Review
. 2014 Oct; 20(40):14805-20.
doi: 10.3748/wjg.v20.i40.14805.

Intestinal microbiota pathogenesis and fecal microbiota transplantation for inflammatory bowel disease

Zi-Kai Wang 1 Yun-Sheng Yang 1 Ye Chen 1 Jing Yuan 1 Gang Sun 1 Li-Hua Peng 1 
Affiliations
  • PMID: 25356041
  •     148 References
  •     36 citations

Abstract

The intestinal microbiota plays an important role in inflammatory bowel disease (IBD). The pathogenesis of IBD involves inappropriate ongoing activation of the mucosal immune system driven by abnormal intestinal microbiota in genetically predisposed individuals. However, there are still no definitive microbial pathogens linked to the onset of IBD. The composition and function of the intestinal microbiota and their metabolites are indeed disturbed in IBD patients. The special alterations of gut microbiota associated with IBD remain to be evaluated. The microbial interactions and host-microbe immune interactions are still not clarified. Limitations of present probiotic products in IBD are mainly due to modest clinical efficacy, few available strains and no standardized administration. Fecal microbiota transplantation (FMT) may restore intestinal microbial homeostasis, and preliminary data have shown the clinical efficacy of FMT on refractory IBD or IBD combined with Clostridium difficile infection. Additionally, synthetic microbiota transplantation with the defined composition of fecal microbiota is also a promising therapeutic approach for IBD. However, FMT-related barriers, including the mechanism of restoring gut microbiota, standardized donor screening, fecal material preparation and administration, and long-term safety should be resolved. The role of intestinal microbiota and FMT in IBD should be further investigated by metagenomic and metatranscriptomic analyses combined with germ-free/human flora-associated animals and chemostat gut models.

Keywords: Fecal microbiota transplantation; Inflammatory bowel disease; Intestinal microbiota; Probiotics; Synthetic microbiota transplantation.

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Patient attitudes toward the use of fecal microbiota transplantation in the treatment of recurrent Clostridium difficile infection.
Jonathan S Zipursky, Tivon I Sidorsky, +2 authors, Kathryn B Kirkland.
Clin Infect Dis, 2012 Sep 20; 55(12). PMID: 22990849
Durable alteration of the colonic microbiota by the administration of donor fecal flora.
Martin J Grehan, Thomas Julius Borody, +3 authors, Antony Wettstein.
J Clin Gastroenterol, 2010 Aug 19; 44(8). PMID: 20716985
Meta-analysis: the effect and adverse events of Lactobacilli versus placebo in maintenance therapy for Crohn disease.
J Shen, H Z Ran, +2 authors, D S Xiao.
Intern Med J, 2009 Feb 18; 39(2). PMID: 19220543
Inflammatory bowel disease associated with Yersinia enterocolitica O:3 infection.
Arve Saebo, Einar Vik, Ove J Lange, Ludwig Matuszkiewicz.
Eur J Intern Med, 2005 Jun 22; 16(3). PMID: 15967332
Effect of faecal stream diversion on recurrence of Crohn's disease in the neoterminal ileum.
P Rutgeerts, K Goboes, +5 authors, G Vantrappen.
Lancet, 1991 Sep 28; 338(8770). PMID: 1681159
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Mucosa-associated but not luminal Escherichia coli is augmented in Crohn's disease and ulcerative colitis.
Helton Luis de Souza, Vanessa R de Carvalho, +3 authors, Josias Rodrigues.
Gut Pathog, 2012 Dec 14; 4(1). PMID: 23234341    Free PMC article.
Fecal bacteriotherapy for ulcerative colitis: patients are ready, are we?
Stacy A Kahn, Rita Gorawara-Bhat, David T Rubin.
Inflamm Bowel Dis, 2011 May 28; 18(4). PMID: 21618362    Free PMC article.
Adherent-invasive Escherichia coli in inflammatory bowel disease.
Nathalie Rolhion, Arlette Darfeuille-Michaud.
Inflamm Bowel Dis, 2007 May 04; 13(10). PMID: 17476674
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Reduced diversity and imbalance of fecal microbiota in patients with ulcerative colitis.
Hideyuki Nemoto, Keiko Kataoka, +6 authors, Koji Yasutomo.
Dig Dis Sci, 2012 May 25; 57(11). PMID: 22623042
Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases.
Daniel N Frank, Allison L St Amand, +3 authors, Norman R Pace.
Proc Natl Acad Sci U S A, 2007 Aug 19; 104(34). PMID: 17699621    Free PMC article.
Highly Cited.
Secukinumab failure in Crohn's disease: the yeast connection?
Jean Frédéric Colombel, Boualem Sendid, Thierry Jouault, Daniel Poulain.
Gut, 2012 Dec 13; 62(5). PMID: 23232049
Inflammatory bowel disease in Asia: a systematic review.
Lani Prideaux, Michael A Kamm, +2 authors, Siew C Ng.
J Gastroenterol Hepatol, 2012 Apr 14; 27(8). PMID: 22497584
Highly Cited. Systematic Review.
Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment.
Xochitl C Morgan, Timothy L Tickle, +12 authors, Curtis Huttenhower.
Genome Biol, 2012 Sep 28; 13(9). PMID: 23013615    Free PMC article.
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Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn's disease.
Si Ming Man, Li Zhang, +3 authors, Hazel Mitchell.
Inflamm Bowel Dis, 2009 Nov 04; 16(6). PMID: 19885905
Saccharomyces boulardii does not prevent relapse of Crohn's disease.
Arnaud Bourreille, Guillaume Cadiot, +10 authors, FLORABEST Study Group.
Clin Gastroenterol Hepatol, 2013 Mar 08; 11(8). PMID: 23466709
Smokers with active Crohn's disease have a clinically relevant dysbiosis of the gastrointestinal microbiota.
Jane L Benjamin, Charlotte R H Hedin, +13 authors, Kevin Whelan.
Inflamm Bowel Dis, 2011 Nov 22; 18(6). PMID: 22102318
A national survey of the prevalence and impact of Clostridium difficile infection among hospitalized inflammatory bowel disease patients.
Geoffrey C Nguyen, Gilaad G Kaplan, Mary L Harris, Steven R Brant.
Am J Gastroenterol, 2008 Jun 03; 103(6). PMID: 18513271
Endoscopic fecal microbiota transplantation: "first-line" treatment for severe clostridium difficile infection?
Lawrence J Brandt, Thomas Julius Borody, Jordana Campbell.
J Clin Gastroenterol, 2011 Jul 01; 45(8). PMID: 21716124
Fecal microbiota transplantation: current status and future directions.
Thomas Julius Borody, Jordana Campbell.
Expert Rev Gastroenterol Hepatol, 2011 Oct 25; 5(6). PMID: 22017691
Interleukin 10-deficient colitis: new similarities to human inflammatory bowel disease.
R J Kennedy, M Hoper, +3 authors, K R Gardiner.
Br J Surg, 2000 Oct 24; 87(10). PMID: 11044159
The intestinal microbiota dysbiosis and Clostridium difficile infection: is there a relationship with inflammatory bowel disease?
Justyna Bien, Vindhya Palagani, Przemyslaw Bozko.
Therap Adv Gastroenterol, 2013 Jan 16; 6(1). PMID: 23320050    Free PMC article.
Increased prevalence of Methanosphaera stadtmanae in inflammatory bowel diseases.
Pascale Blais Lecours, David Marsolais, +4 authors, Caroline Duchaine.
PLoS One, 2014 Feb 06; 9(2). PMID: 24498365    Free PMC article.
Serum concentration of interleukin 10, anti-mannan Candida antibodies and the fungal colonization of the gastrointestinal tract in patients with ulcerative colitis.
D Ksiadzyna, J Semianow-Wejchert, +2 authors, L Paradowski.
Adv Med Sci, 2009 Sep 18; 54(2). PMID: 19758974
Enterohepatic helicobacter in ulcerative colitis: potential pathogenic entities?
John M Thomson, Richard Hansen, +8 authors, Georgina L Hold.
PLoS One, 2011 Mar 09; 6(2). PMID: 21383845    Free PMC article.
VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis.
Rodrigo Bibiloni, Richard N Fedorak, +5 authors, R Balfour Sartor.
Am J Gastroenterol, 2005 Jun 30; 100(7). PMID: 15984978
Highly Cited.
A pilot trial of Saccharomyces boulardii in ulcerative colitis.
Mario Guslandi, Patrizia Giollo, Pier Alberto Testoni.
Eur J Gastroenterol Hepatol, 2003 Jul 04; 15(6). PMID: 12840682
Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis.
T Mimura, F Rizzello, +7 authors, M A Kamm.
Gut, 2003 Dec 20; 53(1). PMID: 14684584    Free PMC article.
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Should we standardize the 1,700-year-old fecal microbiota transplantation?
Faming Zhang, Wensheng Luo, +2 authors, Guozhong Ji.
Am J Gastroenterol, 2012 Nov 20; 107(11). PMID: 23160295
Highly Cited.
Metabolomics of fecal extracts detects altered metabolic activity of gut microbiota in ulcerative colitis and irritable bowel syndrome.
Gwénaëlle Le Gall, Samah O Noor, +6 authors, Arjan Narbad.
J Proteome Res, 2011 Jul 19; 10(9). PMID: 21761941
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Probiotics for induction of remission in ulcerative colitis.
P Mallon, D McKay, S Kirk, K Gardiner.
Cochrane Database Syst Rev, 2007 Oct 19; (4). PMID: 17943867
Systematic Review.
Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis.
Erasmo Miele, Filomena Pascarella, +3 authors, Annamaria Staiano.
Am J Gastroenterol, 2009 Jan 29; 104(2). PMID: 19174792
Highly Cited.
Microbiota dynamics in patients treated with fecal microbiota transplantation for recurrent Clostridium difficile infection.
Yang Song, Shashank Garg, +5 authors, W Florian Fricke.
PLoS One, 2013 Dec 05; 8(11). PMID: 24303043    Free PMC article.
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Clinical utility of probiotics in inflammatory bowel disease.
Alisha M Cain, Kelly Dowhower Karpa.
Altern Ther Health Med, 2011 May 28; 17(1). PMID: 21614946
Review.
Fungi and inflammatory bowel diseases: Alterations of composition and diversity.
Stephan J Ott, Tanja Kühbacher, +7 authors, Stefan Schreiber.
Scand J Gastroenterol, 2008 Jun 28; 43(7). PMID: 18584522
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Characterization of adherent bacteroidales from intestinal biopsies of children and young adults with inflammatory bowel disease.
Naamah L Zitomersky, Benjamin J Atkinson, +4 authors, Athos Bousvaros.
PLoS One, 2013 Jun 19; 8(6). PMID: 23776434    Free PMC article.
Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics.
R Balfour Sartor.
Gastroenterology, 2004 May 29; 126(6). PMID: 15168372
Highly Cited. Review.
Role of Klebsiella and collagens in Crohn's disease: a new prospect in the use of low-starch diet.
Taha Rashid, Alan Ebringer, Harmale Tiwana, Mark Fielder.
Eur J Gastroenterol Hepatol, 2009 Apr 09; 21(8). PMID: 19352192
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Colonisation by Faecalibacterium prausnitzii and maintenance of clinical remission in patients with ulcerative colitis.
E Varela, C Manichanh, +5 authors, M Antolin.
Aliment Pharmacol Ther, 2013 Jun 04; 38(2). PMID: 23725320
Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients.
Harry Sokol, Bénédicte Pigneur, +17 authors, Philippe Langella.
Proc Natl Acad Sci U S A, 2008 Oct 22; 105(43). PMID: 18936492    Free PMC article.
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Generating human intestinal tissues from pluripotent stem cells to study development and disease.
Katie L Sinagoga, James M Wells.
EMBO J, 2015 Mar 21; 34(9). PMID: 25792515    Free PMC article.
Review.
Gut Microbiome: What We Do and Don't Know.
Gail A Cresci, Emmy Bawden.
Nutr Clin Pract, 2015 Oct 10; 30(6). PMID: 26449893    Free PMC article.
Review.
A comprehensive review of the nasal microbiome in chronic rhinosinusitis (CRS).
M Mahdavinia, A Keshavarzian, +2 authors, R P Schleimer.
Clin Exp Allergy, 2015 Oct 29; 46(1). PMID: 26510171    Free PMC article.
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Pathological and therapeutic interactions between bacteriophages, microbes and the host in inflammatory bowel disease.
Janka Babickova, Roman Gardlik.
World J Gastroenterol, 2015 Nov 04; 21(40). PMID: 26525290    Free PMC article.
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Influence of environmental factors in the development of inflammatory bowel diseases.
Evangelia Legaki, Maria Gazouli.
World J Gastrointest Pharmacol Ther, 2016 Feb 09; 7(1). PMID: 26855817    Free PMC article.
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Crohn's Disease: Evolution, Epigenetics, and the Emerging Role of Microbiome-Targeted Therapies.
Ersilia M DeFilippis, Randy Longman, +2 authors, Ellen J Scherl.
Curr Gastroenterol Rep, 2016 Feb 26; 18(3). PMID: 26908281
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Fecal Microbiota Transplantation: Current Applications, Effectiveness, and Future Perspectives.
Hyun Ho Choi, Young-Seok Cho.
Clin Endosc, 2016 Mar 10; 49(3). PMID: 26956193    Free PMC article.
Highly Cited. Review.
Chinese physicians' perceptions of fecal microbiota transplantation.
Rong-Rong Ren, Gang Sun, +17 authors, Ye Chen.
World J Gastroenterol, 2016 May 25; 22(19). PMID: 27217707    Free PMC article.
Progress in Our Understanding of the Gut Microbiome: Implications for the Clinician.
Sara Iqbal, Eamonn M M Quigley.
Curr Gastroenterol Rep, 2016 Jul 28; 18(9). PMID: 27448618
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The rapid spread of carbapenem-resistant Enterobacteriaceae.
Robert F Potter, Alaric W D'Souza, Gautam Dantas.
Drug Resist Updat, 2016 Dec 04; 29. PMID: 27912842    Free PMC article.
Highly Cited. Review.
Dissecting the Interplay Between Intestinal Microbiota and Host Immunity in Health and Disease: Lessons Learned from Germfree and Gnotobiotic Animal Models.
Ulrike Fiebiger, Stefan Bereswill, Markus M Heimesaat.
Eur J Microbiol Immunol (Bp), 2016 Dec 17; 6(4). PMID: 27980855    Free PMC article.
Highly Cited. Review.
Antioxidant, Immunomodulating, and Microbial-Modulating Activities of the Sustainable and Ecofriendly Spirulina.
Alberto Finamore, Maura Palmery, Sarra Bensehaila, Ilaria Peluso.
Oxid Med Cell Longev, 2017 Feb 10; 2017. PMID: 28182098    Free PMC article.
Review.
Interaction between the gut microbiome and mucosal immune system.
Na Shi, Na Li, Xinwang Duan, Haitao Niu.
Mil Med Res, 2017 May 04; 4. PMID: 28465831    Free PMC article.
Highly Cited. Review.
Fecal microbiota transplantation for refractory Crohn's disease.
Seon Ho Bak, Hyun Ho Choi, +4 authors, Young-Seok Cho.
Intest Res, 2017 May 20; 15(2). PMID: 28522956    Free PMC article.
Faecal Microbiota Transplantation for Clostridium Difficile - a local perspective.
C Diamond, T McNeilly.
Ulster Med J, 2018 Mar 15; 86(2). PMID: 29535482    Free PMC article.
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Technical Aspects of Fecal Microbial Transplantation (FMT).
N Bhutiani, J E Schucht, K R Miller, Stephen A McClave.
Curr Gastroenterol Rep, 2018 Jun 11; 20(7). PMID: 29886561
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Innate and Adaptive Cell Populations Driving Inflammation in Dry Eye Disease.
José L Reyes, Danielle T Vannan, +4 authors, Alicia Vázquez Mendoza.
Mediators Inflamm, 2018 Aug 31; 2018. PMID: 30158831    Free PMC article.
Review.
Fecal Microbiota Transplantation Ameliorates Experimentally Induced Colitis in Mice by Upregulating AhR.
Yan-Ling Wei, Yu-Qin Chen, +8 authors, Dong-Feng Chen.
Front Microbiol, 2018 Sep 11; 9. PMID: 30197631    Free PMC article.
Diarrhea as a Potential Cause and Consequence of Reduced Gut Microbial Diversity Among Undernourished Children in Peru.
Saba Rouhani, Nicholas W Griffin, +9 authors, Jeffrey I Gordon.
Clin Infect Dis, 2019 Nov 28; 71(4). PMID: 31773127    Free PMC article.
Therapeutic effects of lentinan on inflammatory bowel disease and colitis-associated cancer.
Yanrong Liu, Jianmin Zhao, +11 authors, Cheng Yang.
J Cell Mol Med, 2018 Nov 26; 23(2). PMID: 30472806    Free PMC article.
Fecal Microbial Transplantation and Its Potential Application in Cardiometabolic Syndrome.
Avner Leshem, Nir Horesh, Eran Elinav.
Front Immunol, 2019 Jul 02; 10. PMID: 31258528    Free PMC article.
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Individual and cohort-specific gut microbiota patterns associated with tissue-specific insulin sensitivity in overweight and obese males.
Gerben D A Hermes, Dorien Reijnders, +5 authors, Erwin G Zoetendal.
Sci Rep, 2020 May 07; 10(1). PMID: 32371932    Free PMC article.
Characteristics of Fecal Microbiota Transplantation Use in Inflammatory Bowel Disease Cohort.
Christina M Bauer, Xian Zhang, Millie D Long, Robert S Sandler.
Crohns Colitis 360, 2020 May 19; 2(2). PMID: 32421761    Free PMC article.
Gut microbiota modulation: a novel strategy for prevention and treatment of colorectal cancer.
Winnie Fong, Qing Li, Jun Yu.
Oncogene, 2020 Jun 10; 39(26). PMID: 32514151    Free PMC article.
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Fecal microbiota transplantation: donor relation, fresh or frozen, delivery methods, cost-effectiveness.
Daryl Ramai, Karl Zakhia, +2 authors, Madhavi Reddy.
Ann Gastroenterol, 2019 Jan 02; 32(1). PMID: 30598589    Free PMC article.
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Carbapenemases in Enterobacteriaceae: Detection and Antimicrobial Therapy.
Xiaoyan Cui, Haifang Zhang, Hong Du.
Front Microbiol, 2019 Sep 05; 10. PMID: 31481937    Free PMC article.
Review.
Association Between Impaired Vα7.2+CD161++CD8+ (MAIT) and Vα7.2+CD161-CD8+ T-Cell Populations and Gut Dysbiosis in Chronically HIV- and/or HCV-Infected Patients.
Esther Merlini, Maddalena Cerrone, +5 authors, Giulia Marchetti.
Front Microbiol, 2019 Sep 27; 10. PMID: 31555223    Free PMC article.
Fecal microbiota transplantation in refractory ulcerative colitis - a case report.
B D Moutinho, J P Baima, +4 authors, L Y Sassaki.
J Int Med Res, 2019 Jan 12; 47(2). PMID: 30632438    Free PMC article.
Hypoglycemic Mechanism of the Berberine Organic Acid Salt under the Synergistic Effect of Intestinal Flora and Oxidative Stress.
Hong-Xin Cui, Ya-Nan Hu, Jing-Wan Li, Ke Yuan.
Oxid Med Cell Longev, 2019 Jan 22; 2018. PMID: 30662584    Free PMC article.
The Intestinal Microbiota and Colorectal Cancer.
Yiwen Cheng, Zongxin Ling, Lanjuan Li.
Front Immunol, 2020 Dec 18; 11. PMID: 33329610    Free PMC article.
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Fecal microbiota transplantation for COVID-19; a potential emerging treatment strategy.
Seyed Aria Nejadghaderi, Ehsan Nazemalhosseini-Mojarad, Hamid Asadzadeh Aghdaei.
Med Hypotheses, 2021 Jan 23; 147. PMID: 33482620    Free PMC article.
Clinical efficacy of fecal microbiota transplantation for patients with small intestinal bacterial overgrowth: a randomized, placebo-controlled clinic study.
Fenghua Xu, Ning Li, +3 authors, Yanling Wei.
BMC Gastroenterol, 2021 Feb 08; 21(1). PMID: 33549047    Free PMC article.
Effect of berberine on hyperglycaemia and gut microbiota composition in type 2 diabetic Goto-Kakizaki rats.
Jin-Dong Zhao, Yan Li, +10 authors, Zhao-Hui Fang.
World J Gastroenterol, 2021 Mar 16; 27(8). PMID: 33716449    Free PMC article.
Fermented Maillard Reaction Products by Lactobacillus gasseri 4M13 Alters the Intestinal Microbiota and Improves Dysfunction in Type 2 Diabetic Mice with Colitis.
Yu-Jin Jeong, Ho-Young Park, Han-Kyul Nam, Kwang-Won Lee.
Pharmaceuticals (Basel), 2021 Apr 04; 14(4). PMID: 33800583    Free PMC article.
A Link between Chronic Kidney Disease and Gut Microbiota in Immunological and Nutritional Aspects.
Paulina Mertowska, Sebastian Mertowski, +4 authors, Wojciech Załuska.
Nutrients, 2021 Oct 24; 13(10). PMID: 34684638    Free PMC article.
Review.
In vitro Prebiotic Effect of Bread-Making Process in Inflammatory Bowel Disease Microbiome.
Aleix Lluansí, Marc Llirós, +20 authors, Xavier Aldeguer.
Front Microbiol, 2021 Oct 29; 12. PMID: 34707578    Free PMC article.