Skip to main content
×
×
Home

Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study

  • Adele Costabile (a1), Annett Klinder (a1), Francesca Fava (a1), Aurora Napolitano (a2), Vincenzo Fogliano (a2), Clare Leonard (a3), Glenn R. Gibson (a1) and Kieran M. Tuohy (a1)...
Abstract

Epidemiological studies have shown an inverse association between dietary intake of whole grains and the risk of chronic disease. This may be related to the ability to mediate a prebiotic modulation of gut microbiota. However, no studies have been conducted on the microbiota modulatory capability of whole-grain (WG) cereals. In the present study, the impact of WG wheat on the human intestinal microbiota compared to wheat bran (WB) was determined. A double-blind, randomised, crossover study was carried out in thirty-one volunteers who were randomised into two groups and consumed daily 48 g breakfast cereals, either WG or WB, in two 3-week study periods, separated by a 2-week washout period. Numbers of faecal bifidobacteria and lactobacilli (the target genera for prebiotic intake), were significantly higher upon WG ingestion compared with WB. Ingestion of both breakfast cereals resulted in a significant increase in ferulic acid concentrations in blood but no discernible difference in faeces or urine. No significant differences in faecal SCFA, fasting blood glucose, insulin, total cholesterol (TC), TAG or HDL-cholesterol were observed upon ingestion of WG compared with WB. However, a significant reduction in TC was observed in volunteers in the top quartile of TC concentrations upon ingestion of either cereal. No adverse intestinal symptoms were reported and WB ingestion increased stool frequency. Daily consumption of WG wheat exerted a pronounced prebiotic effect on the human gut microbiota composition. This prebiotic activity may contribute towards the beneficial physiological effects of WG wheat.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Dr A. Costabile, fax +44 (0)118 931 0080, email a.costabile@reading.ac.uk
References
Hide All
1 Jacobs, DR Jr, Marquart, L, Slavin, J & Kushi, LH (1998) Whole-grain intake and cancer: an expanded review and meta-analysis. Nutr Cancer 30, 8596.
2 Anderson, JW, Hanna, TJ, Peng, X & Kryscio, RJ (2000) Whole grain foods and heart disease risk. J Am Coll Nutr 19, 291S299S.
3 Kushi, LH, Meyer, KA & Jacobs, DR Jr (1999) Cereals, legumes, and chronic disease risk reduction: evidence from epidemiologic studies. Am J Clin Nutr 3, 451S458S.
4 Slavin, J (2003) Why whole grains are protective: biological mechanisms. Proc Nutr Soc 62, 129134.
5 Rastall, RA, Gibson, GR, Gill, HS, Guarner, F, Klaenhammer, TR, Pot, B, Reid, G, Rowland, IR & Sanders, ME (2005) Modulation of the microbial ecology of the human colon by probiotics, prebiotics and synbiotics to enhance human health: an overview of enabling science and potential applications. FEMS 52, 145152.
6 Fava, F, Gitau, R, Lovegrove, J & Tuohy, KM (2006) The gut microflora and lipid metabolism: implications for human health. Curr Med Chem 13, 30053021.
7 Cummings, JH, Antoine, JM, Azpiroz, F, et al. (2004) PASSCLAIM-gut health and immunity. Eur J Nutr 43, II118II173.
8 Rakoff-Nahoum, S, Paglino, J, Eslami-Varzaneh, F, Edberg, S & Medzhitov, R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118, 229241.
9 Gibson, GR & Roberfroid, MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125, 14011412.
10 Abrams, SA, Griffin, IJ, Hawthorne, KM, Liang, L, Gunn, SK, Darlington, G & Ellis, KJ (2005) A combination of prebiotic short- and long-chain inulin-type fructans enhances calcium absorption and bone mineralization in young adolescents. Am J Clin Nutr 82, 471476.
11 Williams, CM & Jackson, KG (2002) Inulin and oligofructose: effects on lipid metabolism from human studies. Br J Nutr 87, S261S264.
12 Burns, AJ & Rowland, IR (2004) Antigenotoxicity of probiotics and prebiotics on faecal water-induced DNA damage in human colon adenocarcinoma cells. Mutat Res 551, 233243.
13 Klinder, A, Förster, A, Caderni, G, Femia, AP & Pool-Zobel, BL (2004) Faecal water genotoxicity is predictive of tumor preventive activities by inulin-like oligofructoses, probiotics (Lactobacillus rhamnosus and Bifidobacterium lactis) and their synbiotic combination. Nutr Cancer 49, 144155.
14 Pool-Zobel, BL (2005) Inulin-type fructans and reduction in colon cancer risk: review of experimental and human data. Br J Nutr 93, S73S90.
15 Esposito, F, Arlotti, G, Napolitano, A, Vitale, D & Fogliano, V (2005) Durum wheat bran by-products: a novel functional ingredients. Food Res Int 38, 11671173.
16 Wong, JM, de Souza, R, Kendall, CW, Emam, A & Jenkins, DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40, 235243.
17 Scalbert, A, Morand, C, Manach, C & Remesy, C (2002) Absorption and metabolism of polyphenols in the gut and impact on health. Biomed Pharmacother 56, 276282.
18 Tuohy, KM, Kolida, S, Lustenberger, AM & Gibson, GR (2001) The prebiotic effects of biscuits containing partially hydrolysed guar gum and fructo-oligosaccharides – a human volunteer study. Br J Nutr 86, 341348.
19 Harmsen, HJM, Wildeboer-Veloo, ACM, Grijpstra, J, Knol, J, Degener, JE & Welling, GW (2000) Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human faeces from volunteers of different age groups. Appl Environ Microbiol 66, 45234527.
20 Manz, W, Amann, R, Ludwig, W, Vancanneyt, M & Schleifer, KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiol 142, 10971106.
21 Langendijk, PS, Schut, F, Jansen, GJ, Raangs, GC, Kamphuis, GR, Wilkinson, MH & Welling, GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in faecal samples. Appl Environ Microbiol 61, 30693075.
22 Franks, AH, Harmsen, HJM, Raangs, GC, Jansen, GJ, Schut, F & Welling, GW (1998) Variations of bacterial populations in human faeces measured by fluorescence in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64, 33363345.
23 Harmsen, HJM, Elfferich, P, Schut, F & Welling, GW (1999) A 16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescence in situ hybridization. Microb Ecol Health Dis 11, 312.
24 Kroon, PA, Faulds, CB, Ryden, P, Robertson, JA, Williamson, G & Garcia-Conesa, MT (1997) Release of covalently bound of ferulic acid from fibre in the human colon. J Agric Food Chem 45, 661667.
25 Singh, NP, McCoy, MT, Tice, RR & Schneider, EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175, 184191.
26 Pool-Zobel, BL, Bub, A, Müller, H, Wollowski, I & Rechkemmer, G (1997) Consumption of vegetables reduces genetic damage in humans: first results of an intervention trial with carotenoid-rich foods. Carcinogenesis 18, 18471850.
27 Gibson, GR, Probert, HM, Van Loo, J, Rastall, RA & Roberfroid, MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17, 259275.
28 Chen, HL, Lu, YH, Lin, JJ & Ko, LY (2001) Effects of isomalto-oligosaccharides on bowel functions and indicators of nutritional status in constipated elderly men. J Am Coll Nutr 20, (1), 4449.
29 Den Hond, E, Geypens, B & Ghoos, Y (2000) Effect of high performance chicory inulin on constipation. Nutr Res 20, 731736.
30 Gibson, GR, Beatty, ER, Wang, X & Cummings, JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975982.
31 Kleessen, B, Sykura, B, Zunft, HJ & Blaut, M (1997) Effects of inulin and lactose on fecal microflora, microbial activity, and bowel habit in elderly constipated persons. Am J Cli Nutr 65, 13971402.
32 Wang, HF, Lim, PS, Kao, MD, Chan, EC, Lin, LC & Wang, NP (2001) Use of isomalto-oligosaccharide in the treatment of lipid profiles and constipation in hemodialysis patients. Ren Nutr 11, 7379.
33 Coudray, C, Bellanger, J, Castiglia-Delavaud, C, Remesy, C, Vermorel, M & Rayssignuier, Y (1997) Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron, and zinc in healthy young men. Eur J Clin Nutr 51, 375380.
34 Griffin, IJ, Davila, PM & Abrams, SA (2002) Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. Br J Nutr 87, S187S191.
35 Van den Heuvel, EGH, Muys, T, Van Dokkum, W & Schaafsma, G (1997) Lactulose stimulates calcium absorption in postmenopausal women. J Bone Miner Res 7, 12111216.
36 Van den Heuvel, EGH, Muys, T, Van Dokkum, W & Schaafsma, G (1999) Oligofructose stimulates calcium absorption in adolescents. Am J Clin Nutr 69, 544548.
37 Rafter, J, Bennett, M, Caderni, G, et al. (2007) Dietary synbiotics reduce cancer risk factors in polypectomized and colon cancer patients. Am J Clin Nutr 85, 488496.
38 Hidaka, H, Tashiro, Y & Eida, T (1991) Proliferation of bifidobacteria by oligosaccharides and their useful effect on human health. Bifid Microflora 10, 6579.
39 Davidson, MH, Synecki, C, Maki, KC & Drennan, KB (1998) Effects of dietary inulin in serum lipids in men and women with hypercholesterolemia. Nutr Res 3, 503517.
40 Causey, JL, Feirtag, JM, Gallaher, DD, Tungland, BC & Slavin, JL (2000) Effects of dietary inulin on serum lipids, blood glucose and the gastrointestinal environment in hypercholesterolemic men. Nutr Res 20, 191201.
41 Shaw, DI, Hall, WL & Williams, CM (2005) Metabolic syndrome: what is it and what are the implications? Proc Nutr Soc 64, (3), 349357.
42 Leitch, EC, Walker, AW, Duncan, SH, Holtrop, G & Flint, HJ (2007) Selective colonization of insoluble substrates by human faecal bacteria. Environ Microbiol 9, 667679.
43 Ahmed, R, Segal, I & Hassan, H (2000) Fermentation of dietary starch in humans. Am J Gastroenterology 95, 10171020.
44 Alles, MS, Hartemink, R, Meyboom, S, Harryvan, JL, Van Laere, KMJ, Nagengast, FM & Hautvast, JGAJ (1999) Effects of transgalactooligosaccharides on the composition of the human intestinal microflora and on putative risk markers for colon cancer. Am J Clin Nutr 69, 980991.
45 Bouhnik, Y, Neut, C, Raskine, L, Michel, C, Riottot, M, Andrieux, C, Guillemot, F, Dyard, F & Flourie, B (2004) Prospective, randomized, parallel-group trial to evaluate the effects of lactulose and polyethylene glycol-4000 on colonic flora in chronic idiopathic constipation. Alimentary Pharm & Therapeutics 19, 889899.
46 Brighenti, F, Casiraghi, MC, Canzi, E & Ferrari, A (1999) Effect of consumption of a ready-to-eat breakfast cereal containing inulin on the intestinal milieu and blood lipids in healthy male volunteers. Eur J Clin Nutr 53, 726733.
47 Hylla, S, Gostner, A, Dusel, G, Anger, H, Batram, H-P, Christl, SU, Kasper, H & Scheppach, W (1998) Effects of resistant starch on the colon in healthy volunteers: possible implications for cancer prevention. Am J Clin Nutr 67, 136142.
48 Kruse, H-P, Kleessen, B & Blaut, M (1999) Effects of inulin on faecal bifidobacteria in human subjects. Br J Nutr 82, 375382.
49 Campbell, JM, Fahey, GC & Wolf, BW (1997) Selected indigestible oligosaccharides affect large bowel mass, cecal and faecal short-chain fatty acids, pH and microflora in rats. J Nutr 127, 130136.
50 Kleessen, B, Stoof, G, Proll, J, Schmiedl, D, Noack, J & Blaut, M (1997) Feeding resistant starch affects faecal and caecal microflora and short-chain fatty acids in rats. J Anim Sci 75, 24532462.
51 Kern, SM, Bennett, RN, Mellon, FA, Kroon, PA & Garcia-Conesa, MT (2003) Absorption of hydroxycinnamates in humans after high-bran cereal consumption. J Agric Food Chem 51, 60506055.
52 Andreasen, MF, Landbo, AK, Christensen, LP, Hansen, A & Meyer, AS (2001) Antioxidant effects of phenolic rye (Secale cereale L.) extracts, monomeric hydroxycinnamates, and ferulic acid dehydrodimers on human low-density lipoproteins. J Agric Food Chem 51, 40904096.
53 Scalbert, A & Williamson, (2000) Dietary intake and bioavailabity of polyphenols. J Nutr 130, 2073S2085S.
54 Natella, F, Belelli, F, Gentili, V, Ursini, F & Scaccini, C (2002) Grape seed proanthocyanidins prevent plasma postprandial oxidative stress in humans. J Agric Food Chem 50, 77207725.
55 Cremin, P, Kasim-Karakas, S & Waterhouse, AL (2001) LC/ES-MS detection of hydroxycinnamates in human plasma and urine. J Agric Food Chem 49, 17471750.
56 Rondini, L, Peyrat-Maillard, MN, Marsset-Bagliéri, A & Berset, C (2002) Sulfated ferulic acid is the main in vivo metabolite found after short-term ingestion of free ferulic acid in rats. J Agric Food Chem 50, 30373041.
57 Rondini, L, Peyrat-Maillard, MN, Marsset-Baglieri, A, Fromentin, G, Durand, P, Tomé, D, Prost, M & Berset, C (2004) Bound ferulic acid from bran is more bioavailable than the free compound in rat. J Agric Food Chem 52, 43384343.
58 Osswald, K, Becker, TW, Grimm, M, Jahreis, G & Pool-Zobel, BL (2000) Inter- and intra-individual variation of faecal water – genotoxicity in human colon cells. Mut Res 472, 5970.
59 Venturi, M, Hambly, RJ, Glinghammar, B, Rafter, JJ & Rowland, IR (1997) Genotoxic activity in human faecal water and the role of bile acids: a study using the alkaline comet assay. Carcinogenesis 18, 23532359.
60 Woods, JA, Dunne, C, Collins, JK, Shanahan, F & O'Brien, NM (2002) Genotoxicity of fecal water in a free-living Irish population. Nutr Cancer 42, (1), 6269.
61 Cross, AJ, Greetham, HL, Pollock, JR, Rowland, IR & Bingham, SA (2006) Variability in fecal water genotoxicity, determined using the Comet assay, is independent of endogenous N-nitroso compound formation attributed to red meat consumption. Environ Mol Mutagen 47, (3), 179184.
62 Klinder, A, Karlsson, PC, Clune, Y, Hughes, R, Glei, M, Rafter, J, Rowland, IR, Collins, JK & Pool-Zobel, BL (2007) Faecal water as a non-invasive biomarker in nutritional intervention: comparison of preparation methods and refinements of different endpoints. Accepted for publication in Nutr Cancer 57, (2), 158167.
63 Luo, J, Rizkalla, SW, Alamowitch, C, et al. (1996) Chronic consumption of short-chain fructooligosaccharides by healthy subjects decreased basal hepatic glucose production but had no effect on insulin stimulated glucose mechanism. Am J Clin Nutr 63, 939945.
64 Pedersen, A, Sandström, B & Van Amelsvoort, JMM (1997) The effect of ingestion of inulin on blood lipids and gastrointestinal symptoms in healthy females. Br J Nutr 78, 215222.
65 Alles, MS, De Roos, NM, Bakz, JC, Van de Lisdonk, E, Zock, PL & Hautvast, JGAJ (1999) Consumption of fructo-oligosaccharides does not favorably affect blood glucose and serum lipid concentrations in patients with type 2 diabetes. Am J Clin Nutr 69, 6469.
66 Jackson, KG, Taylor, GRJ, Clohessy, AM & Williams, CM (1998) The effect of the daily intake of inulin on fasting lipid, insulin and glucose concentrations in middle-aged men and women. Br J Nutr 82, 2330.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 130
Total number of PDF views: 751 *
Loading metrics...

Abstract views

Total abstract views: 2152 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th September 2018. This data will be updated every 24 hours.