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      Systemic availability and metabolism of colonic‐derived short‐chain fatty acids in healthy subjects: a stable isotope study

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          Abstract

          Key points

          • The short‐chain fatty acids (SCFAs) are bacterial metabolites produced during the colonic fermentation of undigested carbohydrates, such as dietary fibre and prebiotics, and can mediate the interaction between the diet, the microbiota and the host.

          • We quantified the fraction of colonic administered SCFAs that could be recovered in the systemic circulation, the fraction that was excreted via the breath and urine, and the fraction that was used as a precursor for glucose, cholesterol and fatty acids.

          • This information is essential for understanding the molecular mechanisms by which SCFAs beneficially affect physiological functions such as glucose and lipid metabolism and immune function.

          Abstract

          The short‐chain fatty acids (SCFAs), acetate, propionate and butyrate, are bacterial metabolites that mediate the interaction between the diet, the microbiota and the host. In the present study, the systemic availability of SCFAs and their incorporation into biologically relevant molecules was quantified. Known amounts of 13C‐labelled acetate, propionate and butyrate were introduced in the colon of 12 healthy subjects using colon delivery capsules and plasma levels of 13C‐SCFAs 13C‐glucose, 13C‐cholesterol and 13C‐fatty acids were measured. The butyrate‐producing capacity of the intestinal microbiota was also quantified. Systemic availability of colonic‐administered acetate, propionate and butyrate was 36%, 9% and 2%, respectively. Conversion of acetate into butyrate (24%) was the most prevalent interconversion by the colonic microbiota and was not related to the butyrate‐producing capacity in the faecal samples. Less than 1% of administered acetate was incorporated into cholesterol and <15% in fatty acids. On average, 6% of colonic propionate was incorporated into glucose. The SCFAs were mainly excreted via the lungs after oxidation to 13CO 2, whereas less than 0.05% of the SCFAs were excreted into urine. These results will allow future evaluation and quantification of SCFA production from 13C‐labelled fibres in the human colon by measurement of 13C‐labelled SCFA concentrations in blood.

          Key points

          • The short‐chain fatty acids (SCFAs) are bacterial metabolites produced during the colonic fermentation of undigested carbohydrates, such as dietary fibre and prebiotics, and can mediate the interaction between the diet, the microbiota and the host.

          • We quantified the fraction of colonic administered SCFAs that could be recovered in the systemic circulation, the fraction that was excreted via the breath and urine, and the fraction that was used as a precursor for glucose, cholesterol and fatty acids.

          • This information is essential for understanding the molecular mechanisms by which SCFAs beneficially affect physiological functions such as glucose and lipid metabolism and immune function.

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          Author and article information

          Contributors
          kristin.verbeke@med.kuleuven.be
          Journal
          J Physiol
          J. Physiol. (Lond.)
          10.1111/(ISSN)1469-7793
          TJP
          jphysiol
          The Journal of Physiology
          John Wiley and Sons Inc. (Hoboken )
          0022-3751
          1469-7793
          18 September 2016
          15 January 2017
          : 595
          : 2 ( doiID: 10.1113/tjp.2017.595.issue-2 )
          : 541-555
          Affiliations
          [ 1 ] Translational Research in Gastrointestinal Disorders
          [ 2 ] Leuven Food Science and Nutrition Research Centre
          [ 3 ] Center for Food and Microbial Technology
          [ 4 ] Drug Delivery and Disposition KU Leuven Leuven Belgium
          [ 5 ] Stable Isotope Biochemistry Laboratory, Scottish Universities Environmental Research Centre University of Glasgow Glasgow UK
          [ 6 ] Department of Pathology, Bacteriology and Avian Diseases Ghent University Merelbeke Belgium
          [ 7 ] Group Health and Social Work UC Leuven‐Limburg Leuven Belgium
          [ 8 ] Industrial Microbiology and Food Biotechnology Vrije Universiteit Brussel Brussel Belgium
          Author notes
          [*] [* ] Corresponding author K. Verbeke: Translational Research in Gastrointestinal Disorders, Herestraat 49 Box 701, B‐3000 Leuven, Belgium. Email: kristin.verbeke@ 123456med.kuleuven.be
          Author information
          http://orcid.org/0000-0002-1203-9063
          Article
          PMC5233652 PMC5233652 5233652 TJP7470
          10.1113/JP272613
          5233652
          27510655
          c8c1734a-175d-4223-8253-3f939528c653
          © 2016 The Authors. The Journal of Physiology © 2016 The Physiological Society
          History
          : 17 April 2016
          : 20 July 2016
          Page count
          Figures: 6, Tables: 0, Pages: 15, Words: 9374
          Funding
          Funded by: W. K. Kellogg Chair in Cereal Science and Nutrition
          Funded by: Fund for Scientific Research‐Flanders
          Award ID: FWO‐G.0109.07, FWO‐1.5.131.10
          Categories
          Metabolism and Regulation
          Gastrointestinal, Hepatic and Pancreatic Physiology
          Research Paper
          Alimentary
          Custom metadata
          2.0
          tjp7470
          15 January 2017
          Converter:WILEY_ML3GV2_TO_NLMPMC version:5.0.1 mode:remove_FC converted:12.01.2017

          systemic exposure,colonic fermentation,metabolism,short‐chain fatty acids,stable isotopes

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