Simon D, Morris SA, Weiss LM, Wittner M (1992) Chagas’ disease. Clin Microbiol Rev 5(4):400–419

    Article  CAS  Google Scholar 

  • Tarleton RL, Sun J, Zhang L, Postan M (1994) Depletion of T-cell subpopulations results in exacerbation of myocarditis and parasitism in experimental Chagas’ disease. Infect Immun 62(5):1820–1829

    Article  CAS  Google Scholar 

  • Teixeira ARL, Hecht MM, Guimaro MC, Sousa AO, Nitz N (2011) Pathogenesis of chagas’ disease: parasite persistence and autoimmunity. Clin Microbiol Rev 24(3):592–630

    Article  CAS  Google Scholar 

  • Tyler KM, Engman DM (2001) The life cycle of Trypanosoma cruzi revisited. Int J Parasit 31(5–6):472–481

    Article  CAS  Google Scholar 

  • WHO (2018), Chagas disease (American Trypanosomiasis). Tech. UNDP/World Bank/WHO. Available online at: http://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis) (accessed May 10,2020).

  • Young C, Losikoff P, Chawla A, Glasser L, Forman E (2007) Transfusion-acquired Trypanosoma cruzi infection. Transfusion 47(3):540–544

    Article  Google Scholar 

Download references

Acknowledgements

We are thankful to the Animal Facility at Ouro Preto Federal University (UFOP), Minas Gerais State, Brazil (CCA/UFOP), for providing the animals and multi-user microscopy and flow cytometry facilities from Nucleus of Biological Sciences Research – NUPEB-UFOP for the contribution with morphometric and cytometric analysis.

Funding

This work was supported by the Universidade Federal de Ouro Preto (PROPPI-UFOP), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paula Melo de Abreu Vieira.

Ethics declarations

Disclaimer

The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Marta Teixeira

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Souza Marques, F., Duarte, T.H.C., Xavier, V.F. et al. Different infective forms trigger distinct lesions in the colon during experimental Chagas disease. Parasitol Res 120, 3475–3486 (2021). https://doi.org/10.1007/s00436-021-07236-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07236-2

Keywords

Navigation