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Contributions of the microbial hydrogen economy to colonic homeostasis

Nature Reviews Gastroenterology & Hepatology volume 9, pages 504–518 (2012)Cite this article

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Abstract

Colonic gases are among the most tangible features of digestion, yet physicians are typically unable to offer long-term relief from clinical complaints of excessive gas. Studies characterizing colonic gases have linked changes in volume or composition with bowel disorders and shown hydrogen gas (H2), methane, hydrogen sulphide, and carbon dioxide to be by-products of the interplay between H2-producing fermentative bacteria and H2 consumers (reductive acetogens, methanogenic archaea and sulphate-reducing bacteria [SRB]). Clinically, H2 and methane measured in breath can indicate lactose and glucose intolerance, small intestinal bacterial overgrowth and IBS. Methane levels are increased in patients with constipation or IBS. Hydrogen sulphide is a by-product of H2 metabolism by SRB, which are ubiquitous in the colonic mucosa. Although higher hydrogen sulphide and SRB levels have been detected in patients with IBD, and to a lesser extent in colorectal cancer, this colonic gas might have beneficial effects. Moreover, H2 has been shown to have antioxidant properties and, in the healthy colon, physiological H2 concentrations might protect the mucosa from oxidative insults, whereas an impaired H2 economy might facilitate inflammation or carcinogenesis. Therefore, standardized breath gas measurements combined with ever-improving molecular methodologies could provide novel strategies to prevent, diagnose or manage numerous colonic disorders.

Key Points

  • The colonic gases hydrogen (H2), carbon dioxide and methane (CH4) are end products of microbial fermentation; their concentrations depend on the interplay between host physiology and H2-producing (hydrogenogenic) and H2-using (hydrogenotrophic) microbes

  • Colonic H2 production is most readily measured via excretion in breath; clinically, breath H2 and CH4 are commonly measured to assess lactose and glucose intolerance and small intestinal bacterial overgrowth, and increasingly IBS

  • Improved understanding of microbial H2 metabolism and its relation to expired gas concentrations will reinforce the breath gas test as a widely applicable, easy and cost-effective diagnostic or prognostic tool

  • Use of breath gas tests in diagnosis could enable novel therapeutic or preventative measures for a wide array of colonic diseases

  • Although emphasis has been given to the potential inflammatory or carcinogenic properties of colonic gases, emerging evidence suggests these gases might have a beneficial effect in colonic health

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Figure 1: Milestones in the measurement of colonic gases in breath and flatus.
Figure 2: Biochemical pathways of H2 production from bacterial fermentation.
Figure 3: H2 gas is inherently produced during microbial fermentation in the human colon.

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Acknowledgements

Related research was supported by grants from the NIH (RO1 CA135379) and Carle Foundation-University of Illinois Translational Research Program. The authors thank Matthew T. Leslie for help in the bibliographical search. This Review is dedicated to the scientific legacies of Dr Michael D. Levitt and Dr. Meyer J. Wolin, both of whom consistently contributed key studies over many years relating to the importance of the microbial hydrogen economy on colonic homeostasis.

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  1. University of Illinois at Urbana-Champaign, 1207 W. Gregory Drive, Urbana, 61801, IL, USA

    Franck Carbonero, Ann C. Benefiel & H. Rex Gaskins

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Carbonero, F., Benefiel, A. & Gaskins, H. Contributions of the microbial hydrogen economy to colonic homeostasis. Nat Rev Gastroenterol Hepatol 9, 504–518 (2012). https://doi.org/10.1038/nrgastro.2012.85

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