Gastroenterology
Volume 133, Issue 1 , Pages 24-33 , July 2007

The Fecal Microbiota of Irritable Bowel Syndrome Patients Differs Significantly From That of Healthy Subjects

  • Anna Kassinen

      Affiliations

    • Department of Basic Veterinary Sciences, Division of Microbiology and Epidemiology, University of Helsinki, Helsinki, Finland
  • ,
  • Lotta Krogius-Kurikka

      Affiliations

    • Department of Basic Veterinary Sciences, Division of Microbiology and Epidemiology, University of Helsinki, Helsinki, Finland
  • ,
  • Harri Mäkivuokko

      Affiliations

    • Danisco Innovation, Kantvik, Finland
  • ,
  • Teemu Rinttilä

      Affiliations

    • Department of Basic Veterinary Sciences, Division of Microbiology and Epidemiology, University of Helsinki, Helsinki, Finland
    • T.R. and J.A.’s current affiliation is Alimetrics Ltd, Helsinki, Finland.
  • ,
  • Lars Paulin

      Affiliations

    • Institute of Biotechnology, University of Helsinki, Helsinki, Finland
  • ,
  • Jukka Corander

      Affiliations

    • Department of Mathematics and Statistics, University of Helsinki, Helsinki, Finland
  • ,
  • Erja Malinen

      Affiliations

    • Department of Basic Veterinary Sciences, Division of Microbiology and Epidemiology, University of Helsinki, Helsinki, Finland
  • ,
  • Juha Apajalahti

      Affiliations

    • Danisco Innovation, Kantvik, Finland
    • T.R. and J.A.’s current affiliation is Alimetrics Ltd, Helsinki, Finland.
  • ,
  • Airi Palva

      Affiliations

    • Department of Basic Veterinary Sciences, Division of Microbiology and Epidemiology, University of Helsinki, Helsinki, Finland
    • Corresponding Author InformationAddress requests for reprints to: Airi Palva, PhD, Department of Basic Veterinary Sciences, Division of Microbiology and Epidemiology, PO Box 66, 00014 University of Helsinki, Finland. fax: (358) 9 191 57033.

Received 8 September 2006 ,Accepted 29 March 2007.

References 

  1. Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterology. 2006;130:1480–1491
  2. In:  Drossman DA,  Corazziari E,  Talley NJ,  Thompson WG,  Whitehead WE editor. Rome II: the functional gastrointestinal disorders. 2nd ed. McLean, VA: Degnon Associates; 2000;
  3. Drossman DA, Camilleri M, Mayer EA, Whitehead WE. AGA technical review on irritable bowel syndrome. Gastroenterology. 2002;123:2108–2131
  4. Mellon AF, Deshpande SA, Mathers JC, Bartlett K. Effect of oral antibiotics on intestinal production of propionic acid. Arch Dis Child. 2000;82:169–172
  5. Surawicz CM. Probiotics, antibiotic-associated diarrhoea and Clostridium difficile diarrhoea in humans. Best Pract Res Clin Gastroenterol. 2003;17:775–783
  6. Hayashi H, Sakamoto M, Benno Y. Fecal microbial diversity in a strict vegetarian as determined by molecular analysis and cultivation. Microbiol Immunol. 2002;46:819–831
  7. Bajzer M, Seeley RJ. Obesity and gut flora. Nature. 2006;444:1009–1010
  8. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–1023
  9. Wensinck F. Proceedings: the faecal flora of patients with Crohn’s disease. Antonie van Leeuwenhoek. 1975;41:214–215
  10. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, et al. Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut. 2003;52:237–242
  11. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut. 2004;53:685–693
  12. Kirjavainen PV, Apostolou E, Arvola T, Salminen SJ, Gibson GR, Isolauri E. Characterizing the composition of intestinal microflora as a prospective treatment target in infant allergic disease. FEMS Immunol Med Microbiol. 2001;32:1–7
  13. Watanabe S, Narisawa Y, Arase S, Okamatsu H, Ikenaga T, Tajiri Y, et al. Differences in fecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol. 2003;111:587–591
  14. Balsari A, Ceccarelli A, Dubini F, Fesce E, Poli G. The fecal microbial population in the irritable bowel syndrome. Microbiologica. 1982;5:185–194
  15. King TS, Elia M, Hunter JO. Abnormal colonic fermentation in irritable bowel syndrome. Lancet. 1998;352:1187–1189
  16. Rodriguez LA, Ruigomez A. Increased risk of irritable bowel syndrome after bacterial gastroenteritis: cohort study. BMJ (Clin Res Ed). 1999;318:565–566
  17. Si JM, Yu YC, Fan YJ, Chen SJ. Intestinal microecology and quality of life in irritable bowel syndrome patients. World J Gastroenterol. 2004;10:1802–1805
  18. Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, et al. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol. 1999;65:4799–4807
  19. Wilson KH, Blitchington RB. Human colonic biota studied by ribosomal DNA sequence analysis. Appl Environ Microbiol. 1996;62:2273–2278
  20. Reysenbach AL, Giver LJ, Wickham GS, Pace NR. Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol. 1992;58:3417–3418
  21. Holben WE, Harris D. DNA-based monitoring of total bacterial community structure in environmental samples. Mol Ecol. 1995;4:627–631
  22. Malinen E, Rinttilä T, Kajander K, Mättö J, Kassinen A, Krogius L, et al. Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol. 2005;100:373–382
  23. Thompson WG, Longstreth GF, Drossman DA, Heaton KW, Irvine EJ, Muller-Lissner SA. Functional bowel disorders and functional abdominal pain. Gut. 1999;45(Suppl 2):II43–II47
  24. Apajalahti JH, Särkilahti LK, Mäki BR, Heikkinen JP, Nurminen PH, Holben WE. Effective recovery of bacterial DNA and percent-guanine-plus-cytosine-based analysis of community structure in the gastrointestinal tract of broiler chickens. Appl Environ Microbiol. 1998;64:4084–4088
  25. Holben WE, Jansson JK, Chelm BK, Tiedje JM. DNA probe method for the detection of specific microorganisms in the soil bacterial community. Appl Environ Microbiol. 1988;54:703–711
  26. Hicks RE, Amann RI, Stahl DA. Dual staining of natural bacterioplankton with 4′,6-diamidino-2-phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16S rRNA sequences. Appl Environ Microbiol. 1992;58:2158–2163
  27. Wang RF, Kim SJ, Robertson LH, Cerniglia CE. Development of a membrane-array method for the detection of human intestinal bacteria in fecal samples. Mol Cell Probes. 2002;16:341–350
  28. Edwards U, Rogall T, Blocker H, Emde M, Bottger EC. Isolation and direct complete nucleotide determination of entire genes (Characterization of a gene coding for 16S ribosomal RNA). Nucleic Acids Res. 1989;17:7843–7853
  29. Staden R, Beal KF, Bonfield JK. In: The Staden package, 1998 (Methods in molecular biology). Clifton, NJ: The Humana Press Inc., Totowa; 2000;p. 115–130132
  30. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, et al. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003;31:3497–3500
  31. Schloss PD, Handelsman J. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol. 2005;71:1501–1506
  32. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988;85:2444–2448
  33. Cole JR, Chai B, Farris RJ, Wang Q, Kulam SA, McGarrell DM, et al. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res. 2005;33:D294–D296
  34. Schloss PD, Larget BR, Handelsman J. Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol. 2004;70:5485–5492
  35. Corander J, Tang J. Bayesian analysis of population structure based on linked molecular information. Math Biosci. 2007;205:19–31
  36. Good IJ. The population frequencies of species and the estimation of population parameters. Biometrika. 1953;237–264
  37. Seber GAF. Multivariate observations. Mississauga, Canada: Wiley; 1984;
  38. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar , et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–1371
  39. Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology. 2002;148:257–266
  40. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307:1915–1920
  41. Apajalahti JH, Kettunen H, Kettunen A, Holben WE, Nurminen PH, Rautonen N, et al. Culture-independent microbial community analysis reveals that inulin in the diet primarily affects previously unknown bacteria in the mouse cecum. Appl Environ Microbiol. 2002;68:4986–4995
  42. Apajalahti JH, Kettunen A, Nurminen PH, Jatila H, Holben WE. Selective plating underestimates abundance and shows differential recovery of bifidobacterial species from human feces. Appl Environ Microbiol. 2003;69:5731–5735
  43. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–1638
  44. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124:837–848
  45. Hayashi H, Sakamoto M, Benno Y. Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiol Immunol. 2002;46:535–548
  46. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444:1027–1131
  47. Benno Y, Endo K, Mizutani T, Namba Y, Komori T, Mitsuoka T. Comparison of fecal microflora of elderly persons in rural and urban areas of Japan. Appl Environ Microbiol. 1989;55:1100–1105
  48. Moore WE, Moore LH. Intestinal floras of populations that have a high risk of colon cancer. Appl Environ Microbiol. 1995;61:3202–3207
  49. Verdu EF, Collins SM. Irritable bowel syndrome and probiotics: from rationale to clinical use. Curr Opin Gastroenterol. 2005;21:697–701
  50. Kajander K, Hatakka K, Poussa T, Färkkilä M, Korpela R. A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment Pharmacol Ther. 2005;22:387–394
  51. Kim HJ, Vazquez Roque MI, Camilleri M, Stephens D, Burton DD, Baxter K, et al. A randomized controlled trial of a probiotic combination VSL# 3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil. 2005;17:687–696
  52. Mättö J, Maunuksela L, Kajander K, Palva A, Korpela R, Kassinen A, et al. Composition and temporal stability of gastrointestinal microbiota in irritable bowel syndrome—a longitudinal study in IBS and control subjects. FEMS Immunol Med Microbiol. 2005;43:213–222
  53. Maukonen J, Satokari R, Mättö J, Söderlund H, Mattila-Sandholm T, Saarela M. Prevalence and temporal stability of selected clostridial groups in irritable bowel syndrome in relation to predominant faecal bacteria. J Med Microbiol. 2006;55:625–633

 The authors have no conflicts of interest to disclose.Supported by the Finnish Funding Agency for Technology and Innovation (Tekes), Finnish Graduate School of Applied Biosciences.

PII: S0016-5085(07)00734-2

doi: 10.1053/j.gastro.2007.04.005

Gastroenterology
Volume 133, Issue 1 , Pages 24-33 , July 2007