Clinical application and potential of fecal microbiota transplantation

Annual Review of Medicine

Volumn 70, Issue , 2019, Pages 335-351

  Ooijevaar, R E ^a   Terveer, E M ^b   Verspaget, H W ^b   Kuijper, E J ^b   Keller, J J ^b,c  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c MEDICAL CENTER HAAGLANDEN   (Netherlands)

Author keywords

CDI; Clostridioides Clostridium difficile infection; fecal microbiota transplantation; FMT; hepatic encephalopathy; IBD; IBS; inflammatory bowel disease; irritable bowel syndrome

Indexed keywords

SHORT CHAIN FATTY ACID;

ANTIBIOTIC RESISTANCE; AUTISM; BILE ACID METABOLISM; CLINICAL PROTOCOL; CLOSTRIDIUM DIFFICILE INFECTION; DYSBIOSIS; FECAL MICROBIOTA TRANSPLANTATION; FECES ANALYSIS; GRAFT VERSUS HOST REACTION; HEPATIC ENCEPHALOPATHY; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; IRRITABLE COLON; METABOLIC SYNDROME X; MICROBIAL COLONIZATION; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; STANDARDIZATION; TREATMENT INDICATION; CLOSTRIDIUM INFECTION; FEMALE; FORECASTING; MALE; PATIENT SAFETY; PROCEDURES; RISK ASSESSMENT; TREATMENT OUTCOME;

CLOSTRIDIUM INFECTIONS; FECAL MICROBIOTA TRANSPLANTATION; FEMALE; FORECASTING; HUMANS; IRRITABLE BOWEL SYNDROME; MALE; PATIENT SAFETY; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK ASSESSMENT; TREATMENT OUTCOME;

EID: 85060583802     PISSN: 00664219     EISSN: 1545326X     Source Type: Book Series    
DOI: 10.1146/annurev-med-111717-122956     Document Type: Review

References (100)

1. Debast SB, Bauer MP, Kuijper EJ, Eur. Soc. Clin.Microbiol. Infect. Dis. 2014. European Society of Clinical Microbiology and Infectious Diseases: Update of the treatment guidance document for Clostridium difficile infection. Clin. Microbiol. Infect. 20(Suppl. 2):1-26
2. McDonald LC, Gerding DN, Johnson S, et al. 2018. 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). Clin. Infect. Dis. 66:987-94
3. Quraishi MN, Widlak M, Bhala N, et al. 2017. Systematic review with meta-analysis: The efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment. Pharmacol. Ther. 46:479-93
4. SmitsWK, Lyras D, Lacy DB, et al. 2016. Clostridium difficile infection. Nat. Rev. Dis. Primers 2:16020
5. Sender R, Fuchs S, Milo R. 2016. Revised estimates for the number of human and bacteria cells in the body. PLOS Biol. 14:e1002533
6. Lozupone CA, Stombaugh JI, Gordon JI, et al. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489:220-30
7. Rothschild D, WeissbrodO, Barkan E, et al. 2018. Environment dominates over host genetics in shaping human gut microbiota. Nature 555:210-15
8. Hum. Microbiome Proj. Consort. 2012. Structure, function and diversity of the healthy human microbiome. Nature 486:207-14
9. Kim S, Covington A, Pamer EG. 2017. The intestinal microbiota: Antibiotics, colonization resistance, and enteric pathogens. Immunol. Rev. 279:90-105
10. Cotter PD, Ross RP, Hill C. 2013. Bacteriocins-a viable alternative to antibiotics?Nat. Rev. Microbiol. 11:95-105
11. Hecht AL, Casterline BW, Earley ZM, et al. 2016. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep. 17:1281-91
12. OfirG, Sorek R. 2018. Contemporary phage biology: From classicmodels to new insights. Cell 172:1260-70
13. Khoruts A, Sadowsky MJ. 2016. Understanding the mechanisms of faecal microbiota transplantation. Nat. Rev. Gastroenterol. Hepatol. 13:508-16
14. Hooper LV, Macpherson AJ. 2010. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat. Rev. Immunol. 10:159-69
15. Morrison DJ, Preston T. 2016. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7:189-200
16. den Besten G, van Eunen K, Groen AK, et al. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54:2325-40
17. Park J, Kim M, Kang SG, et al. 2015. Short-chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol. 8:80-93
18. Rooks MG, Garrett WS. 2016. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16:341-52
19. Corrêa-Oliveira R, Fachi JL, Vieira A, et al. 2016. Regulation of immune cell function by short-chain fatty acids. Clin. Transl. Immunol. 5:e73
20. Wahlstr öm A, Sayin SI, Marschall HU, Bäckhed F. 2016. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism. Cell Metab. 24:41-50
21. Ridlon JM, Kang DJ, Hylemon PB. 2006. Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47:241-59
22. Inagaki T, Moschetta A, Lee YK, et al. 2006. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. PNAS 103:3920-25
23. Cipriani S, Mencarelli A, Chini MG, et al. 2011. The bile acid receptor GPBAR-1 (TGR5) modulates integrity of intestinal barrier and immune response to experimental colitis. PLOS ONE 6:e25637
24. Högenauer K, Arista L, Schmiedeberg N, et al. 2014. G-protein-coupled bile acid receptor 1 (GPBAR1, TGR5) agonists reduce the production of proinflammatory cytokines and stabilize the alternative macrophage phenotype. J. Med. Chem. 57:10343-54
25. Vavassori P, Mencarelli A, Renga B, et al. 2009. The bile acid receptor FXR is a modulator of intestinal innate immunity. J. Immunol. 183:6251-61
26. Thanissery R, Winston JA, Theriot CM. 2017. Inhibition of spore germination, growth, and toxin activity of clinically relevant C. difficile strains by gut microbiota derived secondary bile acids. Anaerobe 45:86-100
27. Chang JY, Antonopoulos DA, Kalra A, et al. 2008. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J. Infect. Dis. 197:435-38
28. Deshpande A, Pasupuleti V, Thota P, et al. 2015. Risk factors for recurrent Clostridium difficile infection: A systematic review and meta-analysis. Infect. Control Hosp. Epidemiol. 36:452-60
29. Adamu BO, Lawley TD. 2013. Bacteriotherapy for the treatment of intestinal dysbiosis caused by Clostridium difficile infection. Curr. Opin. Microbiol. 16:596-601
30. Cammarota G, Masucci L, Ianiro G, et al. 2015. Randomised clinical trial: Faecal microbiota transplantation by colonoscopy vs. vancomycin for the treatment of recurrent Clostridium difficile infection. Aliment. Pharmacol. Ther. 41:835-43
31. Kao D, Roach B, SilvaM, et al. 2017. Effect of oral capsule- versus colonoscopy-delivered fecal microbiota transplantation on recurrent Clostridium difficile infection: A randomized clinical trial. JAMA 318:1985-93
32. van Nood E, Vrieze A, Nieuwdorp M, et al. 2013. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368:407-15
33. Lee CH, Steiner T, Petrof EO, et al. 2016. Frozen versus fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: A randomized clinical trial. JAMA 315:142-49
34. Hocquart M, Lagier JC, Cassir N, et al. 2018. Early fecal microbiota transplantation improves survival in severe Clostridium difficile infections. Clin. Infect. Dis. 66:645-50
35. OrensteinR, DubberkeE, Hardi R, et al. 2016. Safety and durability ofRBX2660 (microbiota suspension) for recurrent Clostridium difficile infection: Results of the PUNCH CDstudy. Clin. Infect. Dis. 62:596-602
36. Baur D, Gladstone BP, Burkert F, et al. 2017. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: A systematic review and meta-analysis. Lancet Infect. Dis. 17:990-1001
37. Youngster I, Mahabamunuge J, SystromHK, et al. 2016. Oral, frozen fecal microbiota transplant (FMT) capsules for recurrent Clostridium difficile infection. BMC Med. 14:134
38. Maier L, Pruteanu M, Kuhn M, et al. 2018. Extensive impact of non-antibiotic drugs on human gut bacteria. Nature 555:623-28
39. Angelberger S, Reinisch W, Makristathis A, et al. 2013. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am. J. Gastroenterol. 108:1620-30
40. Quera R, Espinoza R, Estay C, Rivera D. 2014. Bacteremia as an adverse event of fecal microbiota transplantation in a patient with Crohn's disease and recurrent Clostridium difficile infection. J. Crohns Colitis 8:252-53
41. Vermeire S, Joossens M, Verbeke K, et al. 2012. Pilot study on the safety and efficacy of faecal microbiota transplantation in refractory Crohn's disease. Gastroenterology 142(Suppl. 1):S360
42. Terveer EM, van Beurden YH, Goorhuis A, et al. 2017. How to: Establish and run a stool bank. Clin. Microbiol. Infect. 23:924-30
43. McIlroy J, Ianiro G, Mukhopadhya I, et al. 2018. Review article: The gut microbiome in inflammatory bowel disease-avenues for microbial management. Aliment. Pharm. Ther. 47:26-42
44. Critch J, Day AS, Otley A, et al. 2012. Use of enteral nutrition for the control of intestinal inflammation in pediatric Crohn disease. J. Pediatr. Gastroenterol. Nutr. 54:298-305
45. Ledder O, Turner D. 2018. Antibiotics in IBD: Still a role in the biological era? Inflamm. Bowel Dis. 24:1676-88
46. De Cruz P, Prideaux L, Wagner J, et al. 2012. Characterization of the gastrointestinal microbiota in health and inflammatory bowel disease. Inflamm. Bowel Dis. 18:372-90
47. Costello S, Waters O, Bryant R, et al. 2017. Short duration, low intensity pooled faecal microbiota transplantation induces remission in patients with mild-moderately active ulcerative colitis: A randomised controlled trial. J. Crohns Colitis 11:S23
48. Moayyedi P, Surette MG, Kim PT, et al. 2015. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149:102-9.e6
49. Paramsothy S, Kamm MA, Kaakoush NO, et al. 2017. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: A randomised placebo-controlled trial. Lancet 389:1218-28
50. Rossen NG, Fuentes S, van der Spek MJ, et al. 2015. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 149:110-18.e4
51. Costello SP, Soo W, Bryant RV, et al. 2017. Systematic review with meta-analysis: Faecal microbiota transplantation for the induction of remission for active ulcerative colitis. Aliment. Pharmacol. Ther. 46:213-24
52. Paramsothy S, Paramsothy R, RubinDT, et al. 2017. Faecal microbiota transplantation for inflammatory bowel disease: A systematic review and meta-analysis. J. Crohns Colitis 11:1180-99
53. Cui B, Feng Q, Wang H, et al. 2015. Fecal microbiota transplantation through mid-gut for refractory Crohn's disease: Safety, feasibility, and efficacy trial results. J. Gastroenterol. Hepatol. 30:51-58
54. Vermeire S, Joossens M, Verbeke K, et al. 2016. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J. Crohns Colitis 10:387-94
55. Chen T, Zhou Q, Zhang D, et al. 2018. Effect of faecal microbiota transplantation for treatment of Clostridium difficile infection in patients with inflammatory bowel disease: A systematic review and metaanalysis of cohort studies. J. Crohns Colitis 12:710-17
56. Zhuang X, Xiong L, Li L, et al. 2017. Alterations of gut microbiota in patients with irritable bowel syndrome: A systematic review and meta-analysis. J. Gastroenterol. Hepatol. 32:28-38
57. Camilleri M, Madsen K, Spiller R, et al. 2012. Intestinal barrier function in health and gastrointestinal disease. Neurogastroenterol. Motil. 24:503-12
58. De Palma G, Lynch MDJ, Lu J, et al. 2017. Transplantation of fecal microbiota from patients with irritable bowel syndrome alters gut function and behavior in recipient mice. Sci. Transl.Med. 9:eaaf6397
59. Johnsen PH, Hilpüsch F, Cavanagh JP, et al. 2018. Faecal microbiota transplantation versus placebo for moderate-to-severe irritable bowel syndrome: A double-blind, randomised, placebo-controlled, parallelgroup, single-centre trial. Lancet Gastroenterol. Hepatol. 3:17-24
60. Halkjær SI, Boolsen AW, Günther S, et al. 2017. Can fecal microbiota transplantation cure irritable bowel syndrome? World J. Gastroenterol. 23:4112-20
61. Bajaj JS, Heuman DM, Hylemon PB, et al. 2014. Altered profile of human gut microbiome is associated with cirrhosis and its complications. J. Hepatol. 60:940-47
62. Zhang Z, Zhai H, Geng J, et al. 2013. Large-scale survey of gut microbiota associated with MHE via 16S rRNA-based pyrosequencing. Am. J. Gastroenterol. 108:1601-11
63. Shawcross DL, Davies NA, Williams R, Jalan R. 2004. Systemic inflammatory response exacerbates the neuropsychological effects of induced hyperammonemia in cirrhosis. J. Hepatol. 40:247-54
64. Ahluwalia V, Betrapally NS, Hylemon PB, et al. 2016. Impaired gut-liver-brain axis in patients with cirrhosis. Sci. Rep. 6:26800
65. Bajaj JS, Kassam Z, Fagan A, et al. 2017. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: A randomized clinical trial. Hepatology 66:1727-38
66. MacMillan ML, DeFor TE, Weisdorf DJ. 2012. What predicts high risk acute graft-versus-host disease (GVHD) at onset?: Identification of those at highest risk by a novel acute GVHD risk score. Br. J. Haematol. 157:732-41
67. Mathewson ND, Jenq R, Mathew AV, et al. 2016. Gut microbiome-derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versus-host disease. Nat. Immunol. 17:505-13
68. Kakihana K, Fujioka Y, Suda W, et al. 2016. Fecal microbiota transplantation for patients with steroidresistant acute graft-versus-host disease of the gut. Blood 128:2083-88
69. Spindelboeck W, Schulz E, Uhl B, et al. 2017. Repeated fecal microbiota transplantations attenuate diarrhea and lead to sustained changes in the fecal microbiota in acute, refractory gastrointestinal graftversus-host-disease. Haematologica 102:e210-13
70. Millan B, Park H, Hotte N, et al. 2016. Fecal microbial transplants reduce antibiotic-resistant genes in patients with recurrent Clostridium difficile infection. Clin. Infect. Dis. 62:1479-86
71. Liu B, Pop M. 2009. ARDB-antibiotic resistance genes database. Nucleic Acids Res. 37:D443-47
72. Bilinski J, Grzesiowski P, Sorensen N, et al. 2017. Fecal microbiota transplantation in patients with blood disorders inhibits gut colonizationwith antibiotic-resistant bacteria: Results of a prospective, single-center study. Clin. Infect. Dis. 65:364-70
73. Davido B, Batista R, Michelon H, et al. 2017. Is faecal microbiota transplantation an option to eradicate highly drug-resistant enteric bacteria carriage? J. Hosp. Infect. 95:433-37
74. Dinh A, Fessi H, Duran C, et al. 2018. Clearance of carbapenem-resistant Enterobacteriaceae versus vancomycin-resistant enterococci carriage after fecal microbiota transplant: A prospective comparative study. J. Hosp. Infect. 99:481-86
75. Singh R, de Groot PF, Geerlings SE, et al. 2018. Fecal microbiota transplantation against intestinal colonization by extended spectrum beta-lactamase producing Enterobacteriaceae: A proof of principle study. BMC Res. Notes 11:190
76. Kommineni S, Bretl DJ, Lam V, et al. 2015. Bacteriocin production augments niche competition by enterococci in the mammalian gastrointestinal tract. Nature 526:719-22
77. de Groot PF, Frissen MN, de Clercq NC, Nieuwdorp M. 2017. Fecal microbiota transplantation in metabolic syndrome: History, present and future. Gut Microbes 8:253-67
78. Kootte RS, Levin E, Salojärvi J, et al. 2017. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab. 26:611-19.e6
79. Vrieze A, Van Nood E, Holleman F, et al. 2012. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143:913-16.e7
80. McElhanon BO, McCracken C, Karpen S, Sharp WG. 2014. Gastrointestinal symptoms in autism spectrum disorder: A meta-analysis. Pediatrics 133:872-83
81. Niehus R, Lord C. 2006. Earlymedical history of children with autism spectrum disorders. J. Dev. Behav. Pediatr. 27:S120-27
82. Slykerman RF, Thompson J, Waldie KE, et al. 2017. Antibiotics in the first year of life and subsequent neurocognitive outcomes. Acta Paediatr. 106:87-94
83. Hsiao EY, McBride SW, Hsien S, et al. 2013. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell 155:1451-63
84. Kang D-W, Adams JB, Gregory AC, et al. 2017. Microbiota transfer therapy alters gut ecosystem and improves gastrointestinal and autism symptoms: An open-label study. Microbiome 5:10
85. Borody T, Leis S, Campbell J, et al. 2011. Fecal microbiota transplantation (FMT) in multiple sclerosis (MS). Am. J. Gastroenterol. 106:S352
86. Fang S, Kraft CS, Dhere T, et al. 2016. Successful treatment of chronic Pouchitis utilizing fecal microbiota transplantation (FMT): A case report. Int. J. Colorectal Dis. 31:1093-94
87. Günaltay S, Rademacher L, Hultgren Hörnquist E, et al. 2017. Clinical and immunologic effects of faecal microbiota transplantation in a patient with collagenous colitis. World J. Gastroenterol. 23:1319-24
88. Makkawi S, Camara-Lemarroy C, Metz L. 2018. Fecal microbiota transplantation associated with 10 years of disease stability in a patient with SPMS. Neurol. Neuroimmunol. Neuroinflamm. 5(4):e459
89. Tian H, Ge X, Nie Y, et al. 2017. Fecal microbiota transplantation in patients with slow-transit constipation: A randomized, clinical trial. PLOS ONE 12:e0171308
90. van Beurden YH, van Gils T, van Gils NA, et al. 2016. Serendipity in refractory celiac disease: Full recovery of duodenal villi and clinical symptoms after fecal microbiota transfer. J. Gastrointestin. Liver Dis. 25:385-88
91. Freedman SN, Shahi SK, Mangalam AK. 2018. The "gut feeling": Breaking down the role of gut microbiome in multiple sclerosis. Neurotherapeutics 15:109-25
92. Shahi SK, Freedman SN, Mangalam AK. 2017. Gutmicrobiome inmultiple sclerosis: The players involved and the roles they play. Gut Microbes 8:607-15
93. BererK, Gerdes LA, Cekanaviciute E, et al. 2017. Gutmicrobiota frommultiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. PNAS 114:10719-24
94. Cekanaviciute E, Yoo BB, Runia TF, et al. 2017. Gut bacteria from multiple sclerosis patients modulate human T cells and exacerbate symptoms in mouse models. PNAS 114:10713-18
95. Sampson TR, Debelius JW, Thron T, et al. 2016. Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease. Cell 167:1469-80.e12
96. UngerMM, Spiegel J, DillmannKU, et al. 2016. Short chain fatty acids and gutmicrobiota differ between patients with Parkinson's disease and age-matched controls. Parkinsonism Relat. Disord. 32:66-72
97. Sun MF, Zhu YL, Zhou ZL, et al. 2018. Neuroprotective effects of fecal microbiota transplantation on MPTP-induced Parkinson's disease mice: Gut microbiota, glial reaction and TLR4/TNF-α signaling pathway. Brain Behav. Immun. 70:48-60
98. Sivan A, Corrales L, Hubert N, et al. 2015. Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350:1084-89
99. Gopalakrishnan V, Spencer CN, Nezi L, et al. 2018. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 359:97-103
100. Routy B, Le Chatelier E, Derosa L, et al. 2018. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 359:91-97