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Meta-Analysis
. 2018 Nov 13;11(11):CD012774.
doi: 10.1002/14651858.CD012774.pub2.

Fecal transplantation for treatment of inflammatory bowel disease

Aamer Imdad  1 , Maribeth R Nicholson, Emily E Tanner-Smith, Joseph P Zackular, Oscar G Gomez-Duarte, Dawn B Beaulieu, Sari Acra
Affiliations
Meta-Analysis

Fecal transplantation for treatment of inflammatory bowel disease

Aamer Imdad et al. Cochrane Database Syst Rev. .

Update in

  • Fecal transplantation for treatment of inflammatory bowel disease.
    Imdad A, Pandit NG, Zaman M, Minkoff NZ, Tanner-Smith EE, Gomez-Duarte OG, Acra S, Nicholson MR. Imdad A, et al. Cochrane Database Syst Rev. 2023 Apr 25;4(4):CD012774. doi: 10.1002/14651858.CD012774.pub3. Cochrane Database Syst Rev. 2023. PMID: 37094824 Free PMC article. Review.

Abstract

Background: Inflammatory bowel disease (IBD) is a chronic, relapsing disease of the gastrointestinal tract that is thought to be associated with a complex interplay between microbes and the immune system, leading to an abnormal inflammatory response in genetically susceptible individuals. Dysbiosis, characterized by the alteration of the composition of the resident commensal bacteria in a host compared to healthy individuals, is thought to play a major role in the pathogenesis of ulcerative colitis (UC) and Crohn's disease (CD), two subtypes of IBD. There is growing interest to correct the underlying dysbiosis through the use of fecal microbiota transplantation (FMT) for the treatment of IBD.

Objectives: The objective of this systematic review was to assess the efficacy and safety of FMT for the treatment of IBD.

Search methods: We searched the MEDLINE, Embase, Cochrane Library, and Cochrane IBD Group Specialized Register databases from inception to 19 March 2018. We also searched ClinicalTrials.gov, ISRCTN metaRegister of Controlled Trials, and the Conference Proceedings Citation Index.

Selection criteria: Only randomized trials or non-randomized studies with a control arm were considered for inclusion. Adults or pediatric participants with UC or CD were eligible for inclusion. Eligible interventions were FMT defined as the administration of fecal material containing distal gut microbiota from a healthy donor to the gastrointestinal tract of a someone with UC or CD. The comparison group included participants who did not receive FMT and were given placebo, autologous FMT, or no intervention.

Data collection and analysis: Two authors independently screened the titles and extracted data from the included studies. We used the Cochrane risk of bias tool to assess study bias. The primary outcomes were induction of clinical remission, clinical relapse, and serious adverse events. Secondary outcomes included clinical response, endoscopic remission and endoscopic response, quality of life scores, laboratory measures of inflammation, withdrawals, and microbiome outcomes. We calculated the risk ratio (RR) and corresponding 95% confidence interval (95% CI) for dichotomous outcomes and the mean difference and 95% CI for continuous outcomes. Random-effects meta-analysis models were used to synthesize effect sizes across trials. The overall certainty of the evidence supporting the primary and selected secondary outcomes was rated using the GRADE criteria.

Main results: Four studies with a total of 277 participants were included. These studies assessed the efficacy of FMT for treatment of UC in adults; no eligible trials were found for the treatment of CD. Most participants had mild to moderate UC. Two studies were conducted in Australia, one study was conducted in Canada, and another in the Netherlands. Three of the included studies administered FMT via the rectal route and one study administered FMT via the nasoduodenal route. Three studies were rated as low risk of bias. One study (abstract publication) was rated as unclear risk of bias. Combined results from four studies (277 participants) suggest that FMT increases rates of clinical remission by two-fold in patients with UC compared to controls. At 8 weeks, 37% (52/140) of FMT participants achieved remission compared to 18% (24/137) of control participants (RR 2.03, 95 % CI, 1.07 to 3.86; I² = 50%; low certainty evidence). One study reported data on relapse at 12 weeks among participants who achieved remission. None of the FMT participants (0/7) relapsed at 12 weeks compared to 20% of control participants (RR 0.28, 95% CI 0.02 to 4.98, 17 participants, very low certainty evidence). It is unclear whether there is a difference in serious adverse event rates between the intervention and control groups. Seven per cent (10/140) of FMT participants had a serious adverse event compared to 5% (7/137) of control participants (RR 1.40, 95% CI 0.55 to 3.58; 4 studies; I² = 0%; low certainty evidence). Serious adverse events included worsening of UC necessitating intravenous steroids or surgery; infection such as Clostridium difficile and cytomegalovirus, small bowel perforation and pneumonia. Adverse events were reported by two studies and the pooled data did not show any difference between the study groups. Seventy-eight per cent (50/64) of FMT participants had an adverse event compared to 75% (49/65) of control participants (RR 1.03, 95% CI 0.81 to 1.31; I² = 31%; moderate certainty evidence). Common adverse events included abdominal pain, nausea, flatulence, bloating, upper respiratory tract infection, headaches, dizziness, and fever. Four studies reported on clinical response at 8 weeks. Forty-nine per cent (68/140) of FMT participants had a clinical response compared to 28% (38/137) of control participants (RR 1.70, 95% CI 0.98 to 2.95, I² = 50%, low certainty evidence). Endoscopic remission at 8 weeks was reported by three studies and the combined results favored FMT over the control group. Thirty per cent (35/117) of FMT participants achieved endoscopic remission compared to 10% (11/112) of control participants (RR 2.96, 95 % CI 1.60 to 5.48, I² = 0%; low certainty evidence).

Authors' conclusions: Fecal microbiota transplantation may increase the proportion of participants achieving clinical remission in UC. However, the number of identified studies was small and the quality of evidence was low. There is uncertainty about the rate of serious adverse events. As a result, no solid conclusions can be drawn at this time. Additional high-quality studies are needed to further define the optimal parameters of FMT in terms of route, frequency, volume, preparation, type of donor and the type and disease severity. No studies assessed efficacy of FMT for induction of remission in CD or in pediatric participants. In addition, no studies assessed long-term maintenance of remission in UC or CD. Future studies are needed to address the therapeutic benefit of FMT in CD and the long-term FMT-mediated maintenance of remission in UC or CD.

PubMed Disclaimer

Conflict of interest statement

Aamer Imdad: None known

Maribeth R Nicholson: None known

Sari Acra: None known

Oscar Gomez‐Duarte: receives funding from the NIH for research on enteric pathogens. In addition to his employment at the University at Buffalo, he offers lectures at the University of Santander for which he receive honoraria. He is a member of the Revista Colombiana de Anestesiologia Editorial board which compensates him for time as an editor.

Emily E Tanner‐Smith: None known

Joseph P Zackular: None known

Dawn M Borromeo Beaulieu: a consultant for Abbvie, Takeda and Janssen

Figures

1
1
Study flow diagram
2
2
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
3
3
Forest plot of comparison: 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, outcome: 1.1 Clinical remission at 8 weeks.
4
4
Forest plot of comparison: 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, outcome: 1.8 Serious adverse events.
1.1
1.1. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 1 Clinical remission at 8 weeks.
1.2
1.2. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 2 Clinical remission at 12 Weeks.
1.3
1.3. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 3 Clinical remission at 8 weeks: Subgroup analysis by route of administration.
1.4
1.4. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 4 Clinical remission at 8 weeks: Subgroup analysis by type of donor.
1.5
1.5. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 5 Clinical remission at 8 weeks: Sensitivity analysis using fixed‐effect model.
1.6
1.6. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 6 Clinical remission: Composite of clinical score and endoscopic score.
1.7
1.7. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 7 Clinical relapse at 12 weeks.
1.8
1.8. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 8 Serious adverse events.
1.9
1.9. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 9 Serious adverse events: Subgroup analysis by route of administration.
1.10
1.10. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 10 Serious adverse events: Subgroup analysis by type of donor.
1.11
1.11. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 11 Serious adverse events: Sensitivity analysis using fixed‐effect model.
1.12
1.12. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 12 Any adverse events.
1.13
1.13. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 13 Clinical response at 8 weeks.
1.14
1.14. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 14 Clinical response at 12 weeks.
1.15
1.15. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 15 Endoscopic remission at 8 weeks.
1.16
1.16. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 16 Endoscopic remission at 12 weeks.
1.17
1.17. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 17 Endoscopic response at 8 weeks.
1.18
1.18. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 18 Endoscopic response at 12 weeks.
1.19
1.19. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 19 Withdrawals.
1.20
1.20. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 20 ESR at the longest follow up.
1.21
1.21. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 21 CRP at the longest follow‐up.
1.22
1.22. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 22 Fecal calprotectin at the longest follow‐up.
1.23
1.23. Analysis
Comparison 1 Fecal microbiota transplantation versus control for participants with ulcerative colitis, Outcome 23 Quality of life score: IBDQ.
See this image and copyright information in PMC

References

References to studies included in this review

Costello 2017a {published data only}
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References to studies excluded from this review

Angelberger 2016 {published data only}
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References to ongoing studies

NCT01790061 {published data only}
    1. NCT01790061. Standardized Fecal Microbiota Transplantation for Ulcerative Colitis [Efficacy, Durability and Safety of Standardized Fecal Microbiota Transplantation in Patients With Moderate to Severe Ulcerative Colitis]. clinicaltrials.gov/ct2/show/NCT01790061 (first received 13 February 2013).
NCT01793831 {published data only}
    1. NCT01793831. Standardized Fecal Microbiota Transplantation for Crohn's Disease [Efficacy and Safety of Standardized Fecal Microbiota Transplantation for Moderate to Severe Crohn's Disease]. clinicaltrials.gov/ct2/show/NCT01793831 (first received 18 February 2013).
NCT01961492 {published data only}
    1. NCT01961492. Fecal Microbiota Transplantation in Patients with Ulcerative Colitis [Single Fecal Microbiota Transplantation Via Colonoscope as an Adjunct Therapy in the Treatment of Ulcerative Colitis]. clinicaltrials.gov/ct2/show/NCT01961492 (first received 11 October 2013).
NCT02272868 {published data only}
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NCT02291523 {published data only}
    1. NCT02291523. The Effect of Therapeutic Fecal Transplant on the Gut Microbiome in Children with Ulcerative Colitis (FMT_UC) [The Effect of Therapeutic Fecal Transplant on the Gut Microbiome in Children With Ulcerative Colitis]. clinicaltrials.gov/ct2/show/NCT02291523 (first received 14 November 2014).
NCT02335281 {published data only}
    1. NCT02335281. Standardized Fecal Microbiota Transplantation for Inflammatory Bowel Disease (SFMT‐IBD) [Efficacy, Durability and Safety of Standardized Fecal Microbiota Transplantation for Severe Inflammatory Bowel Disease]. clinicaltrials.gov/ct2/show/NCT02335281 (first received 9 January 2015).
NCT02390726 {published data only}
    1. NCT02390726. Fecal Microbiota Transplant in the Treatment of Ulcerative Colitis (FMTUC) [Fecal Microbiota Transplant in the Treatment of Ulcerative Colitis]. clinicaltrials.gov/ct2/show/NCT02390726 (first received 17 March 2015).
NCT02487238 {published data only}
    1. NCT02487238. Pediatric FEcal Microbiota Transplant for Ulcerative Colitis (PediFETCh) [A Single‐Blind, Randomized, Placebo‐Controlled Trial of Human Fecal Microbiota Transplantation for the Therapy of Pediatric Ulcerative Colitis and Inflammatory Bowel Disease Unclassified]. clinicaltrials.gov/ct2/show/NCT02487238 (first received 1 July 2015).
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NCT02734589 {unpublished data only}
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NCT02998112 {published data only}
    1. NCT02998112. Fecal Microbiota Transplantation for Ulcerative Colitis Through Colonic Transendoscopic Enteral Tubing [Fecal Microbiota Transplantation for Ulcerative Colitis Through Colonic Transendoscopic Enteral Tubing]. clinicaltrials.gov/ct2/show/NCT02998112 (first received 20 December 2016).
NCT03006809 {published data only}
    1. NCT03006809. Optimal Fecal Microbiota Transplant Dosing for Mild to Moderate Ulcerative Colitis [Optimal Fecal Microbiota Transplant Dosing for Mild to Moderate Ulcerative Colitis]. clinicaltrials.gov/ct2/show/NCT03006809 (first received 30 December 2016).
NCT03016780 {unpublished data only}
    1. NCT03016780. Fecal Microbiota Transplantation for Ulcerative Colitis (FMTFUC) [Evaluation of The Effect of Fecal Microbiota Transplantation on Ulcerative Colitis and Its Mechanism]. clinicaltrials.gov/ct2/show/NCT03016780 (first received 11 January 2017).
NCT03104036 {published data only}
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