Etiological treatment of Chagas disease patients with benznidazole lead to a sustained pro-inflammatory profile counterbalanced by modulatory events

Immunobiology

Volumn 220, Issue 5, 2015, Pages 564-574

  Campi Azevedo, A C ^a   Gomes, J A S ^a,b   Teixeira Carvalho, A ^a   Silveira Lemos, D ^a   Vitelli Avelar, D M ^a   Sathler Avelar, R ^a   Peruhype Magalhaes V ^a   Bela S R ^a   Silvestre, K F ^b   Batista, M A ^b   Schachnik, N C C ^a   Correa Oliveira, R ^a,c   Eloi Santos, S M ^a   Martins Filho, O A ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c Instituto Nacional de Ciencia e Tecnologia em Doencas Tropicais INCT DT   (Brazil)

Author keywords

Benznidazole treatment; Chagas disease; Cytokine profile; FC R; Phagocytic capacity; TLR expression

Indexed keywords

B7 ANTIGEN; BENZNIDAZOLE; CD16 ANTIGEN; CD64 ANTIGEN; COMPLEMENT COMPONENT C3B RECEPTOR; COMPLEMENT RECEPTOR; FC RECEPTOR; FC RECEPTOR IIA; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 7; NITRIC OXIDE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA; ANTITRYPANOSOMAL AGENT; AUTACOID; CYTOKINE; FCGR1A PROTEIN, HUMAN; FCGR3A PROTEIN, HUMAN; NITROIMIDAZOLE DERIVATIVE; TLR4 PROTEIN, HUMAN;

ADULT; ARTICLE; BLOOD SAMPLING; CHAGAS DISEASE; CHRONIC DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; INCUBATION TIME; MAJOR CLINICAL STUDY; MICROENVIRONMENT; MORBIDITY; NEUTROPHIL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROLOGY; TRYPANOSOMA CRUZI; UPREGULATION; ADOLESCENT; DRUG EFFECTS; EPIDEMIOLOGY; FEMALE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; YOUNG ADULT;

ADOLESCENT; ADULT; CHAGAS DISEASE; CONTROLLED BEFORE-AFTER STUDIES; CYTOKINES; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOMODULATION; INFLAMMATION MEDIATORS; MALE; MIDDLE AGED; NEUTROPHILS; NITROIMIDAZOLES; RECEPTORS, IGG; TOLL-LIKE RECEPTOR 4; TRYPANOCIDAL AGENTS; YOUNG ADULT;

EID: 84983575831     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2014.12.006     Document Type: Article

References (43)

1. Abel L.C., Rizzo L.V., Ianni B., Albuquerque F., Bacal F., Carrara D., Bocchi E.A., Teixeira H.C., Mady C., Kalil J., Cunha-Neto E. Chronic Chagas' disease cardiomyopathy patients display an increased IFN-gamma response to Trypanosoma cruzi infection. J. Autoimmun. 2001, 17:99-107.
2. Bahia-Oliveira L.M., Gomes J.A., Cançado J.R., Ferrari T.C., Lemos E.M., Luz Z.M., Moreira M.C., Gazzinelli G., Correa-Oliveira R. Immunological and clinical evaluation of chagasic patients subjected to chemotherapy during the acute phase of Trypanosoma cruzi infection 14-30 years ago. J. Infect. Dis. 2000, 182:634-638.
3. Bestetti R.B., Dalbo C.M., Freitas O.C., Teno L.A., Castilho O.T., Oliveira J.S. Noninvasive predictors of mortality for patients with Chagas' heart disease: a multivariate stepwise logistic regression study. Cardiology 1994, 84:261-267.
4. Bonney K.M. Chagas disease in the 21st Century: a public health success or an emerging threat?. Parasite 2014, 21:11.
5. + T central memory response in chronic Chagas disease. Nat. Med. 2008, 14:542-550.
6. Camargo E.P. Growth and differentiation in Trypanosoma cruzi. I. Origin of metacyclic trypanosomes in liquid media. Rev. Inst. Med. Trop. São Paulo 1964, 6:43-100.
7. Costa G.C., da Costa Rocha M.O., Moreira P.R., Menezes C.A., Silva M.R., Gollob K.J., Dutra W.O. Functional IL-10 gene polymorphism is associated with Chagas disease cardiomyopathy. J. Infect. Dis. 2009, 199:451-454.
8. de Andrade A.L., Zicker F., de Oliveira R.M., Almeida Silva S., Luquetti A., Travassos L.R., Almeida I.C., de Andrade S.S., de Andrade J.G., Martelli C.M. Randomized trial of efficacy of benznidazole in treatment of early Trypanosoma cruzi infection. Lancet 1996, 348:1407-1413.
9. + regulatory T cells from indeterminate patients with Chagas disease can suppress the effector cells and cytokines and reveal altered correlations with disease severity. Immunobiology 2012, 217:768-777.
10. Dutra W.O., da Luz Z.M., Cançado J.R., Pereira M.E., Brigido-Nunes R.M., Galvão L.M., Colley D.G., Brener Z., Gazzinelli G., Carvalho-Parra J.F. Influence of parasite presence on the immunologic profile of peripheral blood mononuclear cells from chagasic patients after specific drug therapy. Parasite Immunol. 1996, 18:579-585.
11. Espinosa R.A., Pericchi L.R., Carrasco H.A., Escalante A., Martínez O., González R. Prognostic indicators of chronic chagasic cardiopathy. Int. J. Cardiol. 1991, 30:195-202.
12. Fabbro D.L., Streiger M.L., Arias E.D., Bizai M.L., del Barco M., Amicone N.A. Trypanocide treatment among adults with chronic Chagas disease living in Santa Fe city (Argentina), over a mean follow-up of 21 years: parasitological, serological and clinical evolution. Rev. Soc. Bras. Med. Trop. 2007, 40:1-10.
13. Fragata-Filho A.A., da Silva M.A., Boainain E. Etiologic treatment of acute and chronic Chagas disease. São Paulo Med. J. 1995, 113:867-872.
14. Garcia S., Ramos C.O., Senra J.F., Vilas-Boas F., Rodrigues M.M., Campos-de-Carvalho A.C., Ribeiro-Dos-Santos R., Soares M.B. Treatment with benznidazole during the chronic phase of experimental Chagas' disease decreases cardiac alterations. Antimicrob. Agents Chemother. 2005, 49:1521-1528.
15. Gomes J.A., Bahia-Oliveira L.M., Rocha M.O., Martins-Filho O.A., Gazzinelli G., Correa-Oliveira R. Evidence that development of severe cardiomyopathy in human Chagas' disease is due to a Th1-specific immune response. Infect. Immun. 2003, 71:1185-1193.
16. Gomes J.A., Campi-Azevedo A.C., Teixeira-Carvalho A., Silveira-Lemos D., Vitelli-Avelar D., Sathler-Avelar R., Peruhype-Magalhães V., Silvestre K.F., Batista M.A., Schachnik N.C., Correa-Oliveira R., Eloi-Santos S., Martins-Filho O.A. Impaired phagocytic capacity driven by downregulation of major phagocytosis-related cell surface molecules elicits an overall modulatory cytokine profile in neutrophils and monocytes from the indeterminate clinical form of Chagas disease. Immunobiology 2012, 217:1005-1016.
17. Laucella S.A., Mazliah D.P., Bertocchi G., Alvarez M.G., Cooley G., Viotti R., Albareda M.C., Lococo B., Postan M., Armenti A., Tarleton R.L. Changes in Trypanosoma cruzi-specific immune responses after treatment: surrogate markers of treatment efficacy. Clin. Infect. Dis. 2009, 49:1675-1684.
18. Laucella S.A., Postan M., Martin D., Hubby Fralish B., Albareda M.C., Alvarez M.G., Lococo B., Barbieri G., Viotti R.J., Tarleton R.L. Frequency of interferon-gamma-producing T cells specific for Trypanosoma cruzi inversely correlates with disease severity in chronic human Chagas disease. J. Infect. Dis. 2004, 189:909-918.
19. Luiza-Silva M., Campi-Azevedo A.C., Batista M.A., Martins M.A., Avelar R.S., da Silveira-Lemos D., Bastos-Camacho L.A., de Menezes-Martins R., de Lourdes de Sousa Maia M., Guedes-Farias R.H., da Silva-Freire M., Galler R., Homma A., Leite-Ribeiro J.G., Campos-Lemos J.A., Auxiliadora-Martins M., Eloi-Santos S.M., Teixeira-Carvalho A., Martins-Filho O.A. Cytokine signatures of innate and adaptive immunity in 17DD yellow fever vaccinated children and its association with the level of neutralizing antibody. J. Infect. Dis. 2011, 204:873-883.
20. Ministério da Saúde Brazilian Consensus on Chagas disease, Secretaria de Vigilância em Saúde. Rev Soc Bras Med Trop 2005, 38(Suppl 3):7-29.
21. Marin-Neto J.A., Cunha-Neto E., Maciel B.C., Simões M.V. Pathogenesis of chronic Chagas heart disease. Circulation 2007, 115:1109-1123.
22. Marin-Neto J.A., Rassi A., Avezum A., Mattos A.C., Rassi A., Morillo C.A., Sosa-Estani S., Yusuf S. The BENEFIT trial: testing the hypothesis that trypanocidal therapy is beneficial for patients with chronic Chagas heart disease. Mem. Inst. Oswaldo Cruz 2009, 104(Suppl. 1):319-324. BENEFIT Investigators.
23. Marin-Neto J.A., Rassi A., Morillo C.A., Avezum A., Connolly S.J., Sosa-Estani S., Rosas F., Yusuf S. Rationale and design of a randomized placebo-controlled trial assessing the effects of etiologic treatment in Chagas' cardiomyopathy: the benznidazole evaluation for interrupting trypanosomiasis (BENEFIT). Am. Heart J. 2008, 156:37-43. BENEFIT Investigators.
24. Michailowsky V., Murta S.M., Carvalho-Oliveira L., Pereira M.E., Ferreira L.R., Brener Z., Romanha A.J., Gazzinelli R.T. Interleukin-12 enhances in vivo parasiticidal effect of benznidazole during acute experimental infection with a naturally drug-resistant strain of Trypanosoma cruzi. Antimicrob. Agents Chemother. 1998, 42:2549-2556.
25. Moncayo A., Silveira A.C. Current epidemiological trends for Chagas disease in Latin America and future challenges in epidemiology, surveillance and health policy. Mem. Inst. Oswaldo Cruz 2009, 104:17-30.
26. Piaggio E., Roggero E., Pitashny M., Wietzerbin J., Bottasso O.A., Revelli S.S. Treatment with benznidazole and its immunomodulating effects on Trypanosoma cruzi-infected rats. Parasitol. Res. 2001, 87:539-547.
27. Rassi A., Amato Neto V., de Siqueira A.F., Ferriolli Filho F., Amato V.S., Rassi Júnior A. Protective effect of benznidazole against parasite reactivation in patients chronically infected with Trypanosoma cruzi and treated with corticoids for associated diseases. Rev. Soc. Bras. Med. Trop. 1999, 32:475-482.
28. Revelli S., Le Page C., Piaggio E., Wietzerbin J., Bottasso O. Benznidazole, a drug employed in the treatment of Chagas' disease, down-regulates the synthesis of nitrite and cytokines by murine stimulated macrophages. Clin. Exp. Immunol. 1999, 118:271-277.
29. Reyes P.A., Vallejo M. Trypanocidal drugs for late stage, symptomatic Chagas disease (Trypanosoma cruzi infection). Cochrane Database Syst. Rev. 2005, 19:CD004102.
30. Sathler-Avelar R., Vitelli-Avelar D.M., Elói-Santos S.M., Gontijo E.D., Teixeira-Carvalho A., Martins-Filho O.A. Blood leukocytes from benznidazole-treated indeterminate Chagas disease patients display an overall type-1-modulated cytokine profile upon short-term in vitro stimulation with Trypanosoma cruzi antigens. BMC Infect. Dis. 2012, 12:123-135.
31. Sathler-Avelar R., Vitelli-Avelar D.M., Massara R.L., Borges J.D., Lana M., Teixeira-Carvalho A., Dias J.C., Elói-Santos S.M., Martins-Filho O.A. Benznidazole treatment during early-indeterminate Chagas' disease shifted the cytokine expression by innate and adaptive immunity cells toward a type 1-modulated immune profile. Scand. J. Immunol. 2006, 64:554-563.
32. Sathler-Avelar R., Vitelli-Avelar D.M., Massara R.L., de Lana M., Dias J.C.P., Teixeira-Carvalho A., Elói-Santos S.M., Martins-Filho A.O. Etiological treatment during early chronic indeterminate Chagas disease incites an activated status on innate and adaptive immunity associated with a type 1-modulated cytokine pattern. Microbes Infect. 2008, 10:103-113.
33. Schachnik N.C., Peruhype-Magalhães V., Paula G.M., Lucas F., Freitas V.M., Martins-Filho O.A., Dusse L.M. Intracellular nitric oxide assessment in whole blood leukocytes by flow cytometry: optimization and applicability to monitor patients with chronic graft nephropathy. J. Immunol. Methods 2009, 343:103-111.
34. Schofield C.J., Jannin J., Salvatella R. The future of Chagas disease control. Trends Parasitol. 2006, 22:583-588.
35. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
36. Sosa-Estani S., Segura E.L. Etiological treatment in patients infected by Trypanosoma cruzi: experiences in Argentina. Curr. Opin. Infect. Dis. 2006, 19:583-587.
37. Sousa G.R., Gomes J.A., Fares R.C., Damásio M.P., Chaves A.T., Ferreira K.S., Nunes M.C., Medeiros N.I., Valente V.A., Corrêa-Oliveira R., Rocha M.O. Plasma cytokine expression is associated with cardiac morbidity in Chagas disease. PLoS ONE 2014, 9:e87082.
38. Souza P.E., Rocha M.O., Menezes C.A., Coelho J.S., Chaves A.C., Gollob K.J., Dutra W.O. Trypanosoma cruzi infection induces differential modulation of costimulatory molecules and cytokines by monocytes and T cells from patients with indeterminate and cardiac Chagas' disease. Infect. Immun. 2007, 75:1886-1894.
39. Taylor R. Interpretation of the correlation coefficient: a basic review. JDMS 1990, 1:35-39.
40. Van Amersfoort E.S., Van Strijp J.A. Evaluation of a flow cytometric fluorescence quenching assay of phagocytosis of sensitized sheep erythrocytes by polymorphonuclear leukocytes. Cytometry 1994, 17:294-301.
41. Viotti R., Vigliano C., Armenti H., Segura E. Treatment of chronic Chagas' disease with benznidazole: clinical and serologic evolution of patients with long-term follow-up. Am. Heart J. 1994, 127:151-162.
42. Viotti R., Vigliano C., Lococo B., Bertocchi G., Petti M., Alvarez M.G., Postan M., Armenti A. Long-term cardiac outcomes of treating chronic Chagas disease with benznidazole versus no treatment: a nonrandomized trial. Ann. Intern. Med. 2006, 144:724-734.
43. Viotti R.J., Vigliano C., Laucella S., Lococo B., Petti M., Bertocchi G., Ruiz Vera B., Armenti H. Value of echocardiography for diagnosis and prognosis of chronic Chagas disease cardiomyopathy without heart failure. Heart 2004, 90:655-660.