Advertisement

Parasitology Research

, Volume 110, Issue 3, pp 1269–1275 | Cite as

Blastocystis infection is associated with irritable bowel syndrome in a Mexican patient population

  • Diego Emiliano Jimenez-Gonzalez
  • Williams Arony Martinez-Flores
  • Jesus Reyes-Gordillo
  • Maria Elena Ramirez-Miranda
  • Sara Arroyo-Escalante
  • Mirza Romero-Valdovinos
  • Damien Stark
  • Valeria Souza-Saldivar
  • Fernando Martinez-Hernandez
  • Ana Flisser
  • Angelica Olivo-Diaz
  • Pablo MaravillaEmail author
Original Paper

Abstract

In recent times, some common “non-pathogenic” parasites, such as Blastocystis and Dientamoeba fragilis, have been associated to the aetiology of irritable bowel syndrome (IBS), while host pro-inflammatory cytokine gene polymorphisms might have a role in the pathophysiology of the disease. Therefore, Blastocystis subtypes (ST), D. fragilis and gene promoter single nucleotide polymorphisms of interleukin-6 (IL-6) and tumour necrosis factor-alpha (TNF-α) in IBS patients and controls were studied. After giving written consent, 45 patients with symptoms of IBS according to the Rome III criteria and 45 controls were enrolled. DNA was extracted from peripheral blood for SNP analysis at position -174 for IL-6 as well as -238 and -308 for TNF-α. Blastocystis was more common in the IBS group (p = 0.043). Interestingly, D. fragilis was found more frequently in the control group (p = 0.002); Blastocystis ST1 and 3 were most frequent in both groups. Haploview analysis revealed linkage disequilibrium in TNF-α (p < 0.0001); however, none of the SNPs for IL-6 and TNF-α were found to be significantly related with IBS. The clinical and molecular approaches undertaken for the first time in Latin American IBS patients demonstrated an association with Blastocystis that supports a pathogenic role of this parasite in IBS Furthermore, co-infections with ST1 and ST3 were frequent; thus, the genetic diversity proposed within ST polymorphisms does not rule out that particular strains might be associated with disease. In addition, our results do not support a major contribution of IL-6 and TNF-α gene polymorphisms in the susceptibility to IBS.

Keywords

Irritable Bowel Syndrome Irritable Bowel Syndrome Patient Schistosoma Haematobium Mexican Patient Blastocystis Infection 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors would like to thank Rune Stensvold for his critical comments; Maria Elena Rodriguez-Campa, Alberto Gonzalez-Angulo, Jesus Lopez-Olivera, Joel Martinez-Ocaña, Simon Kawa-Karasik, David Moncada-Barron, Humberto Torres-Pinzon, Maria de Lourdes Puga, Leonor Escobedo-Ramos, Eduardo Lopez-Escamilla, Lucia Guerra-Sanchez, Rocio Jimenez-Lucio and David Sierra performed colonoscopies, obtained biopsies and undertook routine pathogen identification. This study is part of DEJG Master's studies in the Facultad de Ciencias, Universidad Nacional Autonoma de Mexico. This work was supported by CONACYT grant 69,589.

References

  1. Agnew-Blais J, Carnevale J, Gropper A, Shilika E, Bail R, Ngoma M (2010) Schistosomiasis haematobium prevalence and risk factors in a school-age population of peri-urban Lusaka, Zambia. J Trop Pediatr 56:247–253PubMedCrossRefGoogle Scholar
  2. Barkhordari E, Rezaei N, Ansaripour B, Larki P, Alighardashi M, Ahmadi-Ashtiani HR, Mahmoudi M, Keramati MR, Habibollahi P, Bashashati M, Ebrahimi-Daryani N, Amirzargar AA (2010a) Proinflamatory cytokine gene polymorphisms in irritable bowel syndrome. J Clin Immunol 30:74–79PubMedCrossRefGoogle Scholar
  3. Barkhordari E, Rezaei N, Mahmoudi M, Larki P, Ahmadi-Ashtiani HR, Ansaripour B, Alighardashi M, Bashashati M, Amirzargar AA, Ebrahimi-Daryani N (2010b) T-helper 1, T-helper 2, and T-regulatory cytokines gene polymorphisms in irritable bowel syndrome. Inflammation 33:281–286PubMedCrossRefGoogle Scholar
  4. Boorom KF, Smith H, Nimri L, Viscogliosi E, Spanakos G, Parkar U, Li LH, Zhou XN, Ok UZ, Leelayoova S, Jones MS (2008) Oh my aching gut: irritable bowel syndrome, Blastocystis, and asymptomatic infection. BMC Parasit Vectors 1:40CrossRefGoogle Scholar
  5. Camarena A, Juárez A, Mejía M, Estrada A, Carrillo G, Falfán R, Zuñiga J, Navarro C, Granados J, Selman M (2001) Major histocompatibility complex and tumor necrosis factor-α polymorphisms in pigeon Breeder's disease. Am J Respir Crit Care Med 163:1528–1533PubMedGoogle Scholar
  6. Dogruman-Al F, Dagci H, Yoshikawa H, Kurt O, Demirel M (2008) A possible link between subtype 2 and asymptomatic infections of Blastocystis hominis. Parasitol Res 103:685–689PubMedCrossRefGoogle Scholar
  7. Fajardo-Dolci G, Solorio-Abreu J, Romero-Alvarez JC, Zavaleta-Villa B, Cerezo-Camacho O, Jiménez-Lucio R, Olivo-Díaz A (2006) DQA1 and DQB1 association and nasal polyposis. Otolaryngol Head Neck Surg 135:243–247PubMedCrossRefGoogle Scholar
  8. Fishman D, Faulds G, Jeffery R, Mohamed-Ali V, Yudkin JS, Humphries S, Woo P (1998) The effect of novel polymorphisms in the interleukin-6 (IL-6) gene on IL-6 transcription and plasma IL-6 levels, and an association with systemic-onset juvenile chronic arthritis. J Clin Invest 102:1369–1376PubMedCrossRefGoogle Scholar
  9. Gasbarrini A, Lauritano EC, Garcovich M, Sparano L, Gasbarrini G (2008) New insights into the pathophysiology of IBS: intestinal microflora, gas production and gut motility. Eur Rev Med Pharmacol Sci 12(Suppl 1):111–117PubMedGoogle Scholar
  10. Glantz SA (1992) Primer of biostatistics: the program v 3.01. McGraw-Hill, ColumbusGoogle Scholar
  11. Guimaráes S, Sogayar MI (1993) Blastocystis hominis: occurrence in children and staff members of municipal day-care centers from Botucatu, Sáo Paulo State, Brazil. Mem Inst Oswaldo Cruz 88:427–429PubMedCrossRefGoogle Scholar
  12. Heesen M, Kunz D, Bachmann-Mennenga MHF, Bloemeke B (2003) Linkage disequilibrium between tumor necrosis factor (TNF)-alpha-308 G/A promoter and TNF-beta NcoI polymorphisms: association with TNF-alpha response of granulocyte to endotoxin stimulation. Crit Care Med 31:211–214PubMedCrossRefGoogle Scholar
  13. INEGI, Instituto Nacional de Estadística y Geografía, Anuario estadístico de los Estados Unidos Mexicanos 2010. http://www.inegi.org.mx/. Accessed 30 June 2011.
  14. Li LH, Zhou XN, Du ZW, Wang XZ, Wang LB, Jiang JY, Yoshikawa H, Steinmann P, Utzinger J, Wu Z, Chen JX, Chen SH, Zhang L (2007a) Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitol Int 56:281–286PubMedCrossRefGoogle Scholar
  15. Li LH, Zhang XP, Lv S, Zhang L, Yoshikawa H, Wu Z, Steinmann P, Utzinger J, Tong XM, Chen SH, Zhou XN (2007b) Cross-sectional surveys and subtype classification of human Blastocystis isolates from four epidemiological settings in China. Parasitol Res 102:83–90PubMedCrossRefGoogle Scholar
  16. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC (2006) Functional bowel disorders. Gastroenterology 130:1480–1491PubMedCrossRefGoogle Scholar
  17. Meenagh A, Williams F, Ross OA, Patterson C, Gorodezky C, Hammond LWA, Middleton D (2002) Frequency of cytokine polymorphisms in populations from Western Europe, Africa, Asia, the Middle East and South America. Hum Immunol 63:1055–1061PubMedCrossRefGoogle Scholar
  18. Melk A, Henne T, Kollmar T, Strehlau J, Latta K, Offner G, Jhangri GS, Ehrich JH, Von Schnakenburg C (2003) Cytokine single nucleotide polymorphisms and intrarenal gene expression in chronic allograft nephropathy in children. Kidney Int 64:314–320PubMedCrossRefGoogle Scholar
  19. Mendoza-Carrera F, Ramírez-López G, Ayala Martínez NA, García-Zapién AG, Flores-Martínez SE, Sánchez-Corona J (2010) Influence of CRP, IL6, and TNFA gene polymorphisms on circulating levels of C-reactive protein in Mexican adolescents. Arch Med Res 41:472–477PubMedCrossRefGoogle Scholar
  20. Minton EJ, Smillie D, Smith P, Shipley S, McKendrick MW, Gleeson DC, Underwood JC, Cannings C, Wilson AG, Trent Hepatitis C Study Group (2005) Clearance of hepatitis C virus is not associated with single nucleotide polymorphisms in the IL-1, -6, or −10 genes. Hum Immunol 66:127–132PubMedCrossRefGoogle Scholar
  21. Ramirez-Miranda ME, Hernandez-Castellanos R, Lopez-Escamilla E, Moncada D, Rodriguez-Magallan A, Pagaza-Melero C, Gonzalez-Angulo A, Flisser A, Kawa-Karasik S, Maravilla P (2010) Parasites in Mexican patients with irritable bowel syndrome: a case-control study. BMC Parasit Vectors 3:96CrossRefGoogle Scholar
  22. Rodriguez E, Mateos B, Gonzalez JC, Aguilar YM, Alarcon E, Mendoza AA, Mier M, Mora MA, Bernal R (2008) Transicion parasitaria a Blastocystis hominis en niños de la zona centro del estado de Guerrero, Mexico. Parasitol Latinoam 63:20–28CrossRefGoogle Scholar
  23. Saito YA, Petersen GM, Larson JJ, Atkinson EJ, Fridley BL, de Andrade M, Locke GR 3rd, Zimmerman JM, Almazar-Elder AE, Talley NJ (2010) Familial aggregation of irritable bowel syndrome: a family case-control study. Am J Gastroenterol 105:833–841PubMedCrossRefGoogle Scholar
  24. Sambrook J, Fitsch EF, Maniatis T (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  25. Schaneider S, Roessli D, Excoffier L (2000) ARLEQUIN Version 2.000. A software for population genetics data analysis. University of Geneva, SwitzerlandGoogle Scholar
  26. Schmulson M, Vargas JA, López-Colombo A, Remes-Troche JM, López-Alvarenga JC (2010) Prevalencia y caracterización de los subtipos de SII según los criterios de Roma III, en un estudio clínico, multicéntrico. Reporte del grupo mexicano de estudio para el SII Rev Gastroenterol Mex 75:427–438Google Scholar
  27. Shamsuzzaman SM, Hashiguchi Y (2002) Throracic amebiasis. Clin Chest Med 23:479–492PubMedCrossRefGoogle Scholar
  28. Spiegel BM, Farid M, Esrailian E, Talley J, Chang L (2010) Is irritable bowel syndrome a diagnosis of exclusion?: a survey of primary care providers, gastroenterologists, and IBS experts. Am J Gastroenterol 105:848–858PubMedCrossRefGoogle Scholar
  29. Stark D, Beebe N, Marriott D, Ellis J, Harkness J (2005) Detection of D. fragilis in fresh stool specimens using PCR. Int J Parasitol 35:57–62PubMedCrossRefGoogle Scholar
  30. Stark D, van Hal S, Marriott D, Ellis J, Harkness J (2007) Irritable bowel syndrome: a review on the role of intestinal protozoa and the importance of their diagnosis. Int J Parasitol 37:11–20PubMedCrossRefGoogle Scholar
  31. Stark D, Barratt J, Roberts T, Marriott D, Harkness J, Ellis J (2010) A review of the clinical presentation of dientamoebiasis. Am J Trop Med Hyg 82:614–619PubMedCrossRefGoogle Scholar
  32. Stayoussef M, Benmansour J, Al-Jenaidi FA, Rajab MH, Said HB, Ourtani M, Rayana CB, Mahjoub T, Almawi WY (2010) Identification of specific tumor necrosis factor-α-susceptible and -protective haplotypes associated with the risk of type 1 diabetes. Eur Cytokine Netw 21:285–291PubMedGoogle Scholar
  33. Stensvold R, Brillowska-Dabrowska A, Nielsen HV, Arendrup MC (2006) Detection of Blastocystis hominis in unpreserved stool specimens by using polymerase chain reaction. J Parasitol 92:1081–1087PubMedCrossRefGoogle Scholar
  34. Stensvold CR, Suresh GK, Tan KS, Thompson RC, Traub RJ, Viscogliosi E (2007) Terminology for Blastocystis subtypes—a consensus. Trends Parasitol 23:93–96PubMedCrossRefGoogle Scholar
  35. Stensvold CR, Nielsen HV, Mølbak K, Smith HV (2009a) Pursuing the clinical significance of Blastocystis–diagnostic limitations. Trends Parasitol 25:23–29PubMedCrossRefGoogle Scholar
  36. Stensvold CR, Lewis HC, Hammerum AM, Porsbo LJ, Nielsen SS, Olsen KE, Arendrup MC, Nielsen HV, Mølbak K (2009b) Blastocystis: unravelling potential risk factors and clinical significance of a common but neglected parasite. Epidemiol Infect 137:1655–1663PubMedCrossRefGoogle Scholar
  37. Stensvold CR, Alfellani MA, Nørskov-Lauritsen S, Prip K, Victory EL, Maddox C, Nielsen HV, Clark CG (2009c) Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. Int J Parasitol 39:473–479PubMedCrossRefGoogle Scholar
  38. Tan KS (2008) New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 21:639–665PubMedCrossRefGoogle Scholar
  39. Thompson WG, Heaton KW, Smyth GT, Smyth C (2000) Irritable bowel syndrome in general practice: prevalence, characteristics and referral. Gut 46:78–82PubMedCrossRefGoogle Scholar
  40. van der Veek PP, van den Berg M, de Kroon YE, Verspaget HW, Masclee AA (2005) Role of tumor necrosis factor-alpha and interleukin-10 gene polymorphisms in irritable bowel syndrome. Am J Gastroenterol 100:2510–2516PubMedCrossRefGoogle Scholar
  41. Yakoob J, Jafri W, Jafri N, Khan R, Islam M, Beg MA, Zaman V (2004) Irritable bowel syndrome: in search of an etiology: role of Blastocystis hominis. Am J Trop Med Hyg 70:383–385PubMedGoogle Scholar
  42. Yakoob J, Jafri W, Beg MA, Abbas Z, Naz S, Islam M, Khan R (2010a) Blastocystis hominis and D. fragilis in patients fulfilling irritable bowel syndrome criteria. Parasitol Res 107:679–684PubMedCrossRefGoogle Scholar
  43. Yakoob J, Jafri W, Beg MA, Abbas Z, Naz S, Islam M, Khan R (2010b) Irritable bowel syndrome: associated with genotypes of Blastocystis hominis. Parasitol Res 106:1033–1038PubMedCrossRefGoogle Scholar
  44. Yan Y, Su S, Lai R, Liao H, Ye J, Li X, Luo X, Chen G (2006) Genetic variability of Blastocystis hominis isolates in China. Parasitol Res 99:597–601PubMedCrossRefGoogle Scholar
  45. Yoshikawa H, Abe N, Iwasawa M, Kitano S, Nagano I, Wu Z, Takahashi Y (2000) Genomic analysis of Blastocystis hominis strains isolated from two long-term health care facilities. J Clin Microbiol 38:1324–1330PubMedGoogle Scholar
  46. Yoshikawa H, Abe N, Wu Z (2003) Genomic polymorphism among Blastocystis isolates and development of PCR-based identification of zoonotic isolates. J Eukaryot Microbiol 50(Suppl):710–711PubMedCrossRefGoogle Scholar
  47. Yoshikawa H, Wu Z, Kimata I, Iseki M, Ali IK, Hossain MB, Zaman V, Haque R, Takahashi Y (2004a) Polymerase chain reaction based subtype classification among human Blastocystis hominis populations isolated from different countries. Parasitol Res 92:22–29PubMedCrossRefGoogle Scholar
  48. Yoshikawa H, Morimoto K, Wu Z, Singh M, Hashimoto T (2004b) Problems in speciation in the genus Blastocystis. Trends Parasitol 20:251–255PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Diego Emiliano Jimenez-Gonzalez
    • 1
  • Williams Arony Martinez-Flores
    • 1
  • Jesus Reyes-Gordillo
    • 1
  • Maria Elena Ramirez-Miranda
    • 1
  • Sara Arroyo-Escalante
    • 2
  • Mirza Romero-Valdovinos
    • 1
  • Damien Stark
    • 3
  • Valeria Souza-Saldivar
    • 4
  • Fernando Martinez-Hernandez
    • 1
  • Ana Flisser
    • 5
  • Angelica Olivo-Diaz
    • 1
  • Pablo Maravilla
    • 1
    Email author
  1. 1.Hospital General “Dr. Manuel Gea Gonzalez”, Direccion de InvestigacionMexicoMexico
  2. 2.Hospital General “Dr. Manuel Gea Gonzalez”, Laboratorio ClinicoMexicoMexico
  3. 3.Department of MicrobiologySt.Vincent’s HospitalDarlinghurstAustralia
  4. 4.Instituto de EcologiaUniversidad Nacional Autonoma de MexicoMexicoMexico
  5. 5.Departamento de Microbiologia y Parasitologia, Facultad de MedicinaUniversidad Nacional Autonoma de MexicoMexicoMexico

Personalised recommendations