Volume 98, Issue 3
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Achalasia is a motility disorder of the esophagus that might be secondary to a chronic infection. Several studies have investigated esophageal achalasia in patients with Chagas disease (CD) in Latin America, but no related studies have been performed in Colombia. The goals of the present study were to determine the presence of anti- antibodies in patients with esophageal achalasia who visited a referral hospital in Bogotá, Colombia, and to detect the presence of the parasite and its discrete typing units (DTUs). This cross-sectional study was conducted in adult patients (18–65 years old) who were previously diagnosed with esophageal achalasia and from whom blood was drawn to assess antibodies against using four different serological tests. DNA was detected by conventional polymerase chain reaction (cPCR) and quantitative polymerase chain reaction (qPCR). In total, 38 patients, with an average age of 46.6 years (standard deviation of ±16.2) and comprising 16 men and 22 women, were enrolled. Five (13.15%) patients were found to be positive for anti- antibodies by indirect immunofluorescence assay (IFA), and two patients who were negative according to IFA were reactive by both enzyme-linked immunosorbent assay and immunoblot (5.3%). Parasite DNA was detected in two of these seven patients by cPCR and in one of these by qPCR. The parasite DTU obtained was TcI. In summary, this study identified in Colombian patients with esophageal achalasia, indicating that digestive compromise could also be present in patients with chronic CD.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


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  1. Cucunubá ZM, Manne-Goehler JM, Díaz D, Nouvellet P, Bernal O, Marchiol A, Basáñez MG, Conteh L, , 2017. How universal is coverage and access to diagnosis and treatment for Chagas disease in Colombia? A health systems analysis. Soc Sci Med 175: 187198.
  2. Bern C, , 2015. Chagas’ disease. N Engl J Med 373: 456466.
  3. Machado FS, Dutra WO, Esper L, Gollob KJ, Teixeira MM, Factor SM, Weiss LM, Nagajyothi F, Tanowitz HB, Garg NJ, , 2012. Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Semin Immunopathol 34: 753770.
  4. Andrade SG, Magalhaes JB, , 1996. Biodemes and zymodemes of Trypanosoma cruzi strains: correlations with clinical data and experimental pathology. Rev Soc Bras Med Trop 30: 2735.
  5. Zingales B, 2012. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol 12: 240253.
  6. Rassi A, Jr Rassi A, Marcondes de Rezende J, , 2012. American trypanosomiasis (Chagas disease). Infect Dis Clin North Am 26: 275291.
  7. Dantas RO, , 2003. Comparação entre acalásia idiopática e acalásia conseqüente à doença de Chagas: revisão de publicações sobre o tema. Arq Gastroenterol 40: 126130.
  8. Herbella FA, Oliveira DR, Del Grande JC, , 2004. Are idiopathic and Chagasic achalasia two different diseases? Dig Dis Sci 49: 353360.
  9. Andrade C de M, Câmara AC, Nunes DF, Guedes PM, Pereira WO, Chiari E, Diniz RV, Galvão LM, , 2015. Chagas disease: morbidity profile in an endemic area of northeastern Brazil. Rev Soc Bras Med Trop 48: 706715.
  10. Souza DH, Vaz M da G, Fonseca CR, Luquetti A, Rezende Filho J, Oliveira EC, , 2013. Current epidemiological profile of Chagasic megaesophagus in Central Brazil. Rev Soc Bras Med Trop 46: 316321.
  11. Pérez-Ayala A, Pérez-Molina JA, Norman F, Monge-Maillo B, Faro MV, López-Vélez R, , 2011. Gastro-intestinal Chagas disease in migrants to Spain: prevalence and methods for early diagnosis. Ann Trop Med Parasitol 105: 2529.
  12. Pinazo MJ, Lacima G, Elizalde JI, Posada EJ, Gimeno F, Aldasoro E, Valls ME, Gascon J, , 2014. Characterization of digestive involvement in patients with chronic T. cruzi infection in Barcelona, Spain. PLoS Negl Trop Dis 8: e3105.
  13. Gobbi F, 2014. Profile of Trypanosoma cruzi infection in a tropical medicine reference center, northern Italy. PLoS Negl Trop Dis 8: e3361.
  14. Mantilla JC, Zafra GA, Macedo AM, Gonzalez CI, , 2010. Mixed infection of Trypanosoma cruzi I and II in a Colombian cardiomyopathic patient. Hum Pathol 4: 610613.
  15. da Nóbrega AA, de Araújo WN, Vasconcelos AM, , 2014. Mortality due to Chagas disease in Brazil according to a specific cause. Am J Trop Med Hyg 91: 528533.
  16. 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: 435441.
  17. da Silveira AB, Arantes RM, Vago AR, Lemos EM, Adad SJ, Correa-Oliveira R, D’Avila Reis D, , 2005. Comparative study of the presence of Trypanosoma cruzi kDNA, inflammation and denervation in chagasic patients with and without megaesophagus. Parasitology 131: 627634.
  18. Manoel-Caetano Fda S, Carareto CM, Borim AA, Miyazaki K, Silva AE, , 2008. kDNA gene signatures of Trypanosoma cruzi in blood and oesophageal mucosa from chronic chagasic patients. Trans R Soc Trop Med Hyg 102: 11021107.
  19. de Lima MA, Cabrine-Santos M, Tavares MG, Gerolin GP, Lages-Silva E, Ramirez LE, , 2008. Interstitial cells of Cajal in chagasic megaesophagus. Ann Diagn Pathol 12: 271274.
  20. Nascimento RD, de Souza Lisboa A, Fujiwara RT, de Freitas MA, Adad SJ, Oliveira RC, d’Avila Reis D, da Silveira AB, , 2010. Characterization of enteroglial cells and denervation process in chagasic patients with and without megaesophagus. Hum Pathol 41: 528534.
  21. D’ Avila D, Lemos EM, Silva GC, Abad SJ, McCurley T, Correa-Oliveira R, Machado C, , 2001. Phenotypic characterization of the inflammatory cells in chagasic megaoesophagus. Trans R Soc Trop Med Hyg 95: 177178.
  22. Vargas-Zambrano JC, Lasso P, Cuellar A, Puerta CJ, González JM, , 2013. A human astrocytoma cell line is highly susceptible to infection with Trypanosoma cruzi. Mem Inst Oswaldo Cruz 108: 212219.
  23. Ferreira AW, Belem ZR, Lemos EA, Reed SG, Campos-Neto A, , 2001. Enzyme-linked immunosorbent assay for serological diagnosis of Chagas’ disease employing a Trypanosoma cruzi recombinant antigen that consists of four different peptides. J Clin Microbiol 39: 43904395.
  24. Houghton RL, Benson DR, Reynolds LD, McNeill PD, Sleath PR, Lodes MJ, Skeiky YA, Leiby DA, Badaro R, Reed SG, , 1999. A multi-epitope synthetic peptide and recombinant protein for the detection of antibodies to Trypanosoma cruzi in radioimmunoprecipitation-confirmed and consensus-positive sera. J Infect Dis 179: 12261234.
  25. Chang CD, 2006. Evaluation of a prototype Trypanosoma cruzi antibody assay with recombinant antigens on a fully automated chemiluminescence analyzer for blood donor screening. Transfusion 46: 17371744.
  26. Cheng KY, Chang CD, Salbilla VA, Kirchhoff LV, Leiby DA, Schochetman G, Shah DO, , 2007. Immunoblot assay using recombinant antigens as a supplemental test to confirm the presence of antibodies to Trypanosoma cruzi. Clin Vaccine Immunol 14: 355361.
  27. Mateus J, Lasso P, Pavia P, Rosas F, Roa N, Valencia-Hernández CA, González JM, Puerta CJ, Cuéllar A, , 2015. Low frequency of circulating CD8+ T stem cell memory cells in chronic chagasic patients with severe forms of the disease. PLoS Negl Trop Dis 8: e3432.
  28. Barrera YK, Guevara JM, Pavia PX, Montilla M, Nicholls RS, Parra E, Puerta C, , 2008. Evaluation of TcH2AF-R and S35-S36 primers in PCR tests for the detection of Trypanosoma cruzi in mouse cardiac tissue [in Spanish]. Biomedica 28: 616626.
  29. Lasso P, Mateus J, Pavía P, Rosas F, Roa N, Thomas MC, López MC, González JM, Puerta CJ, Cuéllar A, , 2015. Inhibitory receptor expression on CD8+ T cells is linked to functional responses against Trypanosoma cruzi antigens in chronic chagasic patients. J Immunol 195: 37483758.
  30. Piron M, Fisa R, Casamitjana N, López-Chejade P, Puig L, Vergés M, Gascón J, Gómez i Prat J, Portús M, Sauleda S, , 2007. Development of a real-time PCR assay for Trypanosoma cruzi detection in blood samples. Acta Trop 103: 195200.
  31. Duffy T, Bisio M, Altcheh J, Burgos JM, Diez M, Levin MJ, Favaloro RR, Freilij H, Schijman AJ, , 2009. Accurate real-time PCR strategy for monitoring bloodstream parasitic loads in Chagas disease patients. PLoS Negl Trop Dis 3: e419.
  32. Yeo M, 2005. Origins of Chagas disease: didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. Int J Parasitol 35: 225233.
  33. Castillo-Riquelme M, Guhl F, Turriago B, Pinto N, Rosas F, Martínez MF, Fox-Rushby J, Davies C, Campbell-Lendrum D, , 2008. The costs of preventing and treating Chagas disease in Colombia. PLoS Negl Trop Dis 2: e336.
  34. Guhl F, Restrepo M, Angulo VM, Antunes CM, Campbell-Lendrum D, Davies CR, , 2005. Lessons from a national survey of Chagas disease transmission risk in Colombia. Trends Parasitol 21: 259262.
  35. Guhl F, Ramírez JD, , 2013. Retrospective molecular integrated epidemiology of Chagas disease in Colombia. Infect Genet Evol 20: 148154.
  36. Simmons AB, Cardona R, , 1972. Rural-urban migration: who comes, who stays, who returns? The case of Bogota, Colombia, 1929–1968. Int Migr Rev 6: 166181.
  37. Albuja S, Ceballos M, , 2010. Urban displacement and migration in Colombia. Forced Migr Rev 34: 1011.
  38. Torres-Aguilera M, Remes-Troche JM, Roesch-Dietlen F, Vázquez-Jiménez JG, De la Cruz-Patiño E, Grube-Pagola P, Ruiz-Juárez I, , 2011. Esophageal motor disorders in asymptomatic subjects con Trypanosoma cruzi infection [in Spanish]. Rev Gastroenterol Mex 76: 199208.
  39. Llano M, Pavía P, Flórez AC, Cuéllar A, González JM, Puerta C, , 2014. Preliminary evaluation of the commercial kit Chagas (Trypanosoma cruzi) IgG-ELISA® in Colombian individuals [in Spanish]. Biomedica 34: 228236.
  40. Peralta JM, Teixeira MG, Shreffler WG, Pereira JB, Burns JM, Jr Sleath PR, Reed SG, , 1994. Serodiagnosis of Chagas’ disease by enzyme-linked immunosorbent assay using two synthetic peptides as antigens. J Clin Microbiol 32: 971974.
  41. Houghton RL, Benson DR, Reynolds L, McNeill P, Sleath P, Lodes M, Skeiky YA, Badaro R, Krettli AU, Reed SG, , 2000. Multiepitope synthetic peptide and recombinant protein for the detection of antibodies to Trypanosoma cruzi in patients with treated or untreated Chagas’ disease. J Infect Dis 181: 325330.
  42. Vergara U, Veloso C, Gonzalez A, Lorca M, , 1992. Evaluation of an enzyme-linked immunosorbent assay for the diagnosis of Chagas’ disease using synthetic peptides. Am J Trop Med Hyg 46: 3943.
  43. Vergara U, Lorca M, Veloso C, Gonzalez A, Engstrom A, Aslund L, Pettersson U, Frasch AC, , 1991. Assay for detection of Trypanosoma cruzi antibodies in human sera based on reaction with synthetic peptides. J Clin Microbiol 29: 20342037.
  44. Ibañez CF, Affranchino JL, Macina RA, Reyes MB, Leguizamon S, Camargo ME, Aslund L, Pettersson U, Frasch AC, , 1988. Multiple Trypanosoma cruzi antigens containing tandemly repeated amino acid sequence motifs. Mol Biochem Parasitol 30: 2733.
  45. Primavera KS, Umezawa ES, Peres BA, Camargo ME, Hoshino-Shimizu S, , 1990. Chagas’disease: IgA, IgM and IgG antibodies to T. cruzi amastigote, trypomastigote and epimastigote antigens in acute and in different chronic forms of the disease. Rev Inst Med Trop São Paulo 32: 172180.
  46. Umezawa ES, 1999. Evaluation of recombinant antigens for serodiagnosis of Chagas’ disease in South and Central America. J Clin Microbiol 37: 15541560.
  47. Brenière SF, Waleckx E, Barnabé C, , 2016. Over six thousand Trypanosoma cruzi strains classified into discrete typing units (DTUs): attempt at an inventory. PLoS Negl Trop Dis 10: e0004792.
  48. World Health Organization, 2010. Anti-Trypanosoma Cruzi ASSAYS: Operational Characteristics, Report 1. Available at: http://apps.who.int/iris/bitstream/10665/75844/1/9789241500296_eng.pdf. Accessed January 30, 2018.
  49. da Silveira JF, Umezawa ES, Luquetti AO, , 2001. Chagas disease: recombinant Trypanosoma cruzi antigens for serological diagnosis. Trends Parasitol 17: 286291.
  50. Burns JM Jr Shreffler WG Rosman DE Sleath PR March CJ Reed SG, 1992. Identification and synthesis of a major conserved antigenic epitope of Trypanosoma cruzi. Proc Natl Acad Sci USA 89: 12391243.
  51. Hoft DF, Kim KS, Otsu K, Moser DR, Yost WJ, Blumin JH, Donelson JE, Kirchhoff LV, , 1989. Trypanosoma cruzi expresses diverse repetitive protein antigens. Infect Immun 57: 19591967.
  52. Guzmán-Gómez D, López-Monteon A, de la Soledad Lagunes-Castro M, Álvarez-Martínez C, Hernández-Lutzon MJ, Dumonteil E, Ramos-Ligonio A, , 2015. Highly discordant serology against Trypanosoma cruzi in central Veracruz, Mexico: role of the antigen used for diagnostic. Parasit Vectors 8: 466.
  53. Moure Z, 2016. Serodiscordance in chronic Chagas disease diagnosis: a real problem in non-endemic countries. Clin Microbiol Infect 22: 788792.
  54. Batista AM, Aguiar C, Almeida EA, Guariento ME, Wanderley JS, Costa SC, , 2010. Evidence of Chagas disease in seronegative Brazilian patients with megaesophagus. Int J Infect Dis 14: e974e977.
  55. Hernández C, Cucunubá Z, Flórez C, Olivera M, Valencia C, Zambrano P, León C, Ramírez JD, , 2016. Molecular diagnosis of Chagas disease in Colombia: parasitic loads and discrete typing units in patients from acute and chronic phases. PLoS Negl Trop Dis 10: e0004997.
  56. Sales-Campos H, Kappel HB, Andrade CP, Lima TP, de Castilho A, Giraldo LE, Lages-Silva E, , 2015. Trypanosoma cruzi DTU TcII presents higher blood parasitism than DTU TcI in an experimental model of mixed infection. Acta Parasitol 60: 435441.
  57. Britto C, Cardoso MA, Vanni CM, Hasslocher-Moreno A, Xavier SS, Oelemann W, Santoro A, Pirmez C, Morel CM, Wincker P, , 1995. Polymerase chain reaction detection of Trypanosoma cruzi in human blood samples as a tool for diagnosis and treatment evaluation. Parasitology 110: 241247.
  58. Gomes ML, Macedo AM, Vago AR, Pena SD, Galvão LM, Chiari E, , 1998. Trypanosoma cruzi: optimization of polymerase chain reaction for detection in human blood. Exp Parasitol 88: 2833.

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  • Received : 28 May 2017
  • Accepted : 10 Dec 2017

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