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Fecal Microbiota Transplantation (FMT) with Colonoscopy Is Superior to Enema and Nasogastric Tube While Comparable to Capsule for the Treatment of Recurrent Clostridioides difficile Infection: A Systematic Review and Meta-Analysis

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Abstract

Background

Several routes of fecal microbiota transplantation (FMT) administration are available for treating recurrent Clostridioides difficile infections (CDI), the most recent of which are capsules.

Aim

To assess the efficacy of colonoscopy, capsule, enema, and nasogastric tube (NGT) FMT for the treatment of recurrent CDI.

Methods

We reported clinical outcomes of colonoscopy, capsule, enema, and NGT FMT for the treatment of recurrent CDI according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. During January 2000 to January 2018, three databases were searched: PubMed, EMBASE, and CINAHL. Primary outcome was overall cure rate which was assessed using a random effects model; secondary outcomes included adverse effects as well as subgroup analyses comparing donor relationship, sample preparation, and study design.

Results

Twenty-six studies (1309 patients) were included in the study. FMT was administered using colonoscopy in 16 studies (483 patients), NGT in five studies (149 patients), enema in four studies (360 patients), and capsules in four studies (301 patients). The random effects of pooled FMT cure rates were colonoscopy 94.8% (CI 92.4–96.8%; I2 15.6%), capsule 92.1% (CI 88.6–95.0%; I2 7.1%), enema 87.2% (CI 83.4–90.5%; I2 0%), and NGT/NDT 78.1% (CI 71.6–84.1%; I2 0%). On subgroup analysis of colonoscopy FMT, sample preparation methods had comparable cure rates: fresh 94.9% compared to 94.5%. Similarly, cure rates were unaffected by donor relationship: mixed 94.5% compared to unrelated donor 95.7%.

Conclusion

CDI cure rates with FMT performed with colonoscopy are superior to enema and NGT FMT, while those with FMT with colonoscopy and capsule are comparable.

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References

  1. Zimlichman E, Henderson D, Tamir O, et al. Health care associated infections: a metaanalysis of costs and financial impact on the US health care system. Jama Intern Med. 2013;173:2039–2046.

    Article  Google Scholar 

  2. Olsen MA, Yan Y, Reske KA, et al. Recurrent Clostridium difficile infection is associated with increased mortality. Clin Microbiol Infect. 2015;21:164–170.

    Article  CAS  Google Scholar 

  3. Zhang S, Palazuelos-Munoz S, Balsells EM, et al. Cost of hospital management of clostridium difficile infection in United States: a meta analysis and modeling study. Bmc Infect Dis. 2016;16:447.

    Article  Google Scholar 

  4. Gupta A, Khanna S. Fecal microbiota transplantation. J Am Med Assoc. 2017;318:102.

    Article  Google Scholar 

  5. Surawicz CM, Brandt LJ, Binion DG, et al. Guidelines for diagnosis, treatment and prevention of clostridium difficile infections. Am J Gastroenterol. 2013;108:478–498.

    Article  CAS  Google Scholar 

  6. Zhang F, Luo W, Shi Y, et al. Should we standardize the 1700 year old fecal microbiota transplantation? Am J Gastroenterol. 2012;107:1755.

    Article  Google Scholar 

  7. Eiseman B, Silen W, Bascom GS, et al. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44:854–859.

    CAS  PubMed  Google Scholar 

  8. 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. 2003;36:580–585.

    Article  Google Scholar 

  9. 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.

    Article  Google Scholar 

  10. 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 Pharm Ther. 2015;41:835–843.

    Article  CAS  Google Scholar 

  11. Costello SP, Conlon MA, Vuaran MS, et al. Faecal microbiota transplant for recurrent clostridium difficile infection using long term frozen stool is effective: Clinical efficacy and bacterial viability data. Aliment Pharm Ther. 2015;42:1011–1018.

    Article  CAS  Google Scholar 

  12. Gundacker ND, Tamhane A, Walker JB, et al. Comparative effectiveness of faecal microbiota transplant by route of administration. J Hosp Infect. 2017;96:349–352.

    Article  CAS  Google Scholar 

  13. Hirsch BE, Saraiya N, Poeth K, et al. Effectiveness of fecal derived microbiota transfer using orally administered capsules for recurrent clostridium difficile infection. BMC Infect Dis. 2015;15:191–199.

    Article  Google Scholar 

  14. Hota SS, Sales V, Tomlinson G, et al. Oral vancomycin followed by fecal transplantation versus tapering oral vancomycin treatment for recurrent clostridium difficile infection: An open label, randomized controlled trial. Clin Infect Dis. 2017;64:265–271.

    Article  Google Scholar 

  15. Jiang ZD, Ajami NJ, Petrosino JF, et al. Randomised clinical trial: faecal microbiota transplantation for recurrent clostridum difficile infection: fresh, or frozen, or lyophilised microbiota from a small pool of healthy donors delivered by colonoscopy. Aliment Pharm Ther. 2017;45:899–908.

    Article  CAS  Google Scholar 

  16. 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. J Am Med Assoc. 2017;318:1985–1993.

    Article  CAS  Google Scholar 

  17. 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;46:145149.

    Google Scholar 

  18. 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.

    Article  Google Scholar 

  19. 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. 2014;28:434–438.

    Google Scholar 

  20. Lee CH, Belanger JE, Smieja M, 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. 2014;33:1425–1428.

    Article  CAS  Google Scholar 

  21. 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. J Am Med Assoc. 2016;315:142–149.

    Article  CAS  Google Scholar 

  22. MacConnachie AA, Fox R, Kennedy DR, et al. Faecal transplant for recurrent clostridium difficile associated diarrhoea: a UK case series. Qjm Mon J Assoc Phys. 2009;102:781–784.

    CAS  Google Scholar 

  23. 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  Google Scholar 

  24. Mellow MH, Kanatzar A. Colonoscopic fecal bacteriotherapy in the treatment of recurrent clostridium difficile infection: results and follow up. J Okla St Med Assoc. 2011;104:89–91.

    Google Scholar 

  25. van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent clostridium difficile. New Engl J Med. 2013;368:407–415.

    Article  Google Scholar 

  26. 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.

    Article  Google Scholar 

  27. Patel NC, Griesbach CL, DiBaise JK, et al. Fecal microbiota transplant for recurrent clostridium difficile infection: Mayo clinic in Arizona experience. Mayo Clin Proc. 2013;88:799–805.

    Article  Google Scholar 

  28. Rohlke F, Surawicz CM, Stollman N. Fecal flora reconstitution for recurrent clostridium difficile infection: Results and methodology. J Clin Gastroenterol. 2010;44:567–570.

    Article  Google Scholar 

  29. Rubin TA, Aas J, Gessert CE, et al. Fecal microbiome transplantation for recurrent clostridium difficile infection: Report on a case series. Anaerobe. 2013;19:22–26.

    Article  Google Scholar 

  30. Staley C, Hamilton MJ, Vaughn BP, et al. Successful resolution of recurrent clostridium difficile infection using freeze dried, encapsulated fecal microbiota; pragmatic cohort study. Am J Gastroenterol. 2017;112:940–947.

    Article  Google Scholar 

  31. 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.

    Article  Google Scholar 

  32. Youngster I, Mahabamunuge J, Systrom HK, et al. Oral, frozen fecal microbiota transplant (FMT) capsules for recurrent clostridium difficile infection. BMC Med. 2016;14:134–137.

    Article  Google Scholar 

  33. 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.

    Article  Google Scholar 

  34. 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 Pharm Ther. 2017;46:479–493.

    Article  CAS  Google Scholar 

  35. Tang G, Yin W, Liu W. Is frozen fecal microbiota transplantation as effective as fresh fecal microbiota transplantation in patients with recurrent or refractory clostridium difficile infection: a meta analysis? Diagn Micr Infec Dis. 2017;1:322–329.

    Article  Google Scholar 

  36. Allegretti JR, Fischer M, Sagi SV, et al. Fecal microbiota transplantation capsules with targeted colonic versus gastric delivery in recurrent Clostridium difficile infection: A comparative cohort analysis of high and lose dose. Dig Dis Sci. 2019;64:1672–1678. https://doi.org/10.1007/s10620-018-5396-6.

    Article  CAS  PubMed  Google Scholar 

  37. Staley C, Kaiser T, Vaughn BP, et al. Predicting recurrence of Clostridium difficile infection following encapsulated fecal microbiota transplantation. Microbiome.. 2018;6:166.

    Article  Google Scholar 

  38. Li YT, Cai HF, Wang ZH, et al. Systematic review with meta analysis: Long term outcomes of faecal microbiota transplantation for clostridium difficile infection. Aliment Pharm Ther. 2016;43:44.

    Google Scholar 

  39. Le P, Nghiem VT, Mullen PD, Deshpande A. Cost-effectiveness of competing treatment strategies for Clostridium difficile infection: A systematic review. Infect Control Hosp Epidemiol. 2018;39:412–424.

    Article  Google Scholar 

  40. Dehlholm-Lambertsen E, Hall BK, Jørgensen SM, et al. Cost savings following faecal microbiota transplantation for recurrent Clostridium difficile infection. Ther Adv Gastroenterol. 2019;12:1756284819843002.

    Article  Google Scholar 

  41. Luo Y, Lucas AL, Grinspan AM. Fecal transplants by colonoscopy and capsules are cost-effective strategies for treating recurrent clostridioides difficile infection. Dig Dis Sci. 2019;6:1–9. https://doi.org/10.1007/s10620-019-05821-1.

    Article  CAS  Google Scholar 

  42. Shaffer S, Rubin DT, Targownik L, et al. Cost-effectiveness analysis of starting a Fecal Microbiota Transplantation (FMT) Unit for the Treatment of Recurrent C. difficile infection compared with antibiotic therapy 179. Am J Gastroenterol. 2019;114:S110–S111.

    Article  Google Scholar 

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Contributions

DR was involved in conception of idea and study design. DR and KZ contributed to study search, review, and selection. DR, KZ, and AO contributed to data collection and synthesis. DR and PF contributed to statistical analysis and interpretation of results. DR, GP, VS, and JL drafted the manuscript. SC, MR, and AD drafted the manuscript and contributed to critical revision of the article for important intellectual content and final approval of the manuscript.

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Correspondence to Daryl Ramai.

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Ramai, D., Zakhia, K., Fields, P.J. et al. Fecal Microbiota Transplantation (FMT) with Colonoscopy Is Superior to Enema and Nasogastric Tube While Comparable to Capsule for the Treatment of Recurrent Clostridioides difficile Infection: A Systematic Review and Meta-Analysis. Dig Dis Sci 66, 369–380 (2021). https://doi.org/10.1007/s10620-020-06185-7

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