Advertisement

The effects of inulin on gut microbial composition: a systematic review of evidence from human studies

  • Quentin Le Bastard
  • Guillaume Chapelet
  • François Javaudin
  • Didier Lepelletier
  • Eric Batard
  • Emmanuel MontassierEmail author
Review

Abstract

Background

Inulin, consisting of repetitive fructosyl units linked by β(2,1) bonds, is a readily fermentable fiber by intestinal bacteria that generates large quantities of short-chain fatty acids (SCFA). In individuals with constipation, it was reported that inulin ingestion was associated with a significant increase in stool frequency, suggesting a potential impact of inulin on human gut microbiota composition. Progress in high-throughput technologies allow assessment of human-associated microbiomes in terms of diversity and taxonomic or functional composition, and can identify changes in response to a specific supplementation. Hence, to understand the effects of inulin on the human gut microbiome is pivotal to gain insight into their mechanisms of action.

Methods

Here, we conducted a systematic review of human studies in adult individuals showing the effects of inulin on the gut microbiome. We searched in MEDLINE, EMBASE, Web of Science, and Scopus databases for articles in English published in peer-reviewed journals and indexed up until March 2019. We used multiple search terms capturing gut microbiome, gut microflora, intestinal microbiota, intestinal flora, gut microbiota, gut flora, microbial gut community, gut microbial composition, and inulin.

Results

Overall, nine original articles reported the effects of inulin on microbiome composition in adult humans, most of them being randomized, double-blind, placebo-controlled trials (n = 7). Studies varied significantly in design (3 studies associated inulin and oligofructose), supplementation protocols (from 5 to 20 gr per day of inulin consumed) and in microbiome assessment methods (16S sequencing, n = 7). The most consistent change was an increase in Bifidobacterium. Other concordant results included an increase in relative abundance of Anaerostipes, Faecalibacterium, and Lactobacillus, and a decrease in relative abundance of Bacteroides after inulin supplementation.

Conclusions

Our systematic review assessed the evidence for the effects of inulin supplementation on the human gut microbiome. However, these in vivo studies did not confirm in vitro experiments as the taxonomic alterations were not associated with increase in short-chain fatty acids levels.

Keywords

Inulin Prebiotic Gut microbiome Diversity Short-chain fatty acids 

Abbreviations

OTU

Operational taxonomic unit

SCFA

Short-chain fatty acids

Notes

Authors’ contributions

Q.L.B, G.C., F.J, D.L., E.B., and E.M. directly participated in study design and protocol preparation. Q.L.B and E.M. screened abstracts and titles for inclusion. Q.L.B, G.C., F.J, and E.M. participated in review of full-text articles. E.M. drafted the manuscript. All authors participated in manuscript editing and critical review.

Compliance with ethical standards

Competing interests

The authors declare that they have no competing interests.

Ethics approval and consent to participate

Not applicable.

Supplementary material

10096_2019_3721_MOESM1_ESM.docx (15 kb)
Additional file 1. Literature Search Algorithms (DOCX 14 kb)

References

  1. 1.
    Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412CrossRefGoogle Scholar
  2. 2.
    Ellegard L, Andersson H, Bosaeus I (1997) Inulin and oligofructose do not influence the absorption of cholesterol, or the excretion of cholesterol, Ca, Mg, Zn, Fe, or bile acids but increases energy excretion in ileostomy subjects. Eur J Clin Nutr 51:1–5CrossRefGoogle Scholar
  3. 3.
    Roberfroid M, Slavin J (2000) Nondigestible oligosaccharides. Crit Rev Food Sci Nutr 40:461–480CrossRefGoogle Scholar
  4. 4.
    Micka A, Siepelmeyer A, Holz A, Theis S, Schön C (2017) Effect of consumption of chicory inulin on bowel function in healthy subjects with constipation: a randomized, double-blind, placebo-controlled trial. Int J Food Sci Nutr 68:82–89CrossRefGoogle Scholar
  5. 5.
    EFSA Panel on Dietic Products Nutrition and Allergies (NDA) (2015) Scientific opinion on the substantiation of a health claim related to “native chicory inulin” and maintenance of normal defecation by increasing stool frequency pursuant to Article of Regulation (EC) No 1924/2006. EFSA J 13:3951CrossRefGoogle Scholar
  6. 6.
    Ford AC, Moayyedi P, Chey WD, Harris LA, Lacy BE, Saito YA, Quigley EMM, ACG task force on management of irritable bowel syndrome (2018) American College of Gastroenterology Monograph on Management of Irritable Bowel Syndrome. Am J Gastroenterol 113:1–18CrossRefGoogle Scholar
  7. 7.
    Singh V, Yeoh BS, Walker RE (2019) Microbiota fermentation-NLRP3 axis shapes the impact of dietary fibres on intestinal inflammation. Gut. 316250Google Scholar
  8. 8.
    Bafeta A, Koh M, Riveros C, Ravaud P (2018) Harms reporting in randomized controlled trials of interventions aimed at modifying microbiota: a systematic review. Ann Intern Med 169:240–247CrossRefGoogle Scholar
  9. 9.
    Durack J, Lynch SV (2019) The gut microbiome: relationship with disease and opportunities for therapy. J Exp Med 216:20–40CrossRefGoogle Scholar
  10. 10.
    Shmagel A, Demmer R, Knights D, Butler M, Langsetmo L, Lane NE, Ensrud K (2019) Effects of glucosamine and chondroitin sulfate on gut microbial composition: a systematic review of evidence from animal and human studies. Nutrients. 11:2CrossRefGoogle Scholar
  11. 11.
    Le Bastard Q, Al-Ghalith GA, Grégoire M, Chapelet G, Javaudin F, Dailly E, Batard E, Knights D, Montassier E (2018) Systematic review: human gut dysbiosis induced by non-antibiotic prescription medications. Aliment Pharmacol Ther 47:332–345CrossRefGoogle Scholar
  12. 12.
    Claesson MJ, Clooney AG, O’Toole PW (2017) A clinician’s guide to microbiome analysis. Nat Rev Gastroenterol Hepatol 14:585–595CrossRefGoogle Scholar
  13. 13.
    Tyler AD, Smith MI, Silverberg MS (2014) Analyzing the human microbiome: a "how to" guide for physicians. Am J Gastroenterol 109:983–993CrossRefGoogle Scholar
  14. 14.
  15. 15.
    Vandeputte D, Falony G, Vieira-Silva S, Wang J, Sailer M, Theis S, Verbeke K, Raes J (2017) Prebiotic inulin-type fructans induce specific changes in the human gut microbiota. Gut. 66:1968–1974CrossRefGoogle Scholar
  16. 16.
    Holscher HD, Bauer LL, Gourineni V, Pelkman CL, Fahey GC Jr, Swanson KS (2015) Agave inulin supplementation affects the fecal microbiota of healthy adults participating in a randomized, double-blind, placebo-controlled, crossover trial. J Nutr 145:2025–2032CrossRefGoogle Scholar
  17. 17.
    Baxter NT, Schmidt AW, Venkataraman A, Kim KS, Waldron C, Schmidt TM (2019) Dynamics of human gut microbiota and short- chain fatty acids in response to dietary interventions with three fermentable fibers. MBio. 10:e02566–e02518CrossRefGoogle Scholar
  18. 18.
    Healey G, Murphy R, Butts C, Brough L, Whelan K, Coad J (2018) Habitual dietary fibre intake influences gut microbiota response to an inulin-type fructan prebiotic: a randomised, double-blind, placebo-controlled, cross-over, human intervention study. Br J Nutr 119:176–189CrossRefGoogle Scholar
  19. 19.
    Reimer RA, Willis HJ, Tunnicliffe JM, Park H, Madsen KL, Soto-Vaca A (2017) Inulin type fructans and whey protein both modulate appetite but only fructans alter gut microbiota in adults with overweight/obesity: A randomized controlled trial. Mol Nutr Food Res 61Google Scholar
  20. 20.
    Dewulf EM, Cani PD, Claus SP, Fuentes S, Puylaert PG, Neyrinck AM, Bindels LB, de Vos WM, Gibson GR, Thissen JP, Delzenne NM (2013) Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut. 62:1112–1121CrossRefGoogle Scholar
  21. 21.
    Valcheva R, Koleva P, Martínez I, Walter J, Gänzle MG, Dieleman LA (2019) Inulin-type fructans improve active ulcerative colitis associated with microbiota changes and increased short-chain fatty acids levels. Gut Microbes 10:334–357CrossRefGoogle Scholar
  22. 22.
    Costabile A, Kolida S, Klinder A, Gietl E, Bäuerlein M, Frohberg C, Landschütze V, Gibson GR (2010) A double-blind, placebo-controlled, cross-over study to establish the bifidogenic effect of a very-long-chain inulin extracted from globe artichoke (Cynara scolymus) in healthy human subjects. Br J Nutr 104:1007–1017CrossRefGoogle Scholar
  23. 23.
    Joossens M, De Preter V, Ballet V, Verbeke K, Rutgeerts P, Vermeire S (2012) Effect of oligofructose-enriched inulin (OF-IN) on bacterial composition and disease activity of patients with Crohn’s disease: results from a double-blinded randomised controlled trial. Gut. 61:958CrossRefGoogle Scholar
  24. 24.
    Rossi M, Corradini C, Amaretti A, Nicolini M, Pompei A, Zanoni S, Matteuzzi D (2005) Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study of pure and fecal cultures. Appl Environ Microbiol 71:6150–6158CrossRefGoogle Scholar
  25. 25.
    Hughes SA, Shewry PR, Li L, Gibson GR, Sanz ML, Rastall RA (2007) In vitro fermentation by human faecal microflora of wheat arabinoxylans. J Agric Food Chem 55:4589–4595CrossRefGoogle Scholar
  26. 26.
    Kolida S, Gibson GR (2007) Prebiotic capacity of inulinfructans. J Nutr 137:2503–2506CrossRefGoogle Scholar
  27. 27.
    Allen-Vercoe E, Daigneault M, White A, Panaccione R, Duncan SH, Flint HJ, O’Neal L, Lawson PA (2012) Anaerostipes hadrus comb. nov., a dominant species within the human colonic microbiota; reclassification of Eubacterium hadrum Moore et al. 1976. Anaerobe. 18:523–529CrossRefGoogle Scholar
  28. 28.
    Duncan SH, Louis P, Flint HJ (2004) Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product. Appl Environ Microbiol 70:5810–5817CrossRefGoogle Scholar
  29. 29.
    Moens F, De Vuyst L (2007) Inulin-type fructan degradation capacity of Clostridium cluster IV and XIVa butyrate-producing colon bacteria and their associated metabolic outcomes. Benefic Microbes 8:473–490CrossRefGoogle Scholar
  30. 30.
    Deehan EC, Duar RM, Armet AM, Perez-Muñoz ME, Jin M, Walter J (2017) Modulation of the gastrointestinal microbiome with nondigestible fermentable carbohydrates to improve human health. Microbiol Spectr 5:5Google Scholar
  31. 31.
    Zhernakova A, Kurilshikov A, Bonder MJ, Tigchelaar EF, Schirmer M, Vatanen T, Mujagic Z, Vila AV, Falony G, Vieira-Silva S et al (2016) Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 352:565–569CrossRefGoogle Scholar
  32. 32.
    Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D (2016) Population-level analysis of gut microbiome variation. Science. 352:560–564CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Microbiotas Hosts Antibiotics and bacterial Resistances (MiHAR)Université de NantesNantesFrance
  2. 2.Department of Emergency MedicineCHU NantesNantesFrance
  3. 3.Pole de gérontologie cliniqueCentre hospitalier universitaire de NantesNantesFrance
  4. 4.Bacteriology and Infection Control DepartmentNantes University HospitalNantesFrance
  5. 5.EA3826 Thérapeutiques Anti-Infectieuses, Institut de Recherche en Santé 2 Nantes BiotechUniversity of NantesNantesFrance

Personalised recommendations