Advertisement

Digestive Diseases and Sciences

, Volume 55, Issue 8, pp 2135–2143 | Cite as

Methane and the Gastrointestinal Tract

  • Ara B. Sahakian
  • Sam-Ryong Jee
  • Mark Pimentel
Review

Abstract

Introduction

Several gases are produced through enteric fermentation in the intestinal tract. Carbon dioxide, hydrogen, hydrogen sulfide, and methane are thought to be the most common of these. Recent evidence suggests that methane may not be inert. In this review article, we summarize the findings with methane.

Methods

This is a review article discussing the various component gases in the gastrointestinal tract and their relevance to health and disease. Specific attention was paid to understanding methane.

Results

The majority of these gases are eliminated via flatus or absorbed into systemic circulation and expelled from the lungs. Excessive gas evacuation or retention causes gastrointestinal functional symptoms such as belching, flatulence, bloating, and pain. Between 30 and 62% of healthy subjects produce methane. Methane is produced exclusively through anaerobic fermentation of both endogenous and exogenous carbohydrates by enteric microflora in humans. Methane is not utilized by humans, and analysis of respiratory methane can serve as an indirect measure of methane production. Recent literature suggests that gases such as hydrogen sulfide and methane may have active effects on gut function. In the case of hydrogen sulfide, evidence demonstrates that this gaseous product may be produced by human eukaryotic cells. However, in the case of methane, there is increasing evidence that this gas has both physical and biological effects on gut function. It is now often associated with functional constipation and may have an active role here.

Conclusion

This review of the literature discusses the significance of enteric flora, the biogenesis of methane, and its clinical associations. Furthermore, we examine the evidence for an active role of methane in gastrointestinal motility and the potential applications to future therapeutics.

Keywords

Methane Methanogenic flora Intestinal gas Gastrointestinal motility 

References

  1. 1.
    Savage D. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–133. doi: 10.1146/annurev.mi.31.100177.000543.CrossRefPubMedGoogle Scholar
  2. 2.
    Simon GL, Gorbach SL. Intestinal flora in health and disease. Gastroenterology. 1984;86:174–193.PubMedGoogle Scholar
  3. 3.
    Cummings JH. Fermentation in the human large intestine: evidence and implications for health. Lancet. 1983;1:1206–1209. doi: 10.1016/S0140-6736(83)92478-9.CrossRefPubMedGoogle Scholar
  4. 4.
    Strocchi A, Levitt MD. Maintaining intestinal H2 balance: credit the colonic bacteria. Gastroenterology. 1992;102:1424–1426.PubMedGoogle Scholar
  5. 5.
    Wang R. Two’s company, three’s a crowd: can H2S be the third endogenous transmitter? FASEB. 2002;16:1792–1798. doi: 10.1096/fj.02-0211hyp.CrossRefGoogle Scholar
  6. 6.
    Ignarro LJ, Buga GM, Wood KS, et al. Endothelium-derived relaxing factor and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA. 1987;84:9265–9269. doi: 10.1073/pnas.84.24.9265.CrossRefPubMedGoogle Scholar
  7. 7.
    Murray JA, Ledlow A, Launspach J, et al. The effects of recombinant human hemoglobin on esophageal motor functions in humans. Gastroenterology. 1995;109:1241–1248. doi: 10.1016/0016-5085(95)90584-7.CrossRefPubMedGoogle Scholar
  8. 8.
    Mearin F, Mourelle M, Guarner F, et al. Patients with achalasia lack nitric oxide synthase in the gastro-oesophageal junction. Eur J Clin Invest. 1993;23:724–728. doi: 10.1111/j.1365-2362.1993.tb01292.x.CrossRefPubMedGoogle Scholar
  9. 9.
    Pimentel M, Mayer AG, Park S, et al. Methane production during lactulose breath test is associated with gastrointestinal disease presentation. Dig Dis Sci. 2003;48:86–92. doi: 10.1023/A:1021738515885.CrossRefPubMedGoogle Scholar
  10. 10.
    Chatterjee S, Park S, Low K, Kong Y, Pimentel M. The degree of breath methane production in IBS correlates with the severity of constipation. Am J Gastroenterol. 2007;102:837–841. doi: 10.1111/j.1572-0241.2007.01072.x.CrossRefPubMedGoogle Scholar
  11. 11.
    Weaver GA, Krause JA, Miller TL, et al. Incidence of methanogenic bacteria in a sigmoidoscopy population: an association of methanogenic bacteria and diverticulosis. Gut. 1986;27:698–704. doi: 10.1136/gut.27.6.698.CrossRefPubMedGoogle Scholar
  12. 12.
    Haines A, Metz G, Dilawari J, et al. Breath-methane in patients with cancer of the large bowel. Lancet. 1977;2:481–483. doi: 10.1016/S0140-6736(77)91605-1.CrossRefPubMedGoogle Scholar
  13. 13.
    Levitt MD, Bond JH. Volume, composition, and source of intestinal gas. Gastroenterology. 1970;59:921–929.PubMedGoogle Scholar
  14. 14.
    Kirk E. The quantity and composition of human colonic flatus. Gastroenterology. 1949;12:782–794.PubMedGoogle Scholar
  15. 15.
    Levitt MD, Ingelfinger FJ. Hydrogen and methane production in man. Ann N Y Acad Sci. 1968;150:75–81. doi: 10.1111/j.1749-6632.1968.tb19033.x.CrossRefPubMedGoogle Scholar
  16. 16.
    Levitt MD. Production and excretion of hydrogen gas in man. N Engl J Med. 1969;281:122–127.PubMedCrossRefGoogle Scholar
  17. 17.
    Bond JH, Engel RR, Levitt MD. Factors influencing pulmonary methane excretion in man. An indirect method of studying the in situ metabolism of the methane-producing colonic bacteria. J Exp Med. 1971;133:572–588. doi: 10.1084/jem.133.3.572.CrossRefPubMedGoogle Scholar
  18. 18.
    Christl SU, Murgatroyd PR, Gibson GR, et al. Production, metabolism, and excretion of hydrogen in the large intestine. Gastroenterology. 1992;102:1269–1277.PubMedGoogle Scholar
  19. 19.
    Peled Y, Gilat T, Liberman E, et al. The development of methane production in childhood and adolescence. J Pediatr Gastroenterol Nutr. 1985;4:575–579. doi: 10.1097/00005176-198508000-00013.CrossRefPubMedGoogle Scholar
  20. 20.
    Flatz G, Czeizel A, Metneki J, et al. Pulmonary hydrogen and methane excretion following ingestion of an unabsorbable carbohydrate: a study of twins. J Pediatr Gastroenterol Nutr. 1985;4:936–941. doi: 10.1097/00005176-198512000-00014.CrossRefPubMedGoogle Scholar
  21. 21.
    Florin TH, Zhu G, Kirk KM, et al. Shared and unique environmental factors determine the ecology of methanogens in humans and rats. Am J Gastroenterol. 2000;95:2872–2879. doi: 10.1111/j.1572-0241.2000.02319.x.CrossRefPubMedGoogle Scholar
  22. 22.
    Flourie B, Etanchaud F, Florent C, et al. Comparative study of hydrogen and methane production in the human colon using caecal and faecal homogenates. Gut. 1990;31:684–685. doi: 10.1136/gut.31.6.684.CrossRefPubMedGoogle Scholar
  23. 23.
    Pochart P, Lemann F, Flourie B, et al. Pyxigraphic sampling to enumerate methanogens and anaerobes in the right colon of healthy humans. Gastroenterology. 1993;105:1281–1285.PubMedGoogle Scholar
  24. 24.
    Cloarec D, Bornet F, Gouilloud S, et al. Breath hydrogen response to lactulose in healthy subjects: relationship to methane producing status. Gut. 1990;31:300–304. doi: 10.1136/gut.31.3.300.CrossRefPubMedGoogle Scholar
  25. 25.
    McKay LF, Eastwood MA, Brydon WG. Methane excretion in man—a study of breath, flatus, and faeces. Gut. 1985;26:69–74. doi: 10.1136/gut.26.1.69.CrossRefPubMedGoogle Scholar
  26. 26.
    Jones WJ, Nagle DP, Whitman WB. Methanogens and the diversity of archaebacteria. Microbiol Rev. 1987;51:135–177.PubMedGoogle Scholar
  27. 27.
    Hungate RE. Symposium: selected topics in microbial ecology. I. Microbial ecology of the rumen. Bacteriol Rev. 1960;24:353–356.PubMedGoogle Scholar
  28. 28.
    Johnson KA, Johnson DE. Methane emissions from cattle. J Anim Sci. 1995;73:2483–2492.PubMedGoogle Scholar
  29. 29.
    Miller TL, Wolin MJ. Enumeration of Methanobrevibacter smithii in human feces. Arch Microbiol. 1982;131:14–18. doi: 10.1007/BF00451492.CrossRefPubMedGoogle Scholar
  30. 30.
    McKay LF, Holbrook WP, Eastwood MA. Methane and hydrogen production by human intestinal anaerobic bacteria. Acta Pathol Microbiol Immunol Scand. 1982;90:257–260.Google Scholar
  31. 31.
    Blaut M. Metabolism of methanogens. Antonie Van Leeuwenhoek. 1994;66:187–208. doi: 10.1007/BF00871639.CrossRefPubMedGoogle Scholar
  32. 32.
    Gibson GR, Cummings JH, Macfarlane GT, et al. Alternative pathways for hydrogen disposal during fermentation in the human colon. Gut. 1990;31:679–683. doi: 10.1136/gut.31.6.679.CrossRefPubMedGoogle Scholar
  33. 33.
    Thauer RK, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977;41:100–180.PubMedGoogle Scholar
  34. 34.
    Gibson GR, Macfarlane GT, Cummings JH. Sulfate reducing bacteria and hydrogen metabolism in the human large intestine. Gut. 1993;34:437–439. doi: 10.1136/gut.34.4.437.CrossRefPubMedGoogle Scholar
  35. 35.
    Christl SU, Gibson GR, Cummings JH. Role of dietary sulphate in the regulation of methanogenesis in the human large intestine. Gut. 1992;33:1234–1238. doi: 10.1136/gut.33.9.1234.CrossRefPubMedGoogle Scholar
  36. 36.
    Pochart P, Dore J, Lemann F, et al. Interrelations between populations of methanogenic archaea and sulfate-reducing bacteria in the human colon. FEMS Microbiol Lett. 1992;98:225–228.Google Scholar
  37. 37.
    Gibson GR, Cummings JH, Marfarlane GT. Competition for hydrogen between sulphate-reducing bacteria and methanogenic bacteria from the human large intestine. J Appl Bacteriol. 1988;65:241–247.PubMedGoogle Scholar
  38. 38.
    Karlin DA, Jones RD, Stroehlein JR, et al. Breath methane excretion in patients with unresected colorectal cancer. J Natl Cancer Inst. 1982;69:573–576.PubMedGoogle Scholar
  39. 39.
    Kashtan H, Rabau M, Peled Y, et al. Methane production in patients with colorectal carcinoma. Isr J Med Sci. 1989;25:614–616.PubMedGoogle Scholar
  40. 40.
    Kassinen A, Krogius-Kurikka L, Makivuokko H, et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology. 2007;133:24–33. doi: 10.1053/j.gastro.2007.04.005.CrossRefPubMedGoogle Scholar
  41. 41.
    Halvorson HA, Schlett CD, Riddle MS. Postinfectious irritable bowel syndrome—a meta-analysis. Am J Gastroenterol. 2006;101:1894–1899. doi: 10.1111/j.1572-0241.2006.00654.x.CrossRefPubMedGoogle Scholar
  42. 42.
    Pimentel M, Chow EJ, Lin HC. Normalization of lactulose breath testing correlates with symptom improvement in irritable bowel syndrome. A double-blind, randomized, placebo-controlled study. Am J Gastroenterol. 2003;98:412–419.PubMedGoogle Scholar
  43. 43.
    William HL. Lactulose breath testing, bacterial overgrowth, and IBS: just a lot of hot air? Gastroenterology. 2003;125:1898–1900.Google Scholar
  44. 44.
    Fiedorek SC, Pumphrey CL, Casteel HB. Breath methane production in children with constipation and encopresis. J Pediatr Gastroenterol Nutr. 1990;10:473–477. doi: 10.1097/00005176-199005000-00010.CrossRefPubMedGoogle Scholar
  45. 45.
    Peled Y, Weinberg D, Hallak A, et al. Factors affecting methane production in Humans. Dig Dis Sci. 1987;32:267–71. doi: 10.1007/BF01297052.CrossRefPubMedGoogle Scholar
  46. 46.
    Soares AC, Lederman HM, Fagundes-Neto U, et al. Breath methane associated with slow colonic transit time in children with chronic constipation. J Clin Gastroenterol. 2005;39:512–515. doi: 10.1097/01.mcg.0000165665.94777.bd.CrossRefPubMedGoogle Scholar
  47. 47.
    Stephen AM, Wiggins HS, Englyst HN, et al. The effect of age, sex and level of dietary fibre from wheat on large-bowel function in thirty healthy subjects. Br J Nutr. 1986;56:349–361. doi: 10.1079/BJN19860116.CrossRefPubMedGoogle Scholar
  48. 48.
    Drossman DA, Morris CB, Hu Y, et al. A prospective assessment of bowel habit in irritable bowel syndrome in women: defining an alternator. Gastroenterology. 2005;128:580–589. doi: 10.1053/j.gastro.2004.12.006.CrossRefPubMedGoogle Scholar
  49. 49.
    Pimentel M, Chatterjee S, Chow EJ, et al. Neomycin improves constipation-predominant irritable bowel syndrome in a fashion that Is dependent on the presence of methane gas: subanalysis of a double-blind randomized controlled study. Dig Dis Sci. 2006;51:1297–1301. doi: 10.1007/s10620-006-9104-6.CrossRefPubMedGoogle Scholar
  50. 50.
    Pitcher MC, Cummings JH. Hydrogen sulphide: a bacterial toxin in ulcerative colitis? Gut. 1996;39:1–4. doi: 10.1136/gut.39.1.1.CrossRefPubMedGoogle Scholar
  51. 51.
    Pimentel M, Lin HC, Enayati P, et al. Methane, a gas produced by enteric bacteria, slows intestinal transit and augments small intestinal contractile activity. Am J Physiol Gastrointest Liver Physiol. 2006;290:G1089–G1095. doi: 10.1152/ajpgi.00574.2004.CrossRefPubMedGoogle Scholar
  52. 52.
    Bulbring E, Lin RCY. The effect of intraluminal application of 5-hydroxytryptamine and 5-hydroxytryptophan on peristalsis, the local production of 5-hydroxytryptamine and its release in relation to intraluminal pressure and propulsive activity. J Physiol. 1958;140:381–407.PubMedGoogle Scholar
  53. 53.
    Bertaccini G. Tissue 5-hydroxytryptamine and urinary 5-hydroxyindoleacetic acid after partial or total removal of the gastrointestinal tract in the rat. J Physiol. 1960;153:239–249.PubMedGoogle Scholar
  54. 54.
    Bearcroft CP, Perret D, Farthing MJG. Postprandial 5-hydroxytryptaminein diarrhea predominant irritable bowel syndrome: a pilot study. Gut. 1998;42:42–46.PubMedCrossRefGoogle Scholar
  55. 55.
    Pimentel M, Kong Y, Park S. IBS subjects with methane on lactulose breath test have lower postprandial serotonin levels than subjects with hydrogen. Dig Dis Sci. 2004;49:84–87. doi: 10.1023/B:DDAS.0000011607.24171.c0.CrossRefPubMedGoogle Scholar
  56. 56.
    Hede AR, Andersson L, Post C. Effect of a homologous series of halogenated methanes on pulmonary uptake of 5-hydroxytryptamine in isolated perfused rat lung. Acta Pharmacol Toxicol (Copenh). 1985;57:291–296.Google Scholar
  57. 57.
    Wolin MJ. Fermentation in the rumen and human large intestine. Science. 1981;213:1463–1468. doi: 10.1126/science.7280665.CrossRefPubMedGoogle Scholar
  58. 58.
    Miller TL, Wolin MJ. Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylglutaryl SCoA reductase inhibitors. J Dairy Sci. 2001;84:1445–1448.CrossRefPubMedGoogle Scholar
  59. 59.
    Florin THJ, Woods HJ. Inhibition of methanogenesis by human bile. Gut. 1995;37:418–421. doi: 10.1136/gut.37.3.418.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Ara B. Sahakian
    • 1
  • Sam-Ryong Jee
    • 1
  • Mark Pimentel
    • 1
  1. 1.GI Motility Program, Division of GastroenterologyCedars-Sinai Medical CenterLos AngelesUSA

Personalised recommendations