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Review

Fecal transplantation for ulcerative colitis: current evidence and future applications

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Pages 343-351 | Received 28 Aug 2019, Accepted 20 Feb 2020, Published online: 26 Feb 2020

References

  • Bamias G, Corridoni D, Pizarro TT, et al. New insights into the dichotomous role of innate cytokines in gut homeostasis and inflammation. Cytokine. 2012 Sep;59(3):451–459.
  • Cammarota G, Ianiro G, Cianci R, et al. The involvement of gut microbiota in inflammatory bowel disease pathogenesis: potential for therapy. Pharmacol Ther. 2015;149:191–212.
  • Harbord M, Eliakim R, Bettenworth D, et al. Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 2: current management. J Crohn’s Colitis. 2017 Jul 1;11(7):769–784.
  • van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013 Jan 31;368(5):407–415.
  • Cammarota G, Masucci L, Ianiro G, et al. Randomised clinical trial: faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent Clostridium difficile infection. Aliment Pharmacol Ther. 2015 May;41(9):835–843.
  • Kao D, Roach B, Silva M, et al. Effect of oral capsule- vs colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. 2017 Nov 28;318(20):1985–1993.
  • Lee CH, Steiner T, Petrof EO, et al. Frozen vs fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: a randomized clinical trial. JAMA. 2016 Jan 12;315(2):142–149.
  • Kelly CR, Khoruts A, Staley C, et al. Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection: a randomized trial. Ann Intern Med. 2016 Nov 1;165(9):609–616.
  • Kassam Z, Lee CH, Yuan Y, et al. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013 Apr;108(4):500–508.
  • Quraishi MN, Widlak M, Bhala N, et al. Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Ther. 2017 Sep;46(5):479–493.
  • Ianiro G, Maida M, Burisch J, et al. Efficacy of different faecal microbiota transplantation protocols for Clostridium difficile infection: a systematic review and meta-analysis. United European Gastroenterol J. 2018 Oct;6(8):1232–1244.
  • Debast SB, Bauer MP, Kuijper EJ, et al. European society of clinical microbiology and infectious diseases: update of the treatment guidance document for Clostridium difficile infection. Clin Microbiol Infect. 2014 Mar;20(Suppl 2):1–26.
  • McDonald LC, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clinl Infect Dis. 2018 Mar 19;66(7):987–994.
  • Angelberger S, Reinisch W, Makristathis A, et al. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am J Gastroenterol. 2013 Oct;108(10):1620–1630.
  • Kump PK, Grochenig HP, Lackner S, et al. Alteration of intestinal dysbiosis by fecal microbiota transplantation does not induce remission in patients with chronic active ulcerative colitis. Inflamm Bowel Dis. 2013 Sep;19(10):2155–2165.
  • Damman CJ, Brittnacher MJ, Westerhoff M, et al. Low level engraftment and improvement following a single colonoscopic administration of fecal microbiota to patients with ulcerative colitis. PloS One. 2015;10(8):e0133925.
  • Moayyedi P, Surette MG, Kim PT, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015 Jul;149(1):102–109 e6.
  • Costello SP, Hughes PA, Waters O, et al. Effect of fecal microbiota transplantation on 8-week remission in patients with ulcerative colitis: a randomized clinical trial. JAMA. 2019 Jan 15;321(2):156–164.
  • Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017 Mar 25;389(10075):1218–1228.
  • Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology. 2008 Feb;134(2):577–594.
  • Rutgeerts P, Goboes K, Peeters M, et al. Effect of faecal stream diversion on recurrence of Crohn’s disease in the neoterminal ileum. Lancet. 1991 Sep 28;338(8770):771–774.
  • Chassaing B, Darfeuille-Michaud A. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology. 2011 May;140(6):1720–1728.
  • Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16731–16736.
  • Looijer-van Langen MA, Dieleman LA. Prebiotics in chronic intestinal inflammation. Inflamm Bowel Dis. 2009 Mar;15(3):454–462.
  • Koboziev I, Reinoso Webb C, Furr KL, et al. Role of the enteric microbiota in intestinal homeostasis and inflammation. Free Radic Biol Med. 2013 Nov 22;68C:122–133.
  • Salim SY, Soderholm JD. Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm Bowel Dis. 2011 Jan;17(1):362–381.
  • Hermiston ML, Gordon JI. Inflammatory bowel disease and adenomas in mice expressing a dominant negative N-cadherin. Science. 1995 Nov 17;270(5239):1203–1207.
  • Peltekova VD, Wintle RF, Rubin LA, et al. Functional variants of OCTN cation transporter genes are associated with Crohn disease. Nat Genet. 2004 May;36(5):471–475.
  • Johansson ME, Phillipson M, Petersson J, et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15064–15069.
  • Velcich A, Yang W, Heyer J, et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science. 2002 Mar 1;295(5560):1726–1729.
  • Van der Sluis M, De Koning BA, De Bruijn AC, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology. 2006 Jul;131(1):117–129.
  • Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annu Rev Immunol. 2010;28:573–621.
  • Bevins CL, Salzman NH. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nature Rev Microbiol. 2011 May;9(5):356–368.
  • Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004 Jul 23;118(2):229–241.
  • Cario E, Podolsky DK. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun. 2000 Dec;68(12):7010–7017.
  • Gewirtz AT, Navas TA, Lyons S, et al. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001 Aug 15;167(4):1882–1885.
  • Abreu MT, Arnold ET, Thomas LS, et al. TLR4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem. 2002 Jun 7;277(23):20431–20437.
  • Hershberg RM. The epithelial cell cytoskeleton and intracellular trafficking. V. Polarized compartmentalization of antigen processing and Toll-like receptor signaling in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2002 Oct;283(4):G833–9.
  • Aderem A, Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature. 2000 Aug 17;406(6797):782–787.
  • Peloquin JM, Nguyen DD. The microbiota and inflammatory bowel disease: insights from animal models. Anaerobe. 2013 Dec;24:102–106.
  • Lodes MJ, Cong Y, Elson CO, et al. Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest. 2004 May;113(9):1296–1306.
  • Dubinsky MC, Kugathasan S, Mei L, et al. Increased immune reactivity predicts aggressive complicating Crohn’s disease in children. Clin Gastroenterol Hepatol. 2008 Oct;6(10):1105–1111.
  • Targan SR, Landers CJ, Yang H, et al. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn’s disease. Gastroenterology. 2005 Jun;128(7):2020–2028.
  • Vijay-Kumar M, Sanders CJ, Taylor RT, et al. Deletion of TLR5 results in spontaneous colitis in mice. J Clin Invest. 2007 Dec;117(12):3909–3921.
  • Ivison SM, Himmel ME, Hardenberg G, et al. TLR5 is not required for flagellin-mediated exacerbation of DSS colitis. Inflamm Bowel Dis. 2010 Mar;16(3):401–409.
  • Lopetuso LR, Jia R, Wang XM, et al. Epithelial-specific Toll-like Receptor (TLR)5 activation mediates barrier dysfunction in experimental ileitis. Inflamm Bowel Dis. 2017 Mar;23(3):392–403.
  • Rutgeerts P, Vermeire S, Van Assche G. Biological therapies for inflammatory bowel diseases. Gastroenterology. 2009 Apr;136(4):1182–1197.
  • Cominelli F, Nast CC, Clark BD, et al. Interleukin 1 (IL-1) gene expression, synthesis, and effect of specific IL-1 receptor blockade in rabbit immune complex colitis. J Clin Invest. 1990 Sep;86(3):972–980.
  • Andus T, Daig R, Vogl D, et al. Imbalance of the interleukin 1 system in colonic mucosa–association with intestinal inflammation and interleukin 1 receptor antagonist [corrected] genotype 2 [Research Support, Non-U.S. Gov’t]. Gut. 1997 Nov;41(5):651–657.
  • Nishiyama T, Mitsuyama K, Toyonaga A, et al. Colonic mucosal interleukin 1 receptor antagonist in inflammatory bowel disease. Digestion. 1994;55(6):368–373.
  • Ferretti M, Casini-Raggi V, Pizarro TT, et al. Neutralization of endogenous IL-1 receptor antagonist exacerbates and prolongs inflammation in rabbit immune colitis. J Clin Invest. 1994 Jul;94(1):449–453.
  • Casini-Raggi V, Kam L, Chong YJ, et al. Mucosal imbalance of IL-1 and IL-1 receptor antagonist in inflammatory bowel disease. A novel mechanism of chronic intestinal inflammation. J Immunol. 1995 Mar 1;154(5):2434–2440.
  • Pizarro TT, Michie MH, Bentz M, et al. IL-18, a novel immunoregulatory cytokine, is up-regulated in Crohn’s disease: expression and localization in intestinal mucosal cells. J Immunol. 1999 Jun 1;162(11):6829–6835.
  • Monteleone G, Trapasso F, Parrello T, et al. Bioactive IL-18 expression is up-regulated in Crohn’s disease. J Immunol. 1999 Jul 1;163(1):143–147.
  • McNamee EN, Masterson JC, Jedlicka P, et al. Interleukin 37 expression protects mice from colitis. Proc Natl Acad Sci U S A. 2011 Oct 4;108(40):16711–16716.
  • Pastorelli L, Garg RR, Hoang SB, et al. Epithelial-derived IL-33 and its receptor ST2 are dysregulated in ulcerative colitis and in experimental Th1/Th2 driven enteritis. Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):8017–8022.
  • Beltran CJ, Nunez LE, Diaz-Jimenez D, et al. Characterization of the novel ST2/IL-33 system in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2010 Jul;16(7):1097–1107.
  • Kobori A, Yagi Y, Imaeda H, et al. Interleukin-33 expression is specifically enhanced in inflamed mucosa of ulcerative colitis. J Gastroenterol. 2010 Oct;45(10):999–1007.
  • Seidelin JB, Bjerrum JT, Coskun M, et al. IL-33 is upregulated in colonocytes of ulcerative colitis. Immunol Lett. 2010 Jan 18;128(1):80–85.
  • Sponheim J, Pollheimer J, Olsen T, et al. Inflammatory bowel disease-associated interleukin-33 is preferentially expressed in ulceration-associated myofibroblasts. Am J Pathol. 2010 Dec;177(6):2804–2815.
  • Lopetuso LR, De Salvo C, Pastorelli L, et al. IL-33 promotes recovery from acute colitis by inducing miR-320 to stimulate epithelial restitution and repair. Proc Natl Acad Sci U S A. 2018 Oct 2;115(40):E9362–E9370.
  • Bennet JD, Brinkman M. Treatment of ulcerative colitis by implantation of normal colonic flora. Lancet. 1989 Jan 21;1(8630):164.
  • Anderson JL, Edney RJ, Whelan K. Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther. 2012 Sep;36(6):503–516.
  • Ianiro G, Bibbo S, Scaldaferri F, et al. Fecal microbiota transplantation in inflammatory bowel disease: beyond the excitement. Medicine (Baltimore). 2014 Oct;93(19):e97.
  • Rossen NG, Fuentes S, van der Spek MJ, et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology. 2015 Jul;149(1):110–118 e4.
  • Costello SP, Soo W, Bryant RV, et al. Systematic review with meta-analysis: faecal microbiota transplantation for the induction of remission for active ulcerative colitis. Aliment Pharmacol Ther. 2017 Aug;46(3):213–224.
  • Narula N, Kassam Z, Yuan Y, et al. Systematic review and meta-analysis: fecal microbiota transplantation for treatment of active ulcerative colitis. Inflamm Bowel Dis. 2017 Oct;23(10):1702–1709.
  • Imdad A, Nicholson MR, Tanner-Smith EE, et al. Fecal transplantation for treatment of inflammatory bowel disease. Cochrane Database Syst Rev. 2018 Nov 13;11:CD012774.
  • Lam WC, Zhao C, Ma WJ, et al. The clinical and steroid-free remission of fecal microbiota transplantation to patients with ulcerative colitis: a meta-analysis. Gastroenterol Res Pract. 2019;2019:1287493.
  • Cold F, Browne PD, Gunther S, et al. Multidonor FMT capsules improve symptoms and decrease fecal calprotectin in ulcerative colitis patients while treated - an open-label pilot study. Scand J Gastroenterol. 2019 Mar;54(3):289–296.
  • Ianiro G, Valerio L, Masucci L, et al. Predictors of failure after single faecal microbiota transplantation in patients with recurrent Clostridium difficile infection: results from a 3-year, single-centre cohort study. Clin Microbiol Infect. 2017 May;23(5):337e1–337e3.
  • Ianiro G, Masucci L, Quaranta G, et al. Randomised clinical trial: faecal microbiota transplantation by colonoscopy plus vancomycin for the treatment of severe refractory Clostridium difficile infection-single versus multiple infusions. Aliment Pharmacol Ther. 2018 Jul;48(2):152–159.
  • Richard ML, Sokol H. The gut mycobiota: insights into analysis, environmental interactions and role in gastrointestinal diseases. Nat Clin Pract Gastroenterol Hepatol. 2019 Jun;16(6):331–345.
  • Lopetuso LR, Ianiro G, Scaldaferri F, et al. Gut virome and inflammatory bowel disease. Inflamm Bowel Dis. 2016 Jul;22(7):1708–1712.
  • Ko CW, Singh S, Feuerstein JD, et al. American gastroenterological association institute guideline on the management of mild-to-moderate ulcerative colitis. Gastroenterology. 2018 Dec 18;156(3):748–764.
  • Schirmer M, Franzosa EA, Lloyd-Price J, et al. Dynamics of metatranscription in the inflammatory bowel disease gut microbiome. Nat Microbiol. 2018 Mar 3;3(3):337–346.
  • Mullish BH, Quraishi MN, Segal JP, et al. The use of faecal microbiota transplant as treatment for recurrent or refractory Clostridium difficile infection and other potential indications: joint British Society of Gastroenterology (BSG) and Healthcare Infection Society (HIS) guidelines. Gut. 2018 Nov;67(11):1920–1941.
  • Weingarden AR, Vaughn BP. Intestinal microbiota, fecal microbiota transplantation, and inflammatory bowel disease. Gut Microbes. 2017 May 4;8(3):238–252.

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