Digestive Diseases and Sciences

, Volume 50, Issue 4, pp 758–766 | Cite as

Do Interventions Which Reduce Colonic Bacterial Fermentation Improve Symptoms of Irritable Bowel Syndrome?

  • Keith L. E. Dear
  • Marinos Elia
  • John O. Hunter
Article

Abstract

Abnormal fermentation may be an important factor in irritable bowel syndrome (IBS). Gastroenteritis or antibiotic therapy may damage the colonic microflora, leading to increased fermentation and the accumulation of gas. Gas excretion may be measured by whole-body calorimetry but there has only been one such study on IBS to date. We aimed to assess the relationship between IBS symptoms and fermentation rates in IBS. A purpose-built, 1.4-m3, whole-body calorimeter was used to assess excretion of H2 and CH4 in IBS subjects while consuming a standard diet and, again, after open randomization on either the standard diet together with the antibiotic metronidazole or a fiber-free diet to reduce fermentation. Metronidazole significantly reduced the 24-hr excretion of hydrogen (median value compared to the control group, 397 vs 230 ml/24 hr) and total gas (H2 + CH4; 671 vs 422 ml/min) and the maximum rate of gas excretion (1.6 vs 0.8 ml/min), as did a no-fiber polymeric diet (hydrogen, 418 vs 176 ml/min; total gas, 564 vs 205 ml/min; maximum rate of gas excretion, 1.35 vs 0.45 ml/min), with a significant improvement in abdominal symptoms. IBS may be associated with rapid excretion of gaseous products of fermentation, whose reduction may improve symptoms.

Keywords

irritable bowel syndrome bacterial fermentation antibiotics enteral feeds calorimetry hydrogen methane 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Thompson WG, Heaton KW: Functional bowel disorders in apparently healthy people. Gastroenterology 79:283–288, 1980PubMedGoogle Scholar
  2. 2.
    Jones R, Lydeard S: Irritable bowel syndrome in the general population. BMJ 304:87–90, 1992PubMedCrossRefGoogle Scholar
  3. 3.
    Drossman DA, Sandler RS, McKee DC, Lovitz AJ: Bowel patterns among subjects not seeking health care: Use of a questionnaire to identify a population with bowel dysfunction. Gastroenterology 83:529–534, 1982PubMedGoogle Scholar
  4. 4.
    Alun Jones V, Wilson AJ, Hunter JO, Robinson RE: The aetiological role of antibiotic prophylaxis with hysterectomy in irritable bowel syndrome. J Obstet Gynaecol 5:522–523, 1984CrossRefGoogle Scholar
  5. 5.
    Maxwell PR, Rink E, Kumar D, Mendall MA: Antibiotics increase functional abdominal symptoms. Am J Gastro 97:104–108, 2002CrossRefGoogle Scholar
  6. 6.
    McKendrick MW, Read NW: Irritable bowel syndrome: Post Salmonella infection. J Infect 29:1–3, 1994PubMedCrossRefGoogle Scholar
  7. 7.
    Neal KR, Hebden J, Spiller R: Prevalence of gastrointestinal symptoms six months after bacterial gastroenteritis and risk factors for development of the irritable bowel syndrome: postal survey of patients. BMJ 314:779–782, 1997PubMedGoogle Scholar
  8. 8.
    Garcìa Rodrìguez LA, Ruigómez A: Increased risk of irritable bowel syndrome after bacterial gastroenteritis: cohort study. BMJ 318:565–566, 1999Google Scholar
  9. 9.
    Balsari A, Ceccarelli A, Dubin F, Fosce E, Poli G: The faecal micobial population in the irritable bowel syndrome Microbiologica 5:189–194, 1908Google Scholar
  10. 10.
    Bradley HK, Wyatt GM, Bayliss CE, Hunter JO: Instability of the faecal flora of a patient suffering from food-related irritable bowel syndrome. J Med Microbiol 23:29–32, 1987PubMedGoogle Scholar
  11. 11.
    Moore WE, Cato EP, Good IJ, Holderman LV: The effect of diet on the human faecal flora. In Bruce WR, et al. (eds). Banbury Report 7: Gastrointestinal Cancer; Endogenous Factors. Cold Spring Harbor, NY, Cold Spring Harbor Laboratory, 1981, pp 11–24Google Scholar
  12. 12.
    Bentley SJ, Pearson DJ, Rix KJ: Food hypersensitivity in irritable bowel syndrome. Lancet ii:295–297, 1983CrossRefGoogle Scholar
  13. 13.
    Nanda R, James R, Smith H, Dudley CRK, Jewell DP: Food intolerance and the irritable bowel syndrome. Gut 30:1099–1104, 1989PubMedCrossRefGoogle Scholar
  14. 14.
    Parker TJ, Naylor SJ, Riordan AM, Hunter JO: Management of patients with food intolerance in the irritable bowel syndrome: the development and use of an exclusion diet. J Hum Nutr Diet 8:159–166, 1995CrossRefGoogle Scholar
  15. 15.
    Wyatt GM, Bayliss CE, Lakey AF, Bradley HK, Hunter JO, Alun-Jones V: The faecal flora of two patients with food intolerant irritable bowel syndrome during challenge with symptom-provoking foods. J Med Micobiol 26:295–299Google Scholar
  16. 16.
    Argenzio RA, Meuten DJ: Short-chain fatty acids induce reversible injury of porcine colon. Dig Dis Sci 36:1459–1468, 1991PubMedCrossRefGoogle Scholar
  17. 17.
    Murray KE, Adams RF, Early JW, Shaw KJ: Studies of the free faecal amines of infants with gastroenteritis and of healthy infants. Gut 27:1173–1180, 1986PubMedCrossRefGoogle Scholar
  18. 18.
    Gibson GR, Macfarlane GT, Cummings JH: Sulphate reducing bacteria and hydrogen metabolism in the human large intestine. Gut 34:437–439, 1993PubMedCrossRefGoogle Scholar
  19. 19.
    Serra J, Fernando A, Malagelada JR: Intestinal gas dynamics and tolerance in humans. Gastroenterology 115:542–550, 1998PubMedCrossRefGoogle Scholar
  20. 20.
    Christl SU, Murgatroyd PR, Gibson G, Cummings JH: Production, metabolism and excretion of hydrogen in the large intestine. Gastroenterology 102:1269–1277, 1992PubMedGoogle Scholar
  21. 21.
    King TS, Elia M, Hunter JO: Abnormal colonic fermentation in irritable bowel syndrome. Lancet 352:1187–1189, 1998PubMedCrossRefGoogle Scholar
  22. 22.
    Thompson KW, Dotevall G, Drossman D, Heaton KW, Kruis W: Irritable bowel syndrome: guidelines for the diagnosis. Report of the Rome working team. Gastroenterol Int 2:92–95, 1989Google Scholar
  23. 23.
    Kane SV, Sable K, Hanauer SB: The menstrual cycle and its effect on inflammatory bowel disease and irritable bowel disease: A prevalence study. Am J Gastroenterol 10:1867–1872, 1998CrossRefGoogle Scholar
  24. 24.
    Schofield WN: Predicting basal metabolic rate, new standards and review of previous work. Hum Nutr Clin Nutr 39C:5–41, 1985Google Scholar
  25. 25.
    Wells CL, Jechore RP, Maddaus MA, Simmons RL: Effect of clindamycin and metronidazole on the intestinal colonisation and translocation of enterococci in mice. Antimicrob Agents Chemother 32:1769–1775, 1988PubMedGoogle Scholar
  26. 26.
    Lembcke B, Honig M, Caspray WF: Different actions of neomycin metronidazole on breath hydrogen (H2) exhalation. Gastroenterologie 18:155–160, 1980Google Scholar
  27. 27.
    King TS, Hunter JO: Do symptoms improve with quality of life in I.B.S.? Gut 40(Suppl 1):64, 1997 (abstr)Google Scholar
  28. 28.
    El Oufir L, Flourié B, Bruley des Varannes S, Barry L, Cloarec D, Bornet F, Galmiche JP: Relations between transit time, fermentation products, and hydrogen consuming flora in healthy humans. Gut 38:870–877, 1996PubMedCrossRefGoogle Scholar
  29. 29.
    Fotherby GJ, Hunter JO: Idiopathic slow transit constipation: Whole gut transit times measured by a new simplified method, are not shortened by opiate antagonists. Alim Pharmacol Ther 1:331–338, 1987CrossRefGoogle Scholar
  30. 30.
    Brown D, Cole TJ, Dauncey MJ, Marrs RW, Murgatroyd PR: Analysis of gaseous exchange in open circuit indirect calorimetry. Med Biol Eng Comput 22:333–338, 1984PubMedCrossRefGoogle Scholar
  31. 31.
    Bjorneklett A, Jenssen F: Relationship between hydrogen (H2) and methane (CH4) production in man. Scand J Gastroenterol 17:985–992, 1982PubMedGoogle Scholar
  32. 32.
    Francis CY, Whorwell PJ: Bran and irritable bowel syndrome: time for reappraisal. Lancet 344:39–40, 1994PubMedCrossRefGoogle Scholar
  33. 33.
    Levitt MD, Levitt DG: Use of inert gases to study the interaction of blood flow and diffusion during passive absorption from the gastrointestinal tract of the rat. J Clin Invest 52:1852–1862, 1973PubMedCrossRefGoogle Scholar
  34. 34.
    Accarino AM, Azpiroz F, Malagelada JR: Selective dysfunction of mechanosensitive intestinal afferents in irritable bowel syndrome. Gastroenterology 108:636–643, 1995PubMedCrossRefGoogle Scholar
  35. 35.
    Munakata J, Naliboff B, Harraf F, Kodner A, Lembo T, Chang L, Silverman DHS, Mayer AE: Repetitive sigmoid stimulation induces rectal hyperalgesia in patients with irritable bowel syndrome. Gastroenterology 112:55–63, 1997PubMedCrossRefGoogle Scholar
  36. 36.
    Lasser RB, Bond JH, Levitt MD: The role of intestinal gas in functional abdominal pain. N Engl J Med 293:524–526, 1975PubMedCrossRefGoogle Scholar
  37. 37.
    Chami TN, Schuster MM, Bolham ME, Pulliam TJ, Kamal N, Whitehead WE: A simple radiological method to estimate the quantity of bowel gas. Am J Gastroenterol 86:599–602, 1991PubMedGoogle Scholar
  38. 38.
    Levitt MD, Hirsh P, Fetzer CA, Sheahan M, Levine AS: H2 excretion after ingestion of complex carbohydrates. Gastroenterology 92:383–389, 1986Google Scholar
  39. 39.
    Haderstorfer B, Whitehead WE, Schuster MM: Intestinal gas production from bacterial fermentation of undigested carbohydrate in irritable bowel syndrome. Am J Gastroenterol 84:375–378, 1989PubMedGoogle Scholar
  40. 40.
    Spiller RC: Problems and challenges in the design of irritable bowel syndrome clinical trials: experience from published trials. Am J Med 107:91S–97S, 1999PubMedCrossRefGoogle Scholar
  41. 41.
    Holderman LV, Good IJ, Moore WEC: Human faecal flora: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl Environ Microbiol 31:359–375, 1976Google Scholar
  42. 42.
    Bradley HK, Wyatt GM, Bayliss CE, Hunter JO: Instability in the faecal flora of a patient suffering from food-related irritable bowel syndrome. J Med Microbiol 23:29–32, 1987PubMedCrossRefGoogle Scholar
  43. 43.
    Ng W, Tonzetich J: Effect of hydrogen sulphide and methyl mercaptan on the permeability of oral mucosa. J Dent Res 63:994–997, 1984PubMedGoogle Scholar
  44. 44.
    Aslam M, Batten JJ, Florin THJ, Sidebotham RL, Baron JH: Hydrogen sulphide-induced damage to the colonic mucosal barrier in the rat. Gut 33:S69, 1992Google Scholar
  45. 45.
    Ahlman B, Leijonmarck CE, Lind C, Vinnars E, Wernerman J: Free amino acids in biopsy specimens from the human colonic mucosa. J Surg Res 55:647–653, 1993PubMedCrossRefGoogle Scholar
  46. 46.
    Snape WJ, Yoo S: Effect of amino-acids on isolated colonic smooth muscle from the rabbit. J Pharmacol Exp Ther 235:690–695, 1985PubMedGoogle Scholar
  47. 47.
    Painter NS: Bran and the irritable bowel syndrome. Lancet i:540, 1976CrossRefGoogle Scholar
  48. 48.
    Manning AP, Heaton KW, Harvey RF, Uglow P: Wheat fibre and irritable bowel syndrome. Lancet ii: 417–418, 1977CrossRefGoogle Scholar
  49. 49.
    Gibson GR, Cummings JH, Macfarlane GT, Allison C, Segal I, Vorter HH, Walker ARP: Alternative pathways for hydrogen disposal during fermentation in the human colon. Gut 31:679–683, 1990PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Keith L. E. Dear
    • 1
  • Marinos Elia
    • 2
  • John O. Hunter
    • 1
    • 3
  1. 1.Department of GastroenterologyAddenbrooke’s Hospital NHS TrustCambridge
  2. 2.Institute of Human NutritionUniversity of SouthamptonSouthamptonUK
  3. 3.CambridgeUK

Personalised recommendations