Intest Res.  2024 Jan;22(1):44-64. 10.5217/ir.2023.00085.

The practice of fecal microbiota transplantation in inflammatory bowel disease

Affiliations
  • 1Department of Gastroenterology and Human Nutrition, All India Institute of Medical Sciences, New Delhi, India

Abstract

Current evidence posits a central role for gut microbiota and the metabolome in the pathogenesis and progression of inflammatory bowel disease (IBD). Fecal microbiota transplantation (FMT) has been established as a means to manipulate this microbiome safely and sustainably. Several aspects of the technical improvement including pretreatment with antibiotics, use of frozen stool samples as well as short donor-to-recipient time are proposed to improve its response rates. Its efficacy in ulcerative colitis has been proven in clinical trials while data is emerging for Crohn’s disease. This review describes briefly the biology behind FMT, the available evidence for its use in IBD, and the host, recipient and procedural factors which determine the clinical outcomes.

Keyword

Fecal microbiota transplantation; Microbiota; Inflammatory bowel diseases; Microbiome manipulation therapy

Figure

  • Fig. 1. Overview of fecal microbiota transplantation (FMT) in inflammatory bowel disease (IBD). Fecal matter from a healthy donor is collected, processed, and administered into a patient with IBD through one of several routes, typically via colonoscopy. FMT, if engraftment is successful, modulates existing gut microbiota by promoting growth of eubionts and suppressing pathobionts, with downstream effects of promoting anti-inflammatory metabolites (such as short-chain fatty acids or secondary bile acids) and suppressing inflammatory metabolites (triacylglycerol and tetrapyrrole). The interaction with immune system is complex but generally suppresses aberrant inflammation.

  • Fig. 2. Factors that determine success of fecal microbiota transplantation (FMT) in inflammatory bowel disease (IBD). The figure shows several factors including selection of donor, FMT session frequency, choice of frozen versus fresh FMT, pretreatment with antibiotics, and different routes of administration, all of which have been found to affect success of FMT. These serve as guides to allow improvement in FMT technique and creation of an optimum protocol.


Reference

1. Franzosa EA, Sirota-Madi A, Avila-Pacheco J, et al. Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat Microbiol. 2019; 4:293–305.
Article
2. Machiels K, Joossens M, Sabino J, et al. A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut. 2014; 63:1275–1283.
Article
3. Imhann F, Vich Vila A, Bonder MJ, et al. Interplay of host genetics and gut microbiota underlying the onset and clinical presentation of inflammatory bowel disease. Gut. 2018; 67:108–119.
Article
4. Verma R, Verma AK, Ahuja V, Paul J. Real-time analysis of mucosal flora in patients with inflammatory bowel disease in India. J Clin Microbiol. 2010; 48:4279–4282.
Article
5. Ahuja V. Inventory of a reservoir: friends & foes. Indian J Med Res. 2015; 142:4–6.
6. Nguyen LH, Örtqvist AK, Cao Y, et al. Antibiotic use and the development of inflammatory bowel disease: a national casecontrol study in Sweden. Lancet Gastroenterol Hepatol. 2020; 5:986–995.
Article
7. Kedia S, Rampal R, Paul J, Ahuja V. Gut microbiome diversity in acute infective and chronic inflammatory gastrointestinal diseases in North India. J Gastroenterol. 2016; 51:660–671.
Article
8. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol. 2011; 106:563–573.
Article
9. Naser SA, Sagramsingh SR, Naser AS, Thanigachalam S. Mycobacterium avium subspecies paratuberculosis causes Crohn’s disease in some inflammatory bowel disease patients. World J Gastroenterol. 2014; 20:7403–7415.
Article
10. Selby W, Pavli P, Crotty B, et al. Two-year combination antibiotic therapy with clarithromycin, rifabutin, and clofazimine for Crohn’s disease. Gastroenterology. 2007; 132:2313–2319.
Article
11. Khan IA, Pilli S, A S, et al. Prevalence and association of Mycobacterium avium subspecies paratuberculosis with disease course in patients with ulcero-constrictive ileocolonic disease. PLoS One. 2016; 11:e0152063.
Article
12. Khan IA, Nayak B, Markandey M, et al. Differential prevalence of pathobionts and host gene polymorphisms in chronic inflammatory intestinal diseases: Crohn’s disease and intestinal tuberculosis. PLoS One. 2021; 16:e0256098.
Article
13. 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; 105:16731–16736.
Article
14. Magnusson MK, Strid H, Isaksson S, Simrén M, Öhman L. The mucosal antibacterial response profile and fecal microbiota composition are linked to the disease course in patients with newly diagnosed ulcerative colitis. Inflamm Bowel Dis. 2017; 23:956–966.
Article
15. Machiels K, Sabino J, Vandermosten L, et al. Specific members of the predominant gut microbiota predict pouchitis following colectomy and IPAA in UC. Gut. 2017; 66:79–88.
Article
16. Zhou Y, Xu ZZ, He Y, et al. Gut microbiota offers universal biomarkers across ethnicity in inflammatory bowel disease diagnosis and infliximab response prediction. mSystems. 2018; 3:e00188. –17.
Article
17. Magnusson MK, Strid H, Sapnara M, et al. Anti-TNF therapy response in patients with ulcerative colitis is associated with colonic antimicrobial peptide expression and microbiota composition. J Crohns Colitis. 2016; 10:943–952.
Article
18. Ananthakrishnan AN, Luo C, Yajnik V, et al. Gut microbiome function predicts response to anti-integrin biologic therapy in inflammatory bowel diseases. Cell Host Microbe. 2017; 21:603–610.
Article
19. Zhou Y, He Y, Liu L, et al. Alterations in gut microbial communities across anatomical locations in inflammatory bowel diseases. Front Nutr. 2021; 8:615064.
Article
20. Kim S, Kim JH, Park BO, Kwak YS. Perspectives on the therapeutic potential of short-chain fatty acid receptors. BMB Rep. 2014; 47:173–178.
Article
21. Dorrestein PC, Mazmanian SK, Knight R. Finding the missing links among metabolites, microbes, and the host. Immunity. 2014; 40:824–832.
Article
22. Smith PM, Howitt MR, Panikov N, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013; 341:569–573.
Article
23. Lamas B, Richard ML, Leducq V, et al. CARD9 impacts colitis by altering gut microbiota metabolism of tryptophan into aryl hydrocarbon receptor ligands. Nat Med. 2016; 22:598–605.
Article
24. Vich Vila A, Hu S, Andreu-Sánchez S, et al. Faecal metabolome and its determinants in inflammatory bowel disease. Gut. 2023; 72:1472–1485.
Article
25. Schoch CL, Seifert KA, Huhndorf S, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A. 2012; 109:6241–6246.
26. Hoarau G, Mukherjee PK, Gower-Rousseau C, et al. Bacteriome and mycobiome interactions underscore microbial dysbiosis in familial Crohn’s disease. mBio. 2016; 7:e01250-16. –16.
Article
27. Hager CL, Isham N, Schrom KP, et al. Effects of a novel probiotic combination on pathogenic bacterial-fungal polymicrobial biofilms. mBio. 2019; 10:e00338-19.
Article
28. Imai T, Inoue R, Kawada Y, et al. Characterization of fungal dysbiosis in Japanese patients with inflammatory bowel disease. J Gastroenterol. 2019; 54:149–159.
Article
29. Jain U, Ver Heul AM, Xiong S, et al. Debaryomyces is enriched in Crohn’s disease intestinal tissue and impairs healing in mice. Science. 2021; 371:1154–1159.
Article
30. Limon JJ, Tang J, Li D, et al. Malassezia is associated with Crohn’s disease and exacerbates colitis in mouse models. Cell Host Microbe. 2019; 25:377–388.
Article
31. Stockdale SR, Shkoporov AN, Khokhlova EV, et al. Interpersonal variability of the human gut virome confounds disease signal detection in IBD. Commun Biol. 2023; 6:221.
Article
32. Norman JM, Handley SA, Baldridge MT, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell. 2015; 160:447–460.
Article
33. Yan A, Butcher J, Schramm L, Mack DR, Stintzi A. Multiomic spatial analysis reveals a distinct mucosa-associated virome. Gut Microbes. 2023; 15:2177488.
Article
34. Markandey M, Bajaj A, Ilott NE, et al. Gut microbiota: sculptors of the intestinal stem cell niche in health and inflammatory bowel disease. Gut Microbes. 2021; 13:1990827.
Article
35. Altomare A, Putignani L, Del Chierico F, et al. Gut mucosalassociated microbiota better discloses inflammatory bowel disease differential patterns than faecal microbiota. Dig Liver Dis. 2019; 51:648–656.
Article
36. Kabeerdoss J, Jayakanthan P, Pugazhendhi S, Ramakrishna BS. Alterations of mucosal microbiota in the colon of patients with inflammatory bowel disease revealed by real time polymerase chain reaction amplification of 16S ribosomal ribonucleic acid. Indian J Med Res. 2015; 142:23–32.
Article
37. Lennon G, Balfe Á, Bambury N, et al. Correlations between colonic crypt mucin chemotype, inflammatory grade and Desulfovibrio species in ulcerative colitis. Colorectal Dis. 2014; 16:–O161-O169.
Article
38. Sokol H, Vasquez N, Hoyeau-Idrissi N, et al. Crypt abscess-associated microbiota in inflammatory bowel disease and acute self-limited colitis. World J Gastroenterol. 2010; 16:583587.
Article
39. Markandey M, Bajaj A, Verma M, et al. Fecal microbiota transplantation refurbishes the crypt-associated microbiota in ulcerative colitis. iScience. 2023; 26:106738.
Article
40. Abdelbary MM, Hatting M, Bott A, et al. The oral-gut axis: salivary and fecal microbiome dysbiosis in patients with inflammatory bowel disease. Front Cell Infect Microbiol. 2022; 12:1010853.
Article
41. Atarashi K, Suda W, Luo C, et al. Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation. Science. 2017; 358:359–365.
Article
42. Shen ZH, Zhu CX, Quan YS, et al. Relationship between intestinal microbiota and ulcerative colitis: mechanisms and clinical application of probiotics and fecal microbiota transplantation. World J Gastroenterol. 2018; 24:5–14.
Article
43. Paramsothy S, Nielsen S, Kamm MA, et al. Specific bacteria and metabolites associated with response to fecal microbiota transplantation in patients with ulcerative colitis. Gastroenterology. 2019; 156:1440–1454.
Article
44. Mocanu V, Rajaruban S, Dang J, Kung JY, Deehan EC, Madsen KL. Repeated fecal microbial transplantations and antibiotic pre-treatment are linked to improved clinical response and remission in inflammatory bowel disease: a systematic review and pooled proportion meta-analysis. J Clin Med. 2021; 10:959.
Article
45. Lima SF, Gogokhia L, Viladomiu M, et al. Transferable immunoglobulin A-coated Odoribacter splanchnicus in responders to fecal microbiota transplantation for ulcerative colitis limits colonic inflammation. Gastroenterology. 2022; 162:166178.
Article
46. Hoelz H, Heetmeyer J, Tsakmaklis A, et al. Is autologous fecal microbiota transfer after exclusive enteral nutrition in pediatric Crohn’s disease patients rational and feasible? Data from a feasibility test. Nutrients. 2023; 15:1742.
47. Ponce-Alonso M, Garcia-Fernandez S, Aguilera L, et al. P782 A new compatibility test for donor selection for faecal microbiota transplantation in ulcerative colitis. J Crohns Colitis. 2017; 11(suppl_1):S480–S481.
Article
48. U.S. Food and Drug Administration. Information pertaining to additional safety protections regarding use of fecal microbiota for transplantation: testing of stool donors for enteropathogenic Escherichia coli and Shigatoxin-producing Escherichia coli [Internet]. c2020 [cited 2023 Jul 9]. https://www.fda.gov/vaccines-blood-biologics/safety-availability-biologics/information-pertaining-additional-safety-protectionsregarding-use-fecal-microbiota-transplantation-0.
49. Ianiro G, Mullish BH, Kelly CR, et al. Screening of faecal microbiota transplant donors during the COVID-19 outbreak: suggestions for urgent updates from an international expert panel. Lancet Gastroenterol Hepatol. 2020; 5:430–432.
Article
50. Bénard MV, de Bruijn CM, Fenneman AC, et al. Challenges and costs of donor screening for fecal microbiota transplantations. PLoS One. 2022; 17:e0276323.
Article
51. Cammarota G, Ianiro G, Tilg H, et al. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017; 66:569–580.
Article
52. Lopetuso LR, Deleu S, Godny L, et al. The first international Rome consensus conference on gut microbiota and faecal microbiota transplantation in inflammatory bowel disease. Gut. 2023; 72:1642–1650.
Article
53. Bilinski J, Dziurzynski M, Grzesiowski P, et al. Fresh versus frozen stool for fecal microbiota transplantation-assessment by multimethod approach combining culturing, flow cytometry, and next-generation sequencing. Front Microbiol. 2022; 13:872735.
Article
54. Gangwani MK, Aziz M, Aziz A, et al. Fresh versus frozen versus lyophilized fecal microbiota transplant for recurrent Clostridium difficile infection: a systematic review and network meta-analysis. J Clin Gastroenterol. 2023; 57:239–245.
Article
55. Zhao HL, Chen SZ, Xu HM, et al. Efficacy and safety of fecal microbiota transplantation for treating patients with ulcerative colitis: a systematic review and meta-analysis. J Dig Dis. 2020; 21:534–548.
Article
56. Zhang T, Lu G, Zhao Z, et al. Washed microbiota transplantation vs. manual fecal microbiota transplantation: clinical findings, animal studies and in vitro screening. Protein Cell. 2020; 11:251–266.
Article
57. Ding X, Li Q, Li P, et al. Long-term safety and efficacy of fecal microbiota transplant in active ulcerative colitis. Drug Saf. 2019; 42:869–880.
Article
58. Ott SJ, Waetzig GH, Rehman A, et al. Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology. 2017; 152:799–811.
Article
59. Stallmach A, Grunert P, Stallhofer J, et al. Transfer of FRozen Encapsulated multi-donor Stool filtrate for active ulcerative Colitis (FRESCO): study protocol for a prospective, multicenter, double-blind, randomized, controlled trial. Trials. 2022; 23:173.
Article
60. 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; 321:156–164.
Article
61. Shimizu H, Arai K, Asahara T, et al. Stool preparation under anaerobic conditions contributes to retention of obligate anaerobes: potential improvement for fecal microbiota transplantation. BMC Microbiol. 2021; 21:275.
Article
62. Chu ND, Smith MB, Perrotta AR, Kassam Z, Alm EJ. Profiling living bacteria informs preparation of fecal microbiota transplantations. PLoS One. 2017; 12:e0170922.
Article
63. Papanicolas LE, Choo JM, Wang Y, et al. Bacterial viability in faecal transplants: which bacteria survive? EBioMedicine. 2019; 41:509–516.
Article
64. Singh A, Mahajan R, Kahlon BK, et al. Early fecal microbiome transfer after donor defecation determines response in patients with moderate to severe ulcerative colitis. Indian J Gastroenterol. 2022; 41:389–396.
Article
65. Zhang YJ, Bousvaros A, Docktor M, et al. Higher alpha diversity and Lactobacillus blooms are associated with better engraftment after fecal microbiota transplant in inflammatory bowel disease. c2023; [cited 2023 Jul 19]. https://doi.org/10.1101/2023.01.30.23285033.
Article
66. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology. 2004; 126:1620–1633.
Article
67. Ji SK, Yan H, Jiang T, et al. Preparing the gut with antibiotics enhances gut microbiota reprogramming efficiency by promoting xenomicrobiota colonization. Front Microbiol. 2017; 8:1208.
Article
68. Ishikawa D, Sasaki T, Osada T, et al. Changes in intestinal microbiota following combination therapy with fecal microbial transplantation and antibiotics for ulcerative colitis. Inflamm Bowel Dis. 2017; 23:116–125.
Article
69. Kump P, Wurm P, Gröchenig HP, et al. The taxonomic composition of the donor intestinal microbiota is a major factor influencing the efficacy of faecal microbiota transplantation in therapy refractory ulcerative colitis. Aliment Pharmacol Ther. 2018; 47:67–77.
Article
70. 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; 67:19201941.
Article
71. Gweon TG, Lee YJ, Kim KO, et al. Clinical practice guidelines for fecal microbiota transplantation in Korea. J Neurogastroenterol Motil. 2022; 28:28–42.
Article
72. Jalanka J, Salonen A, Salojärvi J, et al. Effects of bowel cleansing on the intestinal microbiota. Gut. 2015; 64:1562–1568.
Article
73. O’Brien CL, Allison GE, Grimpen F, Pavli P. Impact of colonoscopy bowel preparation on intestinal microbiota. PLoS One. 2013; 8:e62815.
Article
74. Harrell L, Wang Y, Antonopoulos D, et al. Standard colonic lavage alters the natural state of mucosal-associated microbiota in the human colon. PLoS One. 2012; 7:e32545.
Article
75. Tariq R, Hayat M, Pardi D, Khanna S. Predictors of failure after fecal microbiota transplantation for recurrent Clostridioides difficile infection: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2021; 40:1383–1392.
Article
76. Youngster I, Sauk J, Pindar C, et al. Fecal microbiota transplant for relapsing Clostridium difficile infection using a frozen inoculum from unrelated donors: a randomized, openlabel, controlled pilot study. Clin Infect Dis. 2014; 58:1515–1522.
Article
77. Yang Z, Bu C, Yuan W, et al. Fecal microbiota transplant via endoscopic delivering through small intestine and colon: no difference for Crohn’s disease. Dig Dis Sci. 2020; 65:150–157.
Article
78. Fang H, Fu L, Wang J. Protocol for fecal microbiota transplantation in inflammatory bowel disease: a systematic review and meta-analysis. Biomed Res Int. 2018; 2018:8941340.
Article
79. 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; 149:110118.
Article
80. Haifer C, Paramsothy S, Kaakoush NO, et al. Lyophilised oral faecal microbiota transplantation for ulcerative colitis (LOTUS): a randomised, double-blind, placebo-controlled trial. Lancet Gastroenterol Hepatol. 2022; 7:141–151.
Article
81. 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; 318:1985–1993.
Article
82. Vaughn BP, Fischer M, Kelly CR, et al. Effectiveness and safety of colonic and capsule fecal microbiota transplantation for recurrent Clostridioides difficile infection. Clin Gastroenterol Hepatol. 2023; 21:1330–1337.
Article
83. Wei ZJ, Dong HB, Ren YT, Jiang B. Efficacy and safety of fecal microbiota transplantation for the induction of remission in active ulcerative colitis: a systematic review and meta-analysis of randomized controlled trials. Ann Transl Med. 2022; 10:802.
Article
84. El-Salhy M, Hatlebakk JG, Gilja OH, Bråthen Kristoffersen A, Hausken T. Efficacy of faecal microbiota transplantation for patients with irritable bowel syndrome in a randomised, double-blind, placebo-controlled study. Gut. 2020; 69:859–867.
Article
85. Ren R, Gao X, Shi Y, et al. Long-term efficacy of low-intensity single donor fecal microbiota transplantation in ulcerative colitis and outcome-specific gut bacteria. Front Microbiol. 2021; 12:742255.
Article
86. Baunwall SM, Lee MM, Eriksen MK, et al. Faecal microbiota transplantation for recurrent Clostridioides difficile infection: an updated systematic review and meta-analysis. EClinicalMedicine. 2020; 29-30:100642.
Article
87. El-Salhy M, Hausken T, Hatlebakk JG. Increasing the dose and/or repeating faecal microbiota transplantation (FMT) increases the response in patients with irritable bowel syndrome (IBS). Nutrients. 2019; 11:1415.
Article
88. Borody TJ, Warren EF, Leis S, Surace R, Ashman O. Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol. 2003; 37:42–47.
Article
89. Chen M, Liu XL, Zhang YJ, Nie YZ, Wu KC, Shi YQ. Efficacy and safety of fecal microbiota transplantation by washed preparation in patients with moderate to severely active ulcerative colitis. J Dig Dis. 2020; 21:621–628.
Article
90. 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; 149:102–109.
Article
91. Kedia S, Virmani S, K Vuyyuru S, et al. Faecal microbiota transplantation with anti-inflammatory diet (FMT-AID) followed by anti-inflammatory diet alone is effective in inducing and maintaining remission over 1 year in mild to moderate ulcerative colitis: a randomised controlled trial. Gut. 2022; 71:24012413.
Article
92. Sood A, Singh A, Mahajan R, et al. Clinical predictors of response to faecal microbiota transplantation in patients with active ulcerative colitis. J Crohns Colitis. 2020; 15:238–243.
Article
93. Kazerouni A, Wein LM. Exploring the efficacy of pooled stools in fecal microbiota transplantation for microbiota-associated chronic diseases. PLoS One. 2017; 12:e0163956.
Article
94. Levast B, Fontaine M, Nancey S, Dechelotte P, Doré J, Lehert P. Single-donor and pooling strategies for fecal microbiota transfer product preparation in ulcerative colitis: a systematic review and meta-analysis. Clin Transl Gastroenterol. 2023; 14:e00568.
Article
95. Li H, Li Y, Qian J. What is the “optimal formula” for donor selection and feces processing for fecal microbiota transplantation in ulcerative colitis? Chin Med J (Engl). 2023; 136:14101412.
Article
96. Wilson BC, Vatanen T, Cutfield WS, O’Sullivan JM. The superdonor phenomenon in fecal microbiota transplantation. Front Cell Infect Microbiol. 2019; 9:2.
Article
97. Okahara K, Ishikawa D, Nomura K, et al. Matching between donors and ulcerative colitis patients is important for longterm maintenance after fecal microbiota transplantation. J Clin Med. 2020; 9:1650.
Article
98. Barnes D, Ng K, Smits S, Sonnenburg J, Kassam Z, Park KT. Competitively selected donor fecal microbiota transplantation: butyrate concentration and diversity as measures of donor quality. J Pediatr Gastroenterol Nutr. 2018; 67:185–187.
99. Haifer C, Luu LD, Paramsothy S, Borody TJ, Leong RW, Kaakoush NO. Microbial determinants of effective donors in faecal microbiota transplantation for UC. Gut. 2023; 72:92–100.
Article
100. He R, Li P, Wang J, Cui B, Zhang F, Zhao F. The interplay of gut microbiota between donors and recipients determines the efficacy of fecal microbiota transplantation. Gut Microbes. 2022; 14:2100197.
Article
101. Olesen SW, Gerardin Y. Re-evaluating the evidence for faecal microbiota transplantation ‘super-donors’ in inflammatory bowel disease. J Crohns Colitis. 2021; 15:453–461.
Article
102. Rees NP, Shaheen W, Quince C, et al. Systematic review of donor and recipient predictive biomarkers of response to faecal microbiota transplantation in patients with ulcerative colitis. EBioMedicine. 2022; 81:104088.
Article
103. Zhang B, Yang L, Ning H, et al. A matching strategy to guide donor selection for ulcerative colitis in fecal microbiota transplantation: meta-analysis and analytic hierarchy process. Microbiol Spectr. 2023; 11:e0215921.
Article
104. Bajaj A, Markandey M, Singh M, et al. P702 Faecal microbiota transplantation sculpts the faecal and mucosal microbial and metabolomic profiles in patients with ulcerative colitis. J Crohns Colitis. 2022; 16(Suppl_1):i598–i601.
Article
105. Tkach S, Dorofeyev A, Kuzenko I, et al. Efficacy and safety of fecal microbiota transplantation via colonoscopy as add-on therapy in patients with mild-to-moderate ulcerative colitis: a randomized clinical trial. Front Med (Lausanne). 2023; 9:1049849.
Article
106. Sarbagili Shabat C, Scaldaferri F, Zittan E, et al. Use of faecal transplantation with a novel diet for mild to moderate active ulcerative colitis: the CRAFT UC randomised controlled trial. J Crohns Colitis. 2022; 16:369–378.
Article
107. Pai N, Popov J, Hill L, et al. Results of the first pilot randomized controlled trial of fecal microbiota transplant in pediatric ulcerative colitis: lessons, limitations, and future prospects. Gastroenterology. 2021; 161:388–393.
Article
108. Crothers JW, Chu ND, Nguyen LT, et al. Daily, oral FMT for long-term maintenance therapy in ulcerative colitis: results of a single-center, prospective, randomized pilot study. BMC Gastroenterol. 2021; 21:281.
Article
109. Fang H, Fu L, Li X, et al. Long-term efficacy and safety of monotherapy with a single fresh fecal microbiota transplant for recurrent active ulcerative colitis: a prospective randomized pilot study. Microb Cell Fact. 2021; 20:18.
Article
110. Březina J, Bajer L, Wohl P, et al. Fecal microbial transplantation versus mesalamine enema for treatment of active leftsided ulcerative colitis: results of a randomized controlled trial. J Clin Med. 2021; 10:2753.
Article
111. Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017; 389:1218–1228.
Article
112. Sood A, Mahajan R, Singh A, et al. Role of faecal microbiota transplantation for maintenance of remission in patients with ulcerative colitis: a pilot study. J Crohns Colitis. 2019; 13:1311–1317.
Article
113. Lahtinen P, Jalanka J, Mattila E, et al. Fecal microbiota transplantation for the maintenance of remission in patients with ulcerative colitis: a randomized controlled trial. World J Gastroenterol. 2023; 29:2666–2678.
Article
114. El Hage Chehade N, Ghoneim S, Shah S, et al. Efficacy of fecal microbiota transplantation in the treatment of active ulcerative colitis: a systematic review and meta-analysis of double-blind randomized controlled trials. Inflamm Bowel Dis. 2023; 29:808–817.
Article
115. Imdad A, Pandit NG, Zaman M, et al. Fecal transplantation for treatment of inflammatory bowel disease. Cochrane Database Syst Rev. 2023; 4–CD012774.
Article
116. Vuyyuru SK, Kedia S, Kalaivani M, et al. Efficacy and safety of fecal transplantation versus targeted therapies in ulcerative colitis: network meta-analysis. Future Microbiol. 2021; 16:12151227.
Article
117. Haifer C, Saikal A, Paramsothy R, et al. Response to faecal microbiota transplantation in ulcerative colitis is not sustained long term following induction therapy. Gut. 2021; 70:22102211.
Article
118. Cui B, Li P, Xu L, et al. Step-up fecal microbiota transplantation strategy: a pilot study for steroid-dependent ulcerative colitis. J Transl Med. 2015; 13:298.
Article
119. Sood A, Mahajan R, Juyal G, et al. Efficacy of fecal microbiota therapy in steroid dependent ulcerative colitis: a real world intention-to-treat analysis. Intest Res. 2019; 17:78–86.
Article
120. Seth AK, Jain P. Fecal microbiota transplantation for induction of remission, maintenance and rescue in patients with corticosteroid-dependent ulcerative colitis: a long-term follow-up real-world cohort study. Intest Res. 2022; 20:251–259.
Article
121. Jadhav A, Bajaj A, Xiao Y, Markandey M, Ahuja V, Kashyap PC. Role of diet-microbiome interaction in gastrointestinal disorders and strategies to modulate them with microbiome-targeted therapies. Annu Rev Nutr. 2023; 43:355–383.
Article
122. Sigall-Boneh R, Levine A, Lomer M, et al. Research gaps in diet and nutrition in inflammatory bowel disease. a topical review by D-ECCO Working Group [Dietitians of ECCO]. J Crohns Colitis. 2017; 11:1407–1419.
Article
123. Costello SP, Day A, Yao CK, Bryant RV. Faecal microbiota transplantation (FMT) with dietary therapy for acute severe ulcerative colitis. BMJ Case Rep. 2020; 13:e233135.
Article
124. Kumagai H, Yokoyama K, Imagawa T, et al. Failure of fecal microbiota transplantation in a three-year-old child with severe refractory ulcerative colitis. Pediatr Gastroenterol Hepatol Nutr. 2016; 19:214–220.
Article
125. Zhou S, Cui Y, Zhang Y, Zhao T, Cong J. Fecal microbiota transplantation for induction of remission in Crohn’s disease: a systematic review and meta-analysis. Int J Colorectal Dis. 2023; 38:62.
Article
126. ClinicalTrials.gov [Internet]. U.S. National Library of Medicine, 2022 [cited 2023 Nov 10]. https://classic.clinicaltrials.gov/ct2/show/NCT03078803.
127. Sokol H, Landman C, Seksik P, et al. Fecal microbiota transplantation to maintain remission in Crohn’s disease: a pilot randomized controlled study. Microbiome. 2020; 8:12.
Article
128. Cleynen I, Boucher G, Jostins L, et al. Inherited determinants of Crohn’s disease and ulcerative colitis phenotypes: a genetic association study. Lancet. 2016; 387:156–167.
129. Arora U, Kedia S, Garg P, et al. Colonic Crohn’s disease is associated with less aggressive disease course than ileal or ileocolonic disease. Dig Dis Sci. 2018; 63:1592–1599.
Article
130. Haac BE, Palmateer NC, Seaton ME, VanYPeren R, Fraser CM, Bafford AC. A distinct gut microbiota exists within Crohn’s disease-related perianal fistulae. J Surg Res. 2019; 242:118–128.
Article
131. Allegretti JR, Kassam Z, Carrellas M, et al. Fecal microbiota transplantation in patients with primary sclerosing cholangitis: a pilot clinical trial. Am J Gastroenterol. 2019; 114:10711079.
Article
132. Zella GC, Hait EJ, Glavan T, et al. Distinct microbiome in pouchitis compared to healthy pouches in ulcerative colitis and familial adenomatous polyposis. Inflamm Bowel Dis. 2011; 17:1092–1100.
Article
133. Cold F, Kousgaard SJ, Halkjaer SI, et al. Fecal microbiota transplantation in the treatment of chronic pouchitis: a systematic review. Microorganisms. 2020; 8:1433.
Article
134. Xiang L, Ding X, Li Q, et al. Efficacy of faecal microbiota transplantation in Crohn’s disease: a new target treatment? Microb Biotechnol. 2020; 13:760–769.
Article
135. Chen T, Zhou Q, Zhang D, et al. Effect of faecal microbiota transplantation for treatment of Clostridium difficile infection in patients with inflammatory bowel disease: a systematic review and meta-analysis of cohort studies. J Crohns Colitis. 2018; 12:710–717.
Article
136. Hirten RP, Grinspan A, Fu SC, et al. Microbial engraftment and efficacy of fecal microbiota transplant for Clostridium difficile in patients with and without inflammatory bowel disease. Inflamm Bowel Dis. 2019; 25:969–979.
Article
137. Kunde S, Pham A, Bonczyk S, et al. Safety, tolerability, and clinical response after fecal transplantation in children and young adults with ulcerative colitis. J Pediatr Gastroenterol Nutr. 2013; 56:597–601.
Article
138. Suskind DL, Brittnacher MJ, Wahbeh G, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis. 2015; 21:556563.
Article
139. Marcella C, Cui B, Kelly CR, Ianiro G, Cammarota G, Zhang F. Systematic review: the global incidence of faecal microbiota transplantation-related adverse events from 2000 to 2020. Aliment Pharmacol Ther. 2021; 53:33–42.
Article
140. DeFilipp Z, Bloom PP, Torres Soto M, et al. Drug-resistant E. coli bacteremia transmitted by fecal microbiota transplant. N Engl J Med. 2019; 381:2043–2050.
Article
141. Quera R, Espinoza R, Estay C, Rivera D. Bacteremia as an adverse event of fecal microbiota transplantation in a patient with Crohn’s disease and recurrent Clostridium difficile infection. J Crohns Colitis. 2014; 8:252–253.
Article
142. Baxter M, Ahmad T, Colville A, Sheridan R. Fatal aspiration pneumonia as a complication of fecal microbiota transplant. Clin Infect Dis. 2015; 61:136–137.
Article
143. Kelly CR, Ihunnah C, Fischer M, et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014; 109:10651071.
Article
144. 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; 46:479–493.
Article
145. Mattila E, Uusitalo-Seppälä R, Wuorela M, et al. Fecal transplantation, through colonoscopy, is effective therapy for recurrent Clostridium difficile infection. Gastroenterology. 2012; 142:490–496.
Article
146. Merrick B, Allen L, Zain NMM, Forbes B, Shawcross DL, Goldenberg SD. Regulation, risk and safety of faecal microbiota transplant. Infect Prev Pract. 2020; 2:100069.
Article
147. Porcari S, Benech N, Valles-Colomer M, et al. Key determinants of success in fecal microbiota transplantation: from microbiome to clinic. Cell Host Microbe. 2023; 31:712–733.
Article
148. U.S. Food and Drug Administration. Enforcement policy regarding investigational new drug requirements for use of fecal microbiota for transplantation to treat Clostridium difficile infection not responsive to standard therapies [Internet]. c2022 [cited 2023 Jul 9]. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/enforcementpolicy-regarding-investigational-new-drug-requirementsuse-fecal-microbiota.
149. U.S. Food and Drug Administration. FDA approves first fecal microbiota product [Internet]. c2022 [cited 2023 May 8]. https://www.fda.gov/news-events/press-announcements/fda-approves-first-fecal-microbiota-product.
150. European Commission. Proposal for a Regulation on substances of human origin [Internet]. c2023 [cited 2023 Jul 10]. https://health.ec.europa.eu/blood-tissues-cells-and-organs/overview/proposal-regulation-substances-human-origin_en.
151. de Stefano MC, Mazzanti B, Vespasiano F, Lombardini L, Cardillo M. The regulatory approach for faecal microbiota transplantation as treatment for Clostridioides difficile infection in Italy. Antibiotics (Basel). 2022; 11:480.
Article
152. Medicines and Healthcare products Regulatory Agency. A guide to what is a medicinal product [Internet]. c2020 [cited 2023 Jul 10]. https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/872742/GN8_FINAL_10_03_2020__combined_.pdf.
153. U.S. Food and Drug Administration Center for Biologics Evaluation and Research. Early clinical trials with live biotherapeutic products: chemistry, manufacturing, and control information [Internet]. c2021 [cited 2023 Sep 9]. https://www.fda.gov/media/82945/download.
154. Lee C, Louie T, Bancke L, et al. Safety of fecal microbiota, livejslm (REBYOTA™) in individuals with recurrent Clostridioides difficile infection: data from five prospective clinical trials. Therap Adv Gastroenterol. 2023; 16:17562848231174277.
155. Henn MR, O’Brien EJ, Diao L, et al. A phase 1b safety study of SER-287, a spore-based microbiome therapeutic, for active mild to moderate ulcerative colitis. Gastroenterology. 2021; 160:115–127.
Article
156. Businesswire. Seres therapeutics announces topline results for SER-287 phase 2b study in mild-to-moderate ulcerative colitis [Internet]. c2021 [cited 2023 Jul 18]. https://www.businesswire.com/news/home/20210722005276/en/Seres-Therapeutics-Announces-Topline-Results-for-SER-287-Phase-2bStudy-in-Mild-to-Moderate-Ulcerative-Colitis.
157. Oka A, Sartor RB. Microbial-based and microbial-targeted therapies for inflammatory bowel diseases. Dig Dis Sci. 2020; 65:757–788.
Article
158. Peng Z, Xiang J, He Z, et al. Colonic transendoscopic enteral tubing: a novel way of transplanting fecal microbiota. Endosc Int Open. 2016; 4:E610–E613.
Article
159. Ianiro G, Punčochář M, Karcher N, et al. Variability of strain engraftment and predictability of microbiome composition after fecal microbiota transplantation across different diseases. Nat Med. 2022; 28:1913–1923.
Article
Full Text Links
  • IR
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr