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Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Functional short-chain carbohydrates (prebiotics) in the diet to improve the microbiome and health of the gastrointestinal tract

J. G. Muir A C , C. K. Yao A and P. G. Gibson A B
+ Author Affiliations
- Author Affiliations

A Department of Gastroenterology, Central Clinical School, Monash University, The Alfred Centre-Level 6, Commercial Road, Melbourne, Vic. 3004, Australia.

B Department of Gastroenterology, The Alfred Hospital, Commercial Road, Melbourne, Vic. 3004, Australia.

C Corresponding author. Email: jane.muir@monash.edu

Animal Production Science 55(12) 1376-1380 https://doi.org/10.1071/AN15277
Submitted: 4 June 2015  Accepted: 31 August 2015   Published: 20 October 2015

Abstract

Advancement in technologies to identify and quantify bacterial species in the gastrointestinal tract has escalated interest in its microbiome worldwide. There is enormous interest in understanding the roles that bacterial species play in gastrointestinal health and overall wellbeing. What constitutes a ‘healthy gut microbiome’ includes: favourable fermentation-dependent characteristics such as butyrate supply to all regions, minimisation of putrefaction of proteins, and adequate laxation. The relative abundance of specific bacterial species with certain functional characteristics is also important and include: traditional prebiotic bacteria – Bifidobacteria; strongly butyrate-producing – Clostridium coccoides and Faecalibacterium prausnitzi as well as a mucus-associated bacterium Akkermansia muciniphila. Manipulation of diet and dietary factors may be essential to favourably influence these fermentation-dependent parameters and select for growth of beneficial bacterial species. In this regard, this laboratory has identified indigestible oligosaccharides with prebiotic effects and now has an extensive database that quantifies indigestible oligosaccharides in a wide variety of foods including whole grains, cereals, legumes, seeds, nuts, fruits and vegetables. Future research in this area should consider the role of dietary components that best establish and maintain a ‘healthy gut microbiome’.

Additional keywords: gut microbiome, fermentation.


References

Barrett J, Gearry R, Muir J, Irving P, Rose R, Rosella O, Haines M, Shepherd S, Gibson P (2010) Dietary poorly absorbed, short‐chain carbohydrates increase delivery of water and fermentable substrates to the proximal colon. Alimentary Pharmacology & Therapeutics 31, 874–882.

Bedani R, Pauly-Silveira ND, Roselino MN, de Valdez GF, Rossi EA (2010) Effect of fermented soy product on the fecal microbiota of rats fed on a beef-based animal diet. Journal of the Science of Food and Agriculture 90, 233–238.
Effect of fermented soy product on the fecal microbiota of rats fed on a beef-based animal diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFarsrzI&md5=faca224ae70a5eb94a8aa06a2b385c7dCAS | 20355036PubMed |

Biesiekierski JR, Rosella O, Rose R, Liels K, Barrett JS, Shepherd SJ, Gibson PR, Muir JG (2011) Quantification of fructans, galacto-oligosaccharides and other short-chain carbohydrates in processed grains and cereals. Journal of Human Nutrition and Dietetics 24, 154–176.
Quantification of fructans, galacto-oligosaccharides and other short-chain carbohydrates in processed grains and cereals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjksVCisw%3D%3D&md5=5d1592cb87c7a63fd1cd05cd6d51d4d8CAS | 21332832PubMed |

Bindelle J, Buldgen A, Leterme P (2008) Nutritional and environmental consequences of dietary fibre in pig nutrition: a review. Biotechnologie, Agronomie, Société et Environnement 12, 69–80.

Birkett A, Muir J, Walker K, Jones G (1995) Dietary composition affects the levels of starch and protein reaching the human colon. Proceedings Nutrition Society of Australia 19, 42

Blachier F, Mariotti F, Huneau JF, Tome D (2007) Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 33, 547–562.
Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlSlsrnO&md5=bf98e5f5e2983cec1e2da9c86a1e3724CAS | 17146590PubMed |

Bourdu S, Dapoigny M, Chapuy E, Artigue F, Vasson MP, Dechelotte P, Bommelaer G, Eschalier A, Ardid D (2005) Rectal instillation of butyrate provides a novel clinically relevant model of noninflammatory colonic hypersensitivity in rats. Gastroenterology 128, 1996–2008.
Rectal instillation of butyrate provides a novel clinically relevant model of noninflammatory colonic hypersensitivity in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFKltr4%3D&md5=da817a19fc0c25ef6aff1c61948d9f5aCAS | 15940632PubMed |

Brownlee IA (2011) The physiological roles of dietary fibre. Food Hydrocolloids 25, 238–250.
The physiological roles of dietary fibre.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOit77F&md5=3ffe5a7502696ab2e5cbdc77fc21108dCAS |

Duncan SH, Belenguer A, Holtrop G, Johnstone AM, Flint HJ, Lobley GE (2007) Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces. Applied and Environmental Microbiology 73, 1073–1078.
Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlyqs7o%3D&md5=fbfdef6cbeff6371b926aa619941e5edCAS | 17189447PubMed |

Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nature Reviews. Gastroenterology & Hepatology 9, 577–589.
The role of the gut microbiota in nutrition and health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKmurrF&md5=2139d73000034b756feb2ed75af7700eCAS |

Gibson GR, Beatty ER, Wang X, Cummings JH (1995) Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology 108, 975–982.
Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlt1emt7g%3D&md5=d1771cd82264c43890d3255d1a9b1b18CAS | 7698613PubMed |

Govers M, Gannon N, Dunshea F, Gibson P, Muir J (1999) Wheat bran affects the site of fermentation of resistant starch and luminal indices related to colon cancer risk: a study in pigs. Gut 45, 840–847.
Wheat bran affects the site of fermentation of resistant starch and luminal indices related to colon cancer risk: a study in pigs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FjtFKqtA%3D%3D&md5=61504cdfed7eea26a46d81394578a917CAS | 10562582PubMed |

Guarner F, Hooper LV, Nunez G (2013) Understanding the microbiota in the midst of Renaissance architecture and olive groves. Nature Immunology 14, 101–105.
Understanding the microbiota in the midst of Renaissance architecture and olive groves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSlsrc%3D&md5=f7d47a2618eaf7e3dbfd732e63c93829CAS | 23334821PubMed |

Halmos EP, Power VA, Shepherd SJ, Gibson PR, Muir JG (2014) A diet low in FODMAPs reduces symptoms of irritable bowel syndrome. Gastroenterology 146, 67–75.e5.
A diet low in FODMAPs reduces symptoms of irritable bowel syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVShsLvP&md5=5395bd919eb341fd3533a8245bd54125CAS | 24076059PubMed |

Halmos EP, Christophersen CT, Bird AR, Shepherd SJ, Gibson PR, Muir JG (2015) Diets that differ in their FODMAP content alter the colonic luminal microenvironment. Gut 64, 93–100.
Diets that differ in their FODMAP content alter the colonic luminal microenvironment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitlOhu7g%3D&md5=27dd8f3f8f95ed935a53ff401f37ed9bCAS | 25016597PubMed |

Heinritz SN, Mosenthin R, Weiss E (2013) Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutrition Research Reviews 26, 191–209.
Use of pigs as a potential model for research into dietary modulation of the human gut microbiota.Crossref | GoogleScholarGoogle Scholar | 24134811PubMed |

Hoskins LC (1993) Mucin degradation in the human gastrointestinal tract and its significance to enteric microbial ecology. European Journal of Gastroenterology & Hepatology 5, 205–213.
Mucin degradation in the human gastrointestinal tract and its significance to enteric microbial ecology.Crossref | GoogleScholarGoogle Scholar |

Lin J, Peng L, Itzkowitz S, Holzman IR, Babyatsky MW (2005) Short-chain fatty acid induces intestinal mucosal injury in newborn rats and down-regulates intestinal trefoil factor gene expression in vivo and in vitro. Journal of Pediatric Gastroenterology and Nutrition 41, 607–611.
Short-chain fatty acid induces intestinal mucosal injury in newborn rats and down-regulates intestinal trefoil factor gene expression in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGhsL%2FP&md5=315a416cb4cf35adae19668ad7c44079CAS | 16254517PubMed |

Muir JG, Yeow EG, Keogh J, Pizzey C, Bird AR, Sharpe K, O’Dea K, Macrae FA (2004) Combining wheat bran with resistant starch has more beneficial effects on fecal indexes than does wheat bran alone. The American Journal of Clinical Nutrition 79, 1020–1028.

Muir JG, Shepherd SJ, Rosella O, Rose R, Barrett JS, Gibson PR (2007) Fructan and free fructose content of common Australian vegetables and fruit. Journal of Agricultural and Food Chemistry 55, 6619–6627.
Fructan and free fructose content of common Australian vegetables and fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsF2jsLc%3D&md5=e9a2862c01cb7d16daa40698df5b59ecCAS | 17625872PubMed |

Muir JG, Rose R, Rosella O, Liels K, Barrett JS, Shepherd SJ, Gibson PR (2009) Measurement of short-chain carbohydrates in common Australian vegetables and fruits by high-performance liquid chromatography (HPLC). Journal of Agricultural and Food Chemistry 57, 554–565.
Measurement of short-chain carbohydrates in common Australian vegetables and fruits by high-performance liquid chromatography (HPLC).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlaqsg%3D%3D&md5=5e03c7b84fc1a6ed6ea8c8d836855218CAS | 19123815PubMed |

Ong DK, Mitchell SB, Barrett JS, Shepherd SJ, Irving PM, Biesiekierski JR, Smith S, Gibson PR, Muir JG (2010) Manipulation of dietary short chain carbohydrates alters the pattern of gas production and genesis of symptoms in irritable bowel syndrome. Journal of Gastroenterology and Hepatology 25, 1366–1373.
Manipulation of dietary short chain carbohydrates alters the pattern of gas production and genesis of symptoms in irritable bowel syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFahsLnN&md5=195c0c77fccc1ade695f61ff304e125fCAS | 20659225PubMed |

Pieper R, Kroger S, Richter JF, Wang J, Martin L, Bindelle J, Htoo JK, von Smolinski D, Vahjen W, Zentek J, Van Kessel AG (2012) Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. The Journal of Nutrition 142, 661–667.
Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFals7s%3D&md5=ab0c3200f3e312a0bea12f3ed9f59ba9CAS | 22357743PubMed |

Quigley EMM (2011) The enteric microbiota in the pathogenesis and management of constipation. Best Practice & Research. Clinical Gastroenterology 25, 119–126.
The enteric microbiota in the pathogenesis and management of constipation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3ksl2ksg%3D%3D&md5=1e338afa2d381c43307ce075184cc436CAS |

Rao AV (1999) Dose-response effects of inulin and oligofructose on intestinal bifidogenesis effects. The Journal of Nutrition 129, 1442S–1445S.

Rist VT, Weiss E, Eklund M, Mosenthin R (2013) Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review. Animal 7, 1067–1078.
Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotlelsbc%3D&md5=3e77243c86c67cf7aaccb2b5d3113ee2CAS | 23410993PubMed |

Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, Wolvers D, Watzl B, Szajewska H, Stahl B, Guarner F, Respondek F, Whelan K, Coxam V, Davicco M-J, Léotoing L, Wittrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A (2010) Prebiotic effects: metabolic and health benefits. British Journal of Nutrition 104, S1–S63.
Prebiotic effects: metabolic and health benefits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1GjsLfK&md5=bc311a5c5bfaa1a1a9d0064bc2c4cb4bCAS | 20920376PubMed |

Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, Duncan G, Johnstone AM, Lobley GE, Wallace RJ, Duthie GG, Flint HJ (2011) High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. The American Journal of Clinical Nutrition 93, 1062–1072.
High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlCqsbc%3D&md5=997f1cbd8410b5eea2f0628a239fa7f8CAS | 21389180PubMed |

Scheppach W, Bartram HP, Richter F (1995) Role of short-chain fatty acids in the prevention of colorectal cancer. European Journal of Cancer 31, 1077–1080.
Role of short-chain fatty acids in the prevention of colorectal cancer.Crossref | GoogleScholarGoogle Scholar |

Scheppach W, Luehrs H, Menzel T (2001) Beneficial health effects of low-digestible carbohydrate consumption. British Journal of Nutrition 85, S23–S30.
Beneficial health effects of low-digestible carbohydrate consumption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivVakt78%3D&md5=501809c6d8ad2c366ad775eb9f9f657aCAS | 11321025PubMed |

Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacological Research 69, 52–60.
The influence of diet on the gut microbiota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1KisLs%3D&md5=abc36a318e6eb1223acf7f2ac6af5ca4CAS | 23147033PubMed |

Staudacher H, Lomer M, Anderson J, Barrett J, Muir J, Irving P, Whelan K (2012) Fermentable carbohydrate restriction reduces luminal bifidobacteria and gastrointestinal symptoms in patients with irritable bowel syndrome. The Journal of Nutrition 142, 1510–1518.

Topping DL, Gooden JM, Brown IL, Biebrick DA, McGrath L, Trimble RP, Choct M, Illman RJ (1997) A high amylose (amylomaize) starch raises proximal large bowel starch and increases colon length in pigs. The Journal of Nutrition 127, 615–622.

Tremaroli V, Backhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489, 242–249.
Functional interactions between the gut microbiota and host metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtleqsrzI&md5=5c62ee4a90e238574dde0ee066ddf331CAS | 22972297PubMed |

Tuohy KM, Rouzaud GCM, Bruck WM, Gibson GR (2005) Modulation of the human gut microflora towards improved health using prebiotics – assessment of efficacy. Current Pharmaceutical Design 11, 75–90.
Modulation of the human gut microflora towards improved health using prebiotics – assessment of efficacy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFGqsg%3D%3D&md5=84041e3e2ad8564cddb225b8cf6c9b5aCAS | 15638753PubMed |

Weinstock GM (2012) Genomic approaches to studying the human microbiota. Nature 489, 250–256.
Genomic approaches to studying the human microbiota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtleqsrzO&md5=ab65221d19db936964a95725d577fbdeCAS | 22972298PubMed |

Wenk C (2001) The role of dietary fibre in the digestive physiology of the pig. Animal Feed Science and Technology 90, 21–33.
The role of dietary fibre in the digestive physiology of the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXislGmtbk%3D&md5=e86c042033007ff953aa7430653ae0b5CAS |

Williams CH, Witherly SA, Buddington RK (1994) Influence of dietary neosugar on selected bacterial groups of the human faecal microbiota. Microbial Ecology in Health and Disease 7, 91–97.
Influence of dietary neosugar on selected bacterial groups of the human faecal microbiota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvFKlur4%3D&md5=39667b78ceb9f0287e058c5659a62f77CAS |