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      The kinetics of gut microbial community composition in patients with irritable bowel syndrome following fecal microbiota transplantation

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          Abstract

          Background

          Gut microbiota alterations are important in irritable bowel syndrome (IBS). The aim was to investigate the effect of fecal microbiota transplantation (FMT) on gut microbiota and the symptoms in patients with IBS.

          Material and methods

          The study included 13 IBS patients according to Rome III criteria and 13 healthy donors. Freshly donated feces were administered to the descending part of the duodenum via a gastroscope. Feces were collected from donors and patients before FMT, and from the patients at 1, 3 and 12 weeks and donors and patients at 20/28 weeks after FMT. Microbiota analysis was performed using GA-map Dysbiosis test (Genetic Analysis AS, Oslo, Norway). The patients completed the following questionnaires before and at the aforementioned weeks after FMT: IBS Symptom Questionnaire (IBS-SQ), IBS-Symptom Severity Scoring system (IBS-SSS), Short Form of Nepean Dyspepsia Index (SF-NDI), Bristol stool form scale, the Eysenck Personality Questionnaire-Neuroticism and Hospital Anxiety and Depression.

          Results

          Donors and IBS patients had significantly different bacterial strain signals before FMT ( Ruminococcus gnavus, Actinobacteria and Bifidobacteria) that became non-significant after 3 weeks following FMT. The changes in gut microbiota were similar between donors and patients at 20/28 weeks after FMT. Thus, patients’ microbiota profiles became more-or-less similar to donors.

          The scores of all the questionnaires were significantly improved at all time points following FMT. No reported adverse effects.

          Conclusions

          FMT was associated with a change in gut microbiota and improvement in IBS symptoms and quality of life lasting for up to 28 weeks.

          Trial registration

          ClinicalTrials.gov ID: NCT03333291

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          Most cited references38

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          The irritable bowel severity scoring system: a simple method of monitoring irritable bowel syndrome and its progress.

          C. FRANCIS, J. Morris, P J Whorwell (1997)
          The clinical assessment and investigation of irritable bowel syndrome would be greatly facilitated by the introduction of a simple, easy to use severity scoring system. Such a system, developed in our department over a number of years, has been submitted to validation in a total of 141 patients and 40 healthy controls. The system, incorporating pain, distension, bowel dysfunction and quality of life/global well-being, was assessed for its ability to reliably score patients previously classified as mild, moderate or severe. The reproducibility and sensitivity to change of the system was also assessed. The maximum achievable score was 500. Mild, moderate and severe cases were indicated by scores of 75 to 175, 175 to 300 and > 300 respectively. Controls scored below 75 and patients scoring in this range can be considered to be in remission. There was a highly significant difference between controls and patients as a whole (P = 0.0001) as well as significant differences (P < 0.01) between all severity categories. Scores repeated within 24 h were very reproducible and sensitivity to change was also extremely good (P < 0.001) with a change of 50 reliably indicating improvement. These results suggest that this scoring system should prove to be a valuable instrument in helping to meet the many challenges offered by irritable bowel syndrome.
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            Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection.

            Ethan Gough, Henna Shaikh, Amee R. Manges (2011)
            Clostridium difficile infection (CDI) is a gastrointestinal disease believed to be causally related to perturbations to the intestinal microbiota. When standard treatment has failed, intestinal microbiota transplantation (IMT) is an alternative therapy for patients with CDI. IMT involves infusing intestinal microorganisms (in a suspension of healthy donor stool) into the intestine of a sick patient to restore the microbiota. However, protocols and reported efficacy for IMT vary. We conducted a systematic literature review of IMT treatment for recurrent CDI and pseudomembranous colitis. In 317 patients treated across 27 case series and reports, IMT was highly effective, showing disease resolution in 92% of cases. Effectiveness varied by route of instillation, relationship to stool donor, volume of IMT given, and treatment before infusion. Death and adverse events were uncommon. These findings can guide physicians interested in implementing the procedure until better designed studies are conducted to confirm best practices.
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              Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection.

              Lawrence Brandt, Olga Aroniadis, Mark Mellow … (2012)
              Clostridium difficile infection (CDI) has increased to epidemic proportions over the past 15 years, and recurrence rates of 30-65% with failure to respond to multiple courses of antimicrobials are common. The aim of this study was to report the efficacy of fecal microbiota transplantation (FMT) in patients with recurrent CDI in five geographically disparate medical centers across the United States. A multicenter long-term follow-up study was performed on the use of FMT for recurrent CDI. We were able to contact 77 of 94 eligible patients who had colonoscopic FMT for recurrent CDI ≥ 3 months before. Respondents completed a 36-item questionnaire via mail and/or phone that solicited pre-FMT, post-FMT, and donor data. Study outcomes included primary cure rate (resolution of symptoms without recurrence within 90 days of FMT) and secondary cure rate (resolution of symptoms after one further course of vancomycin with or without repeat FMT). Seventy-three percent of patients were women and the average age was 65 years. The long-term follow-up period ranged from 3 to 68 months between FMT and data collection (mean: 17 months). The majority of patients were living independently at the time of FMT; however, 40% were ill enough to be hospitalized, homebound, or living in a skilled nursing facility. Spouses and partners accounted for 60% of donors and 27% were either first-degree relatives or otherwise related to the patient. The average symptom duration before FMT was 11 months and patients had failed an average of five conventional antimicrobial regimens; nonetheless, 74% of patients had resolution of their diarrhea in ≤ 3 days. Diarrhea resolved in 82% and improved in 17% of patients within an average of 5 days after FMT. The primary cure rate was 91%. Seven patients either failed to respond or experienced early CDI recurrence (≤ 90 days) after FMT. Four of these patients were successfully treated with vancomycin with or without probiotics; two patients were treated unsuccessfully with vancomycin, but subsequent FMT was successful; one patient was not treated and died in hospice care of unclear cause. The secondary cure rate was 98%. All late recurrences of CDI occurred in the setting of antimicrobial therapy for treatment of infections unrelated to C. difficile. In all, 53% of patients stated they would have FMT as their preferred first treatment option if CDI were to recur. While no definite adverse effects of FMT were noted, two patients had improvement in a pre-existing medical condition and four patients developed diseases of potential interest after FMT. FMT is a rational, durable, safe, and acceptable treatment option for patients with recurrent CDI.
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                Author and article information

                Contributors
                Tarek Mazzawi:
                ORCID: http://orcid.org/0000-0001-7983-3707
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Gülen Arslan Lied: Role: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: Writing – review & editing
                Dag André Sangnes: Role: MethodologyRole: Project administrationRole: Writing – review & editing
                Magdy El-Salhy: Role: Project administrationRole: SupervisionRole: Writing – review & editing
                Johannes R. Hov: Role: Data curationRole: Funding acquisitionRole: Writing – review & editing
                Odd Helge Gilja: Role: Project administrationRole: SupervisionRole: Writing – review & editing
                Jan Gunnar Hatlebakk: Role: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Trygve Hausken: Role: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                John Green: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 14 November 2018
                Publication date Collection: 2018
                Volume: 13
                Issue: 11
                Electronic Location Identifier: e0194904
                Affiliations
                [1 ] Section of Gastroenterology, Department of Medicine, Haukeland University Hospital, Bergen, Norway
                [2 ] Norwegian Competence Centre for Functional Gastro-Intestinal Disorders, Section of Gastroenterology, Department of Medicine, Haukeland University Hospital, Bergen, Norway
                [3 ] Center for Nutrition, Department of Clinical Medicine, University of Bergen, Bergen, Norway
                [4 ] Section of Gastroenterology, Department of Medicine, Stord Hospital, Helse-Fonna, Stord, Norway
                [5 ] Norwegian PSC Research Center, Section of Gastroenterology and Research Institute of Internal Medicine, Division of Surgery, Inflammatory Diseases and Transplantation, Oslo University Hospital and University of Oslo, Oslo, Norway
                University Hospital Llandough, UNITED KINGDOM
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-7983-3707
                Article
                Publisher ID: PONE-D-17-36974
                DOI: 10.1371/journal.pone.0194904
                PMC ID: 6235238
                PubMed ID: 30427836
                SO-VID: 9ed0ea98-5404-4755-b107-391692e7256f
                Copyright © © 2018 Mazzawi et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 4 November 2017
                Date accepted : 28 September 2018
                Page count
                Figures: 5, Tables: 4, Pages: 17
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100005029, Helse Vest Regionalt Helseføretak;
                Award ID: 911802
                Award Recipient :
                Funded by: Norwegian Research Council
                Award ID: 240787/F20
                Award Recipient :
                The study was supported by Western Norway Regional Health Authority (grant no. 911802), www.helse-vest.no. Johannes R. Hov was funded by the Norwegian Research Council (240787/F20), www.forskningsradet.no.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Gut Bacteria
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Irritable Bowel Syndrome
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Irritable Bowel Syndrome
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbiome
                Subject: Biology and Life Sciences
                Subject: Genetics
                Subject: Genomics
                Subject: Microbial Genomics
                Subject: Microbiome
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Microbial Genomics
                Subject: Microbiome
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Gut Bacteria
                Subject: Bifidobacterium
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Research and Analysis Methods
                Subject: Research Design
                Subject: Survey Research
                Subject: Questionnaires
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Actinobacteria
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Custom metadata
                Data Availability All relevant data are within the paper.

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