Sequential combined treatment with allopurinol and benznidazole in the chronic phase of Trypanosoma cruzi infection: A pilot study

Journal of Antimicrobial Chemotherapy

Volumn 68, Issue 2, 2013, Pages 424-437

  Perez Mazliah, D E ^a   Alvarez, M G ^b   Cooley, G ^c   Lococo, B E ^b   Bertocchi, G ^b   Petti, M ^b   Albareda, M C ^a   Armenti, A H ^b   Tarleton, R L ^c   Laucella, S A ^a   Viotti, R ^b  

^a Instituto Nacional de Diagnostico e Investigacion de la Enfermedad de Chagas Dr Mario Fatala Chaben   (Argentina)

^b Hospital Interzonal General de Agudos Eva Peronquot   (Argentina)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Chagas' disease; Chemotherapy; T cells; Trypanosomiasis

Indexed keywords

ALLOPURINOL; BENZNIDAZOLE; CD45RA ANTIGEN; CHEMOKINE RECEPTOR CCR7; GAMMA INTERFERON; INTERLEUKIN 2; L SELECTIN; RECOMBINANT PROTEIN;

ADULT; ANTIMICROBIAL THERAPY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURFACE; CHAGAS DISEASE; CLINICAL ARTICLE; CLINICAL PROTOCOL; CONCENTRATION RESPONSE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DERMATITIS; DRUG TOLERANCE; ENZYME LINKED IMMUNOSPOT ASSAY; EX VIVO STUDY; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MALE; OUTCOME ASSESSMENT; PHENOTYPE; PILOT STUDY; SEROLOGY; T LYMPHOCYTE ACTIVATION; TREATMENT DURATION; TREATMENT RESPONSE;

ADULT; ALLOPURINOL; ANTIPROTOZOAL AGENTS; B-LYMPHOCYTES; CHAGAS DISEASE; CHRONIC DISEASE; DRUG THERAPY, COMBINATION; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; NITROIMIDAZOLES; PILOT PROJECTS; T-LYMPHOCYTES; TREATMENT OUTCOME; TRYPANOSOMA CRUZI;

EID: 84872377363     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dks390     Document Type: Article

References (67)

1. Bern C, Montgomery SP, Herwaldt BL et al. Evaluation and treatment of Chagas disease in the United States: a systematic review. JAMA 2007; 298: 2171-81.
2. Diaz JH. Chagas disease in the United States: a cause for concern in Louisiana? J La State Med Soc 2007; 159: 21-3, 25-9.
3. Piron M, Vergés M, Munõz J et al. Seroprevalence of Trypanosoma cruzi infection in at-risk blood donors in Catalonia (Spain). Transfusion 2008; 48: 1862-8.
4. Feldman AM, McNamara D. Myocarditis. N Engl J Med 2000; 343: 1388-98.
5. de Andrade AL, Zicker F, de Oliveira RM et al. Randomised trial of efficacy of benznidazole in treatment of early Trypanosoma cruzi infection. Lancet 1996; 348: 1407-13.
6. Sosa Estani S, Segura EL, Ruiz AM et al. Efficacy of chemotherapy with benznidazole in children in the indeterminate phase of Chagas' disease. Am J Trop Med Hyg 1998; 59: 526-9.
7. Fabbro De Suasnábar D, Arias E, Streiger M et al. Evolutive behavior towards cardiomyopathy of treated (nifurtimox or benznidazole) and untreated chronic chagasic patients. Rev Inst Med Trop de Sao Paulo 2000; 42: 99-109.
8. Fabbro DL, Streiger ML, Arias ED et al. 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.
9. Viotti R, Vigliano C, Armenti H et al. Treatment of chronic Chagas disease with benznidazole: clinical and serologic evolution of patients with long-term follow-up. Am Heart J 1994; 127: 151-62.
10. Viotti R, Vigliano C, Lococo B et al. Long-term cardiac outcomes of treating chronic Chagas disease with benznidazole versus no treatment: a nonrandomized trial. Ann Intern Med 2006; 144: 724-34.
11. Apt W, Aguilera X, Arribada A et al. Treatment of chronic Chagas' disease with itraconazole and allopurinol. Am J Trop Med Hyg 1998; 59: 133-8.
12. Apt W, Arribada A, Zulantay I et al. Itraconazole or allopurinol in the treatment of chronic American trypanosomiasis: the regression and prevention of electrocardiographic abnormalities during 9 years of follow-up. Ann Trop Med Parasitol 2003; 97: 23-9.
13. Apt W, Arribada A, Zulantay I et al. Itraconazole or allopurinol in the treatment of chronic American trypanosomiasis: the results of clinical and parasitological examinations 11 years post-treatment. Ann Trop Med Parasitol 2005; 99: 733-41.
14. Gallerano RH, Marr JJ, Sosa RR. Therapeutic efficacy of allopurinol in patients with chronic Chagas' disease. Am J Trop Med Hyg 1990; 43: 159-66.
15. Rassi A, Luquetti AO, Rassi A et al. Specific treatment for Trypanosoma cruzi: lack of efficacy of allopurinol in the human chronic phase of Chagas disease. Am J Trop Med Hyg 2007; 76: 58-61.
16. Buckner FS, Navabi N. Advances in Chagas disease drug development: 2009-2010. Curr Opin Infect Dis 2010; 23: 609-16.
17. Nahid P, Pai M, Hopewell PC. Advances in the diagnosis and treatment of tuberculosis. Proc Am Thorac Soc 2006; 3: 103-10.
18. Simon V, Ho DD, Abdool Karim Q. HIV/AIDS epidemiology, pathogenesis, prevention, and treatment. Lancet 2006; 368: 489-504.
19. Ngasala BE, Malmberg M, Carlsson AM et al. Efficacy and effectiveness of artemether-lumefantrine after initial and repeated treatment in children <5 years of age with acute uncomplicated Plasmodium falciparum malaria in rural Tanzania: a randomized trial. Clin Infect Dis 2011; 52: 873-82.
20. YavoW, Faye B, Kuete T et al. Multicentric assessment of the efficacy and tolerability of dihydroartemisinin-piperaquine compared to artemetherlumefantrine in the treatment of uncomplicated Plasmodium falciparum malaria in sub-Saharan Africa. Malar J 2011; 10: 198.
21. Priotto G, Kasparian S, Mutombo W et al. Nifurtimox-eflornithine combination therapy for second-stage African Trypanosoma brucei gambiense trypanosomiasis: a multicentre, randomised, phase III, non-inferiority trial. Lancet 2009; 374: 56-64.
22. Docampo R, Moreno SN. Free radical metabolism of antiparasitic agents. Fed Proc 1986; 45: 2471-6.
23. Díaz de Toranzo EG, Castro JA, Franke de Cazzulo BM et al. Interaction of benznidazole reactive metabolites with nuclear and kinetoplastic DNA, proteins and lipids from Trypanosoma cruzi. Experientia 1988; 44: 880-1.
24. Polak A, Richle R. Mode of action of the 2-nitroimidazole derivative benznidazole. Ann Trop Med Parasitol 1978; 72: 45-54.
25. Marr JJ. Purine analogs as chemotherapeutic agents in leishmaniasis and American trypanosomiasis. J Lab Clin Med 1991; 118: 111-9.
26. WHO. Control of Chagas Disease. Second Report of the WHO Expert Committee. 2002. http://whqlibdoc.who.int/trs/WHO_TRS_905.pdf (26 July 2012, date last accessed).
27. Kuschnir E, Sgammini H, Castro R et al. Evaluation of cardiac function by radioisotopic angiography, in patients with chronic Chagas cardiopathy. Arq Bras Cardiol 1985; 45: 249-56.
28. Viotti R, Vigliano C, Alvarez MG et al. Impact of aetiological treatment on conventional and multiplex serology in chronic Chagas disease. PLoS Negl Trop Dis 2011; 5: e1314.
29. Cooley G, Etheridge RD, Boehlke C et al. High throughput selection of effective serodiagnostics for Trypanosoma cruzi infection. PLoS Negl Trop Dis 2008; 2: e316.
30. Laucella SA, Mazliah DP, Bertocchi G et al. Changes in Trypanosoma cruzi-specific immune responses after treatment: surrogate markers of treatment efficacy. Clin Infect Dis 2009; 49: 1675-84.
31. Laucella SA, Postan M, Martin D et al. Frequency of interferon-g-producing T cells specific for Trypanosoma cruzi inversely correlates with disease severity in chronic human Chagas disease. J Infect Dis 2004; 189: 909-18.
32. + T cells in chronic Chagas disease. PLoS Negl Trop Dis 2008; 2: e288.
33. + T cells in chronic Chagas' disease patients. Int Immunol 2006; 18: 465-71.
34. + T cells to immune senescence. J Immunol 2009; 183: 4103-8.
35. Dutra WO, Martins-Filho OA, Cançado JR et al. Activated T and B lymphocytes in peripheral blood of patients with Chagas' disease. Int Immunol 1994; 6: 499-506.
36. Roujeau JC, Kelly JP, Naldi L et al. Medication use and the risk of Stevens-Johnson syndrome or toxic epidermal necrolysis. N Engl J Med 1995; 333: 1600-7.
37. George J, Carr E, Davies J et al. High-dose allopurinol improves endothelial function by profoundly reducing vascular oxidative stress and not by lowering uric acid. Circulation 2006; 114: 2508-16.
38. Viotti R, Vigliano C. Etiological treatment of chronic Chagas disease: neglected 'evidence' by evidence-based medicine. Expert Rev Anti Infect Ther 2007; 5: 717-26.
39. Sosa-Estani S, Viotti R, Segura E. Therapy, diagnosis and prognosis of chronic Chagas disease: insight gained in Argentina. Mem Inst Oswaldo Cruz 2009; 104: 167-80.
40. Sánchez Negrette O, Sánchez Valdez FJ, Lacunza CD et al. Serological evaluation of specific-antibody levels in patients treated for chronic Chagas' disease. Clin Vaccine Immunol 2008; 15: 297-302.
41. Harari A, Dutoit V, Cellerai C et al. Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol Rev 2006; 211: 236-54.
42. Shin H, Blackburn SD, Blattman JN et al. Viral antigen and extensive division maintain virus-specific CD8 T cells during chronic infection. J Exp Med 2007; 204: 941-9.
43. Wherry EJ, Barber DL, Kaech SM et al. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci USA 2004; 101: 16004-9.
44. + T cells in peripheral blood after initiation of highly active antiretroviral therapy. J Virol 2001; 75: 6508-16.
45. Argüello RJ, Albareda MC, Alvarez MG et al. Inhibitory receptors are expressed by Trypanosoma cruzi-specific effector T cells and in hearts of subjects with chronic Chagas disease. PLoS One 2012; 7: e35966.
46. Dai Y, Qiu Z-F, Li T-S et al. Clinical outcomes and immune reconstitution in 103 advanced AIDS patients undergoing 12-month highly active antiretroviral therapy. Chin Med J (Engl) 2006; 119: 1677-82.
47. Jansen CA, Piriou E, De Cuyper IM et al. Long-term highly active antiretroviral therapy in chronic HIV-1 infection: evidence for reconstitution of antiviral immunity. Antivir Ther 2006; 11: 105-16.
48. Oláh T, Régely K, Mándi Y. The inhibitory effects of allopurinol on the production and cytotoxicity of tumor necrosis factor. Naunyn Schmiedebergs Arch Pharmacol 1994; 350: 96-9.
49. Mizuno K, Okamoto H, Horio T. Inhibitory influences of xanthine oxidase inhibitor and angiotensin I-converting enzyme inhibitor on multinucleated giant cell formation from monocytes by downregulation of adhesion molecules and purinergic receptors. Br J Dermatol 2004; 150: 205-10.
50. Lee P-C, Ho I-C, Lee T-C. Oxidative stress mediates sodium arsenite-induced expression of heme oxygenase-1, monocyte chemoattractant protein-1, and interleukin-6 in vascular smooth muscle cells. Toxicol Sci 2005; 85: 541-50.
51. Moorhouse PC, Grootveld M, Halliwell B et al. Allopurinol and oxypurinol are hydroxyl radical scavengers. FEBS Lett 1987; 213: 23-8.
52. Kurashige S, Akuzawa Y, Mitsuhashi S. Purine metabolic enzymes in lymphocytes. IV. Effects of enzyme inhibitors and enzyme substrates on the blastogenic responses of human lymphocytes. Scand J Immunol 1985; 22: 1-7.
53. Araújo MS, Martins-Filho OA, Pereira ME et al. A combination of benznidazole and ketoconazole enhances efficacy of chemotherapy of experimental Chagas' disease. J Antimicrob Chemother 2000; 45: 819-24.
54. Batista DdGJ, Batista MM, de Oliveira GM et al. Combined treatment of heterocyclic analogues and benznidazole upon Trypanosoma cruzi in vivo. PloS One 2011; 6: e22155.
55. Maldonado RA, Molina J, Payares G et al. Experimental chemotherapy with combinations of ergosterol biosynthesis inhibitors in murine models of Chagas' disease. Antimicrob Agents Chemother 1993; 37: 1353-9.
56. Benaim G, Sanders JM, Garcia-Marchán Y et al. Amiodarone has intrinsic anti-Trypanosoma cruzi activity and acts synergistically with posaconazole. J Med Chem 2006; 49: 892-9.
57. Kuehn CC, Rodrigues Oliveira LG, Santos CD et al. Melatonin and dehydroepiandrosterone combination: does this treatment exert a synergistic effect during experimental Trypanosoma cruzi infection? J Pineal Res 2009; 47: 253-9.
58. López-MunõzR, Faúndez M, Klein S et al. Trypanosoma cruzi: in vitro effect of aspirin with nifurtimox and benznidazole. Exp Parasitol 2010; 124: 167-71.
59. Rassi A, Amato Neto V, de Siqueira AF et al. Treatment of chronic Chagas' disease with an association of nifurtimox and corticoid. Rev Soc Bras Med Trop 2002; 35: 547-50.
60. Avila JL, Avila A. Trypanosoma cruzi: allopurinol in the treatment of mice with experimental acute Chagas disease. Exp Parasitol 1981; 51: 204-8.
61. Gobbi P, Baez A, Lo Presti MS et al. Association of clomipramine and allopurinol for the treatment of the experimental infection with Trypanosoma cruzi. Parasitol Res 2010; 107: 1279-83.
62. Gobbi P, Lo Presti MS, Fernández AR et al. Allopurinol is effective to modify the evolution of Trypanosoma cruzi infection in mice. Parasitol Res 2007; 101: 1459-62.
63. Berens RL, Marr JJ, Steele da Cruz FS et al. Effect of allopurinol on Trypanosoma cruzi: metabolism and biological activity in intracellular and bloodstream forms. Antimicrob Agents Chemother 1982; 22: 657-61.
64. Nakajima-Shimada J, Hirota Y, Aoki T. Inhibition of Trypanosoma cruzi growth in mammalian cells by purine and pyrimidine analogs. Antimicrob Agents Chemother 1996; 40: 2455-8.
65. Almeida DR, Carvalho AC, Branco JN et al. Chagas' disease reactivation after heart transplantation: efficacy of allopurinol treatment. J Heart Lung Transplant 1996; 15: 988-92.
66. Bestetti RB, Theodoropoulos TAD. A systematic review of studies on heart transplantation for patients with end-stage Chagas' heart disease. J Card Fail 2009; 15: 249-55.
67. Tomimori-Yamashita J, Deps PD, Almeida DR et al. Cutaneous manifestation of Chagas' disease after heart transplantation: successful treatment with allopurinol. Br J Dermatol 1997; 137: 626-30.