Methane and the Gastrointestinal Tract

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.

This is a preview of subscription content, log in to check access.

Fig. 1

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.

    Article  CAS  PubMed  Google Scholar 

  2. 2.

    Simon GL, Gorbach SL. Intestinal flora in health and disease. Gastroenterology. 1984;86:174–193.

    CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  4. 4.

    Strocchi A, Levitt MD. Maintaining intestinal H2 balance: credit the colonic bacteria. Gastroenterology. 1992;102:1424–1426.

    CAS  PubMed  Google 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.

    Article  CAS  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Levitt MD, Bond JH. Volume, composition, and source of intestinal gas. Gastroenterology. 1970;59:921–929.

    CAS  PubMed  Google Scholar 

  14. 14.

    Kirk E. The quantity and composition of human colonic flatus. Gastroenterology. 1949;12:782–794.

    CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Levitt MD. Production and excretion of hydrogen gas in man. N Engl J Med. 1969;281:122–127.

    CAS  PubMed  Article  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  26. 26.

    Jones WJ, Nagle DP, Whitman WB. Methanogens and the diversity of archaebacteria. Microbiol Rev. 1987;51:135–177.

    CAS  PubMed  Google Scholar 

  27. 27.

    Hungate RE. Symposium: selected topics in microbial ecology. I. Microbial ecology of the rumen. Bacteriol Rev. 1960;24:353–356.

    CAS  PubMed  Google Scholar 

  28. 28.

    Johnson KA, Johnson DE. Methane emissions from cattle. J Anim Sci. 1995;73:2483–2492.

    CAS  PubMed  Google Scholar 

  29. 29.

    Miller TL, Wolin MJ. Enumeration of Methanobrevibacter smithii in human feces. Arch Microbiol. 1982;131:14–18. doi:10.1007/BF00451492.

    Article  CAS  PubMed  Google 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.

    CAS  Google Scholar 

  31. 31.

    Blaut M. Metabolism of methanogens. Antonie Van Leeuwenhoek. 1994;66:187–208. doi:10.1007/BF00871639.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Thauer RK, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977;41:100–180.

    CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Google 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.

    CAS  PubMed  Article  Google 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.

    Article  CAS  PubMed  Google 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.

    CAS  Google Scholar 

  57. 57.

    Wolin MJ. Fermentation in the rumen and human large intestine. Science. 1981;213:1463–1468. doi:10.1126/science.7280665.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google 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.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mark Pimentel.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sahakian, A.B., Jee, S. & Pimentel, M. Methane and the Gastrointestinal Tract. Dig Dis Sci 55, 2135–2143 (2010). https://doi.org/10.1007/s10620-009-1012-0

Download citation

Keywords

  • Methane
  • Methanogenic flora
  • Intestinal gas
  • Gastrointestinal motility