Long-Term Green Tea Supplementation Does Not Change the Human Gut Microbiota

Pilou L H R Janssens, John Penders, Rick Hursel, Andries E Budding, Paul H M Savelkoul, Margriet S Westerterp-Plantenga, Pilou L H R Janssens, John Penders, Rick Hursel, Andries E Budding, Paul H M Savelkoul, Margriet S Westerterp-Plantenga

Abstract

Background: Green tea catechins may play a role in body weight regulation through interactions with the gut microbiota.

Aim: We examined whether green tea supplementation for 12 weeks induces changes in composition of the human gut microbiota.

Methods: 58 Caucasian men and women were included in a randomized, placebo-controlled design. For 12 weeks, subjects consumed either green tea (>0.56 g/d epigallocatechin-gallate + 0.28 ∼ 0.45 g/d caffeine) or placebo capsules. Fecal samples were collected twice (baseline, vs. week 12) for analyses of total bacterial profiles by means of IS-profiling, a 16S-23S interspacer region-based profiling method.

Results: No significant changes between baseline and week 12 in subjects receiving green tea or placebo capsules, and no significant interactions between treatment (green tea or placebo) and time (baseline and week 12) were observed for body composition. Analysis of the fecal samples in subjects receiving green tea and placebo showed similar bacterial diversity and community structures, indicating there were no significant changes in bacterial diversity between baseline and week 12 in subjects receiving green tea capsules or in subjects receiving placebo capsules. No significant interactions were observed between treatment (green tea or placebo) and time (baseline and week 12) for the gut microbial diversity. Although, there were no significant differences between normal weight and overweight subjects in response to green tea, we did observe a reduced bacterial alpha diversity in overweight as compared to normal weight subjects (p = 0.002).

Conclusion: Green tea supplementation for 12 weeks did not have a significant effect on composition of the gut microbiota.

Trial registration: ClinicalTrials.gov NCT01556321.

Conflict of interest statement

Competing Interests: P.L.H.R. Janssens, J. Penders, R. Hursel, and M.S. Westerterp-Plantenga have no conflicts of interest. A.E. Budding and P.H.M. Savelkoul have proprietary rights on the IS-pro platform technology. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

Figures

Fig 1. CONSORT flow diagram.
Fig 1. CONSORT flow diagram.
Fig 2. BMI categories: BMI 18–25 kg/m…
Fig 2. BMI categories: BMI 18–25 kg/m2 (Mdn = 3.78, n = 43) vs. BMI ≥25 kg/m2 (Mdn = 3.52, n = 17).
All Phyla combined, Shannon diversity index using Mann-Whitney test, *p = 0.002.
Fig 3. Box plots, comparisons of the…
Fig 3. Box plots, comparisons of the between-sample diversity in green tea and placebo as calculated by Bray Curtis dissimilarity.
Beta diversity captures the dissimilarity in microbial composition of the groups between baseline and week 12.
Fig 4. Principal Coordinates Analysis (PCoA) plots…
Fig 4. Principal Coordinates Analysis (PCoA) plots of Bray Curtis distances between samples, with the %explained variance by the principle coordinates.
PCoA per phylum, Bray Curtis, log2, n = 58.

References

    1. Hase T, Komine Y, Meguro S, Takeda Y, Takahashi H, Matsui Y. Anti-obesity effects of tea catechins in humans. J Oleo Sci. 2001;50: 599–605.
    1. Matsuyama T, Tanaka Y, Kamimaki I, Nagao T, Tokimitsu I. Catechin safely improved higher levels of fatness, blood pressure, and cholesterol in children. Obesity. 2008;16: 1338–1348. 10.1038/oby.2008.60
    1. Wang H, Wen Y, Du Y, Yan X, Guo H, Rycroft JA, et al. Effects of catechin enriched green tea on body composition. Obesity (Silver Spring).18: 773–779.
    1. Nagao T, Hase T, Tokimitsu I. A green tea extract high in catechins reduces body fat and cardiovascular risks in humans. Obesity (Silver Spring). 2007;15: 1473–1483.
    1. Nagao T, Meguro S, Soga S, Otsuka A, Tomonobu K, Fumoto S. Tea catechins suppress accumulation of body fat in humans. J Oleo Sci. 2001;50: 717–728.
    1. Most J, Goossens GH, Jocken JW, Blaak EE. Short-term supplementation with a specific combination of dietary polyphenols increases energy expenditure and alters substrate metabolism in overweight subjects. Int J Obes (Lond). 2014;38: 698–706.
    1. Rudelle S, Ferruzzi MG, Cristiani I, Moulin J, Mace K, Acheson KJ, et al. Effect of a thermogenic beverage on 24-hour energy metabolism in humans. Obesity (Silver Spring). 2007;15: 349–355.
    1. Dulloo AG, Duret C, Rohrer D, Girardier L, Mensi N, Fathi M, et al. Efficacy of a green tea extract rich in catechin polyphenols and caffeine in increasing 24-h energy expenditure and fat oxidation in humans. Am J Clin Nutr. 1999;70: 1040–1045.
    1. Berube-Parent S, Pelletier C, Dore J, Tremblay A. Effects of encapsulated green tea and Guarana extracts containing a mixture of epigallocatechin-3-gallate and caffeine on 24 h energy expenditure and fat oxidation in men. Br J Nutr. 2005;94: 432–436.
    1. Harada U, Chikama A, Saito S, Takase H, Nagao T, Hase T. Effects of long-term ingestion of tea catechins on energy expenditure and dietery fat oxidation in healthy subjects. J Health Sci. 2005;51: 248–252.
    1. Hsu TF, Kusumoto A, Abe K, Hosoda K, Kiso Y, Wang MF, et al. Polyphenol-enriched oolong tea increases fecal lipid excretion. Eur J Clin Nutr. 2006;60: 1330–1336.
    1. Janssens PL, Hursel R, Westerterp-Plantenga MS. Long-term green tea extract supplementation does not affect fat absorption, resting energy expenditure, and body composition in adults. J Nutr. 2015;145: 864–870. 10.3945/jn.114.207829
    1. Rastmanesh R. High polyphenol, low probiotic diet for weight loss because of intestinal microbiota interaction. Chem Biol Interact. 2011;189: 1–8. 10.1016/j.cbi.2010.10.002
    1. Zoetendal EG, Akkermans AD, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998;64: 3854–3859.
    1. Ley RE, Turnbaugh P.J. Human gut microbes associated with obesity Nature. 2006;444: 1022–1023.
    1. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101: 15718–15723.
    1. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe. 2008;3: 213–223. 10.1016/j.chom.2008.02.015
    1. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science.341: 1241214 10.1126/science.1241214
    1. Graham C, Mullen A, Whelen K. Obesity and the gastrointestinal microbiota: a review of associations and mechanisms. Nutrition Reviews. 2015;0: 1–10.
    1. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102: 11070–11075.
    1. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444: 1027–1031.
    1. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457: 480–484. 10.1038/nature07540
    1. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature. 2012;489: 220–230. 10.1038/nature11550
    1. Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol. 2012;9: 577–589. 10.1038/nrgastro.2012.156
    1. Wang H, Wen Y, Du Y, Yan X, Guo H, Rycroft JA, et al. Effects of catechin enriched green tea on body composition. Obesity (Silver Spring). 2010;18: 773–779.
    1. Scalbert A, Morand C, Manach C, Remesy C. Absorption and metabolism of polyphenols in the gut and impact on health. Biomed Pharmacother. 2002;56: 276–282.
    1. Williamson G, Clifford MN. Colonic metabolites of berry polyphenols: the missing link to biological activity? Br J Nutr. 2010;104 Suppl 3: S48–66. 10.1017/S0007114510003946
    1. Aura AM, Martin-Lopez P, O'Leary KA, Williamson G, Oksman-Caldentey KM, Poutanen K, et al. In vitro metabolism of anthocyanins by human gut microflora. Eur J Nutr. 2005;44: 133–142.
    1. Lee HC, Jenner AM, Low CS, Lee YK. Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota. Res Microbiol. 2006;157: 876–884.
    1. Okubo T, Ishihara N, Oura A, Serit M, Kim M, Yamamoto T, et al. In vivo effects of tea polyphenol intake on human intestinal microflora and metabolism. Biosci Biotechnol Biochem. 1992;56: 588–591.
    1. Parkar SG, Stevenson DE, Skinner MA. The potential influence of fruit polyphenols on colonic microflora and human gut health. Int J Food Microbiol. 2008;124: 295–298. 10.1016/j.ijfoodmicro.2008.03.017
    1. Tzounis X, Vulevic J, Kuhnle GG, George T, Leonczak J, Gibson GR, et al. Flavanol monomer-induced changes to the human faecal microflora. Br J Nutr. 2008;99: 782–792.
    1. Jin JS, Touyama M, Hisada T, Benno Y. Effects of green tea consumption on human fecal microbiota with special reference to Bifidobacterium species. Microbiol Immunol. 2012;56: 729–739. 10.1111/j.1348-0421.2012.00502.x
    1. Janssens PL, Hursel R, Westerterp-Plantenga MS. Long-Term Green Tea Extract Supplementation Does Not Affect Fat Absorption, Resting Energy Expenditure, and Body Composition in Adults. J Nutr. 2015.
    1. Hursel R, Westerterp-Plantenga MS. Consumption of milk-protein combined with green tea modulates diet-induced thermogenesis. Nutrients. 2011;3: 725–733. 10.3390/nu3080725
    1. Plasqui G, Soenen S, Westerterp-Plantenga MS, Westerterp KR. Measurement of longitudinal changes in body composition during weight loss and maintenance in overweight and obese subjects using air-displacement plethysmography in comparison with the deuterium dilution technique. Int J Obes (Lond). 2011;35: 1124–1130.
    1. Budding AE, Grasman ME, Lin F, Bogaards JA, Soeltan-Kaersenhout DJ, Vandenbroucke-Grauls CM, et al. IS-pro: high-throughput molecular fingerprinting of the intestinal microbiota. FASEB J. 2010;24: 4556–4564. 10.1096/fj.10-156190
    1. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing; 2015. Available: .
    1. Oksanen J, Blanchet FG, Roeland Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. vegan: Community Ecology Package. R package version 2.3–0. 2015.
    1. Bray J, Curtis J. An ordination of the upland forest comunities of Southern Wisconsin. Ecol Monogr. 1957;27: 325–349.
    1. Westerterp-Plantenga MS, Lejeune MP, Kovacs EM. Body weight loss and weight maintenance in relation to habitual caffeine intake and green tea supplementation. Obes Res. 2005;13: 1195–1204.
    1. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505: 559–563. 10.1038/nature12820
    1. Kozuma K, Tsuchiya S, Kohori J, Hase T, Tokimitsu I. Antihypertensive effect of green coffee bean extract on mildly hypertensive subjects. Hypertens Res. 2005;28: 711–718.
    1. Van Citters GW, Lin HC. Management of small intestinal bacterial overgrowth. Curr Gastroenterol Rep. 2005;7: 317–320.
    1. Cowan TE, Palmnas MS, Yang J, Bomhof MR, Ardell KL, Reimer RA, et al. Chronic coffee consumption in the diet-induced obese rat: impact on gut microbiota and serum metabolomics. J Nutr Biochem. 2014;25: 489–495. 10.1016/j.jnutbio.2013.12.009
    1. Jaquet M, Rochat I, Moulin J, Cavin C, Bibiloni R. Impact of coffee consumption on the gut microbiota: a human volunteer study. Int J Food Microbiol. 2009;130: 117–121. 10.1016/j.ijfoodmicro.2009.01.011

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