Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection

Alimentary Pharmacology and Therapeutics

Volumn 46, Issue 5, 2017, Pages 479-493

  Quraishi, M N ^a   Widlak, M ^b   Bhala, N ^a,c   Moore, D ^c   Price, M ^c   Sharma, N ^a,c   Iqbal, T H ^a,c  

^a UNIVERSITY HOSPITALS BIRMINGHAM NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY HOSPITALS COVENTRY AND WARWICKSHIRE NHS TRUST   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VANCOMYCIN;

CLINICAL EFFECTIVENESS; CLINICAL EVALUATION; CLOSTRIDIUM DIFFICILE INFECTION; COMPARATIVE EFFECTIVENESS; DONOR; DRUG EFFICACY; FECAL MICROBIOTA TRANSPLANTATION; HUMAN; META ANALYSIS; PREMEDICATION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RECURRENT INFECTION; REVIEW; RISK ASSESSMENT; SCREENING TEST; SEX RATIO; SYSTEMATIC REVIEW; TREATMENT OUTCOME; CLOSTRIDIUM INFECTION; COMPARATIVE STUDY; CROSS INFECTION; DIARRHEA; ISOLATION AND PURIFICATION; PEPTOCLOSTRIDIUM DIFFICILE; PROCEDURES;

CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; CROSS INFECTION; DIARRHEA; FECAL MICROBIOTA TRANSPLANTATION; HUMANS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TREATMENT OUTCOME; VANCOMYCIN;

EID: 85023628688     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.14201     Document Type: Review

References (72)

1. Public Health England. Clostridium difficile: guidance, data and analysis, 2015. https://www.gov.uk/government/collections/clostridium-difficile-guidance-data-and-analysis Accessed December 1, 2015.
2. National Institute for Health and Clinical Excellence. Faecal Microbiota Transplant for Recurrent Clostridium difficile infection. London: NICE; 2014. https://www.nice.org.uk/guidance/ipg485 Accessed September 2015.
3. Quraishi MN, Segal J, Mullish BH, et al. National survey of practice of faecal microbiota transplantation for Clostridium difficile infection in the UK. J Hosp Infect. 2017;95:444-445.
4. Nelson RL, Kelsey P, Leeman H, et al. Antibiotic treatment for Clostridium difficile-associated diarrhea in adults. Cochrane Database Syst Rev. 2011;3:CD004610.
5. O'Horo JC, Jindai K, Kunzer B, Safdar N. Treatment of recurrent Clostridium difficile infection: a systematic review. Infection. 2014;42:43-59.
6. Mullane KM, Miller MA, Weiss K, et al. Efficacy of fidaxomicin versus vancomycin as therapy for Clostridium difficile infection in individuals taking concomitant antibiotics for other concurrent infections. Clin Infect Dis. 2011;53:440-447.
7. Mullane K, Lee C, Bressler A, et al. Multicenter, randomized clinical trial to compare the safety and efficacy of LFF571 and vancomycin for Clostridium difficile infections. Antimicrob Agents Chemother. 2015;59:1435-1440.
8. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44:854-859.
9. Li Y-T, Cai H-F, Wang Z-H, Xu J, Fang J-Y. Systematic review with meta-analysis: long-term outcomes of faecal microbiota transplantation for Clostridium difficile infection. Aliment Pharmacol Ther. 2016;43:445-457.
10. Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500-508.
11. Drekonja D, Reich J, Gezahegn S, et al. Fecal microbiota transplantation for Clostridium difficile infection: a systematic review. Ann Intern Med. 2015;162:630-638.
12. Drekonja D, Reich J, Gezahegn S, et al. Fecal Microbiota Transplantation for Clostridium difficile Infection: A Systematic Review of the Evidence. Washington (DC): Department of Veterans Affairs (US); 2014.
13. Higgins JPT, Green S, (eds). Cochrane Handbook for Systematic Reviews of Interventions, Version 5.1.0. UK: The Cochrane Collaboration; 2011.
14. Moher D, Liberati A, Tetzlaff J, Altman DG & PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151, 264-269, W64
15. Centre for Reviews and Dissemination: CRD's Guidance for Undertaking Reviews in Health Care. University of York; 2009.
16. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177-188.
17. Riley RD, Higgins JPT, Deeks JJ. Interpretation of random effects meta-analyses. BMJ. 2011;342:d549.
18. Freeman MF, Tukey JW. Transformations related to the angular and the square root. Ann Math Stat. 1950;21:607-611.
19. Higgins JPT, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539-1558.
20. Higgins JPT, Thompson SG, Spiegelhalter DJ. A re-evaluation of random-effects meta-analysis. J R Stat Soc Ser A Stat Soc. 2009;172:137-159.
21. Duval S, Tweedie R. A nonparametric ‘Trim and Fill’ method of accounting for publication bias in meta-analysis. J Am Stat Assoc. 2000;95:89-98.
22. van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368:407-415.
23. 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;41:835-843.
24. 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;315:142-149.
25. Allegretti JR, Storm M, Smith M, et al. Su1739 strain-level analysis of microbial engraftment associated with resolution of recurrent Clostridium difficile following fecal microbiota transplantation. Gastroenterology. 2016;150:S540-S541.
26. Kao D, Roach B, Hotte N, et al. A prospective, dual center, randomized trial comparing colonoscopy versus capsule delivered fecal microbiota transplantation (FMT) in the management of recurrent Clostridium difficile infection (RCDI). Can J Gastroenterol Hepatol. 2016;2016: Article ID 4792898.
27. 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;165:609-616.
28. 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, open-label controlled pilot study. Clin Infect Dis. 2014;58:1515-1522.
29. Aroniadis OC, Brandt LJ, Greenberg A, et al. Long-term follow-up study of fecal microbiota transplantation for severe and/or complicated Clostridium difficile infection: a multicenter experience. J Clin Gastroenterol. 2016;50:398-402.
30. Kelly CR, Ihunnah C, Fischer M, et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065-1071.
31. Mandalia A, Ward A, Tauxe W, Kraft CS, Dhere T. Fecal transplant is as effective and safe in immunocompromised as non-immunocompromised patients for Clostridium difficile. Int J Colorectal Dis. 2016;31:1059-1060.
32. Allegretti JR, Fischer M, Papa E, et al. Su1738 fecal microbiota transplantation delivered via oral capsules achieves microbial engraftment similar to traditional delivery modalities: safety, efficacy and engraftment results from a multi-center cluster randomized dose-finding study. Gastroenterology. 2016;150:S540.
33. Aas J, Gessert CE, Bakken JS. Recurrent Clostridium difficile colitis: case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin Infect Dis Off Publ Infect Dis Soc Am. 2003;36:580-585.
34. Ganc AJ, Ganc RL, Reimao SM, Frisoli Junior A, Pasternak J. Fecal microbiota transplant by push enteroscopy to treat diarrhea caused by Clostridium difficile. Einstein Sao Paulo Braz. 2015;13:338-339.
35. Garborg K, Waagsbo B, Stallemo A, Matre J, Sundoy A. Results of faecal donor instillation therapy for recurrent Clostridium difficile-associated diarrhoea. Scand J Infect Dis. 2010;42:857-861.
36. Kelly CR, de Leon L, Jasutkar N. Fecal microbiota transplantation for relapsing Clostridium difficile infection in 26 patients: methodology and results. J Clin Gastroenterol. 2012;46:145-149.
37. Ray A, Smith R, Breaux J. Fecal microbiota transplantation for Clostridium difficile infection: the ochsner experience. Ochsner J. 2014;14:538-544.
38. Rohlke F, Surawicz CM, Stollman N. Fecal flora reconstitution for recurrent Clostridium difficile infection: results and methodology. J Clin Gastroenterol. 2010;44:567-570.
39. Rubin TA, Gessert CE, Aas J, Bakken JS. Fecal microbiome transplantation for recurrent Clostridium difficile infection: report on a case series. Anaerobe. 2013;19:22-26.
40. Satokari R, Mattila E, Kainulainen V, Arkkila PET. Simple faecal preparation and efficacy of frozen inoculum in faecal microbiota transplantation for recurrent Clostridium difficile infection – an observational cohort study. Aliment Pharmacol Ther. 2015;41:46-53.
41. Yoon SS, Brandt LJ. Treatment of refractory/recurrent C. difficile-associated disease by donated stool transplanted via colonoscopy: a case series of 12 patients. J Clin Gastroenterol. 2010;44:562-566.
42. Allegretti JR, Korzenik JR, Hamilton MJ. Fecal microbiota transplantation via colonoscopy for recurrent C. difficile infection. J Vis Exp. 2014;8:94.
43. Dutta SK, Girotra M, Garg S, et al. Efficacy of combined jejunal and colonic fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol. 2014;12:1572-1576.
44. Agrawal M, Aroniadis OC, Brandt LJ, et al. The long-term efficacy and safety of fecal microbiota transplant for recurrent, severe, and complicated Clostridium difficile infection in 146 elderly individuals. J Clin Gastroenterol. 2016;50:403-407.
45. Kronman MP, Nielson HJ, Adler AL, et al. Fecal microbiota transplantation via nasogastric tube for recurrent Clostridium difficile infection in pediatric patients. J Pediatr Gastroenterol Nutr. 2015;60:23-26.
46. Patel NC, Griesbach CL, DiBaise JK, Orenstein R. Fecal microbiota transplant for recurrent Clostridium difficile infection: Mayo Clinic in Arizona experience. Mayo Clin Proc. 2013;88:799-805.
47. 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.
48. Wadhwa A, Al Nahhas MF, Dierkhising RA, et al. High risk of post-infectious irritable bowel syndrome in patients with Clostridium difficile infection. Aliment Pharmacol Ther. 2016;44:576-582.
49. Orenstein R, Dubberke E, Hardi R, et al. Safety and durability of RBX2660 (microbiota suspension) for recurrent Clostridium difficile infection: results of the PUNCH CD study. Clin Infect Dis. 2016;62:596-602.
50. Petrof EO, et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome. 2013;1:3.
51. 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.e6
52. 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;149:110-118.e4.
53. Letter from the Presidents of the Infectious Disease Society of America, the American Gastroenterological Association, the American Society for Gastrointestinal Endoscopy, et al. Current Consensus Guidance on Donor Screening and Stool Testing for FMT, 2013.
54. Bakken JS, Borody T, Brandt LJ, et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9:1044-1049.
55. König J, Siebenhaar A, Högenauer C, et al. Consensus report: faecal microbiota transfer – clinical applications and procedures. Aliment Pharmacol Ther. 2017;45:222-239.
56. Medicines and Healthcare Regulatory Agency in the UK (MHRA). https://www.hta.gov.uk/policies/regulation-faecal-microbiota-transplant
57. Khanna S, Montassier E, Schmidt B, et al. Gut microbiome predictors of treatment response and recurrence in primary Clostridium difficile infection. Aliment Pharmacol Ther. 2016;44:715-727.
58. Allegretti JR, Kearney S, Li N, et al. Recurrent Clostridium difficile infection associates with distinct bile acid and microbiome profiles. Aliment Pharmacol Ther. 2016;43:1142-1153.
59. Fischer M, Kao D, Mehta SR, et al. Predictors of early failure after fecal microbiota transplantation for the therapy of Clostridium difficile infection: a multicenter study. Am J Gastroenterol. 2016;111:1024-1031.
60. Hamilton MJ, Weingarden AR, Sadowsky MJ, Khoruts A. Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012;107:761-767.
61. Kassam Z, Hundal R, Marshall JK, Lee CH. Fecal transplant via retention enema for refractory or recurrent Clostridium difficile infection. Arch Intern Med. 2012;172:191-193.
62. Khan MA, Sofi AA, Ahmad U, et al. Efficacy and safety of, and patient satisfaction with, colonoscopic-administered fecal microbiota transplantation in relapsing and refractory community- and hospital-acquired Clostridium difficile infection. Can J Gastroenterol Hepatol. 2014;28:434-438.
63. Lee CH, Belanger JE, Kassam Z, et al. The outcome and long-term follow-up of 94 patients with recurrent and refractory Clostridium difficile infection using single to multiple fecal microbiota transplantation via retention enema. Eur J Clin Microbiol Infect Dis. 2014;33:1425-1428.
64. MacConnachie AA, Fox R, Kennedy DR, Seaton RA. Faecal transplant for recurrent Clostridium difficile-associated diarrhoea: a UK case series. QJM Mon J Assoc Physicians. 2009;102:781-784.
65. Pathak R, Enuh HA, Patel A, Wickremesinghe P. Treatment of relapsing Clostridium difficile infection using fecal microbiota transplantation. Clin Exp Gastroenterol. 2013;7:1-6.
66. Tauxe WM, Haydek JP, Rebolledo PA, et al. Fecal microbiota transplant for Clostridium difficile infection in older adults. Ther Adv Gastroenterol. 2016;9:273-281.
67. Zainah H, Hassan M, Shiekh-Sroujieh L, Hassan S, Alangaden G, Ramesh M. Intestinal microbiota transplantation, a simple and effective treatment for severe and refractory Clostridium difficile infection. Dig Dis Sci. 2015;60:181-185.
68. Brandt LJ, Aroniadis OC, Mellow M, et al. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012;107:1079-1087.
69. Costello SP, Conlon MA, Vuaran MS, Roberts-Thomson IC, Andrews JM. Faecal microbiota transplant for recurrent Clostridium difficile infection using long-term frozen stool is effective: clinical efficacy and bacterial viability data. Aliment Pharmacol Ther. 2015;42:1011-1018.
70. Emanuelsson F, Claesson BEB, Ljungstrom L, Tvede M, Ung K-A. Faecal microbiota transplantation and bacteriotherapy for recurrent Clostridium difficile infection: a retrospective evaluation of 31 patients. Scand J Infect Dis. 2014;46:89-97.
71. Youngster I, et al. Oral, capsulized, frozen fecal microbiota transplantation for relapsing Clostridium difficile infection. JAMA. 2014;312:1772-1778.
72. Vigvari S, Nemes Z, Vincze A, et al. Experience with fecal transplantation in the treatment of Clostridium difficile infection. Orv Hetil. 2014;155:1758-1762.