Volume 90, Issue 6, December (2003), pp. 1057-1070 © The Author 2003
doi:10.1079/BJN20031003

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Butyrate is only one of several growth inhibitors produced during gut flora-mediated fermentation of dietary fibre sources

Gabriele Beyer-Sehlmeyer¹, Michael Glei¹, Esther Hartmann¹, Rosin Hughes², Christoph Persin³, Volker Böhm⁴, Ian Rowland², Rainer Schubert⁵, Gerhard Jahreis⁵, Beatrice L. Pool-Zobel^1
1Department of Nutritional Toxicology, Institute for Nutrition, Friedrich Schiller University, Dornburger Str. 25, D-07743 Jena, Germany
²Northern Ireland Centre for Diet and Health (NICHE), School of Biomedical Sciences, University of Ulster, Coleraine, BT52 1SA, UK
³Kampffmeyer Food Service GmbH, Trettaustr. 32-34, 21107 Hamburg, Germany
⁴Department of Human Nutrition, Institute for Nutrition, Friedrich Schiller University, Dornburger Str. 29, D-07743 Jena, Germany
⁵Department of Nutritional Physiology, Institute for Nutrition, Friedrich Schiller University, Dornburger Str. 25, D-07743 Jena, Germany

 (Received 7 March 2003–Revised 9 July 2003–Accepted 4 August 2003)

Dietary fibre sources are fermented by the gut flora to yield short-chain fatty acids (SCFA) together with degraded phytochemicals and plant nutrients. Butyrate, a major SCFA, is potentially chemoprotective by suppressing the growth of tumour cells and enhancing their differentiation. Conversely, it could lead to a positive selection pressure for transformed cells by inducing glutathione S-transferases (GST) and enhancing chemoresistance. Virtually nothing is known about how butyrate's activities are affected by other fermentation products. To investigate such interactions, a variety of dietary fibre sources was fermented with human faecal slurries in vitro, analysed for SCFA, and corresponding SCFA mixtures were prepared. HT29 colon tumour cells were treated for 72 h with individual SCFA or complex samples. The growth of cells, GST activity, and chemoresistance towards 4-hydroxynonenal were determined. Fermentation products inhibited cell growth more than the corresponding SCFA mixtures, and the SCFA mixtures were more active than butyrate, probably due to phytoprotectants and to propionate, respectively, which also inhibit cell growth. Only butyrate induced GST, whereas chemoresistance was caused by selected SCFA mixtures, but not by all corresponding fermentation samples. In summary, fermentation supernatant fractions contain compounds that: (1) enhance the anti-proliferative properties of butyrate (propionate, phytochemical fraction); (2) do not alter its capacity to induce GST; (3) prevent chemoresistance in tumour cells. It can be concluded that fermented dietary fibre sources are more potent inhibitors of tumour cell growth than butyrate alone, and also contain ingredients which counteract the undesired positive selection pressures that higher concentrations of butyrate induce in tumour cells.

Keywords:

Abbreviations:

Keywords:
Short-chain fatty acids, Complex gut fermentation products, Genotoxicity, 4-Hydroxynonenal

Abbreviations:
ABTS, 2,2′-azino-bis(3-ethylbenzothiozolin-6-sulfonic acid, AP, alkaline phosphatase, EC₅₀, effective concentration of a test sample resulting in a 50 % reduction of cell number under the specified cell culture and treatment conditions, GSH, glutathione, GST, glutathione S-transferase, HNE, 4-hydroxynonenal, SCFA, short-chain fatty acid, TEAC, Trolox-equivalent antioxidant capacity