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GutCoidenfThe use of faecal microbiota transplant as treatment forrecurrent or refractory Clostridium difficile infection andother potential indications: joint British Society ofGastroenterology (BSG) and Healthcare Infection Society(HIS) guidelines.GutntJournal:Manuscript IDDate Submitted by the Author:Guidelines27-Jun-2018:FComplete List of Authors:ialArticle Type:gutjnl-2018-316818.R2orMullish, Benjamin; Imperial College London, Division of IntegrativeSystems Medicine and Digestive Disease, Department of Surgery andCancer; Imperial College Healthcare NHS Trust, Department ofGastroenterology and Hepatology, St Mary's HospitalQuraishi, Mohammed; Queen Elizabeth Hospital Birmingham, Departmentof GastroenterologySegal, Jonathan; Imperial College London, Division of Digestive Diseases/Liver Unit; Imperial College Faculty of Medicine - Northwick Park and SaintMarks Campus, Inflammatory Bowel Disease UnitMcCune, Victoria; Public Health Laboratory Birmingham, Public HealthEngland; University of Birmingham, Institute of Microbiology and InfectionBaxter, Melissa; Royal Devon and Exeter NHS Foundation Trust,Department of MicrobiologyMarsden, Gemma; Healthcare Infection SocietyMoore, David; University of Birmingham, School of Health and PopulationSciencesColville, Alaric ; Royal Devon and Exeter NHS Foundation Trust,Department of MicrobiologyBhala, Neeraj; University Hospital Birmingham NHS Foundation Trust,Gastroenterology; University of Birmingham, Institute of TranslationalMedicineIqbal, Tariq; University Hospital Birmingham NHS Trust, Gastroenterology;University of Birmingham, Institute of Translational MedicineSettle, Christopher; City Hospitals Sunderland NHS Foundation Trust,Department of MicrobiologyKontkowski, Graziella; C diff SupportHart, Ailsa; Imperial College Faculty of Medicine - Northwick Park and SaintMarks Campus, Inflammatory Bowel Disease Unit; Imperial CollegeLondon, Division of Integrative Systems Medicine and Digestive Disease,Department of Surgery and CancerHawkey, Peter; University of Birmingham, Institute of Microbiology andInfectionGoldenberg, Simon; King's College London, Centre for Clinical Infection andDiagnostics Research; Guy's and St Thomas' NHS Foundation ut
Page 1 of 454Department of MicrobiologyWilliams, Horace; Imperial College London, Division of Integrative SystemsMedicine and Digestive Disease, Department of Surgery and Cancer;Imperial College Healthcare NHS Trust, Department of Gastroenterologyand Hepatology, St Mary's HospitalKeywords:ENTERIC BACTERIAL MICROFLORA, INTESTINAL MICROBIOLOGY,COLONIC MICROFLORA, INFECTIVE COLITIS, INFLAMMATORY uthttps://mc.manuscriptcentral.com/gut
Gutor:FialntidenfCowvieReOnFigure 1: Proposed summary pathway for donor screening for centres preparing frozen FMT from recurringdonors.60x88mm (300 x 300 960Page 2 of 454
Page 3 of 454GutHIS/ BSG FMT Guideline: Main Document, Gut version.1The use of faecal microbiota transplant as treatment for recurrent or refractory2Clostridium difficile infection and other potential indications: joint British Society of3Gastroenterology (BSG) and Healthcare Infection Society (HIS) guidelines.45Benjamin H Mullish*1,2, Mohammed Nabil Quraishi*3, Jonathan Segal*1,4, Victoria L6McCune5,6, Melissa Baxter7, Gemma L Marsden8, David Moore9, Alaric Colville7, Neeraj7Bhala3,9,10, Tariq H Iqbal3,10, Christopher Settle11, Graziella Kontkowski12, Ailsa L Hart1,4, Peter8M Hawkey6, Simon D Goldenberg 13,14, Horace RT Williams 1,2.idenfCo9101. Division of Integrative Systems Medicine and Digestive Disease, Department of Surgery andnt1112Cancer, Faculty of Medicine, Imperial College London, London, UK.2. Departments of Gastroenterology and Hepatology, St Mary’s Hospital, Imperial Collegeial1314Healthcare NHS Trust, Paddington, London, UK.:F3. Department of Gastroenterology, Queen Elizabeth Hospital Birmingham, University Hospitals15Birmingham NHS Foundation Trust, Birmingham, UK.or164. Inflammatory Bowel Disease Unit, St Mark's Hospital, Harrow, London, UK.175. Public Health England, Public Health Laboratory Birmingham, Birmingham, UK.186. Institute of Microbiology and Infection, University of Birmingham, Birmingham, UK.197. Department of Microbiology, Royal Devon and Exeter NHS Foundation Trust, Exeter, UK.208. Healthcare Infection Society, London, UK.219. Institute of Applied Health Research, University of Birmingham, Birmingham, UK.2210. Institute of Translational Medicine, University of Birmingham, Edgbaston, Birmingham, UK.2311. Department of Microbiology, City Hospitals Sunderland NHS Foundation Trust, Sunderland, UK.2412. C diff Support, UK.2513. Centre for Clinical Infection and Diagnostics Research, King's College London, London, UK.2614. Department of Microbiology, Guy's and St Thomas' NHS Foundation Trust, London 4950515253545556575859602728*Joint first authors.29 30 Joint senior authors.Corresponding author.311https://mc.manuscriptcentral.com/gut
GutPage 4 of 454HIS/ BSG FMT Guideline: Main Document, Gut version.32Contact via:Dr Horace Williams33Department of Gastroenterology343rd Floor, Salton House35St Mary’s Hospital, Imperial College Healthcare NHS Trust3638London, W2 1NYUnited Kingdomnf37CoEmail: h.williams@imperial.ac.uk39Keywords:microbiota; faecal transplant; Clostridium difficile; inflammatory bowel disease4142Word count:16301Abbreviations: FMTfaecal microbiota transplantor44:F43ialnt40ide45CDIClostridium difficile infection46EBVEpstein-Barr virus47CMVcytomegalovirus48BMIbody mass index49GIgastrointestinal50RCTrandomised controlled trial51NAAT nucleic acid amplification test52GDHglutamate dehydrogenase53EIAenzymes immunoassay54PCRpolymerase chain reaction55IBDinflammatory bowel disease56IBSirritable bowel 5354555657585960
Page 5 of 454GutHIS/ BSG FMT Guideline: Main Document, Gut version.57HIVhuman immunodeficiency virus58AIDSacquired immune deficiency syndrome59CPEcarbapenemase-producing Enterobacteriaceae60ESBLextended-spectrum beta-lactamase62Co63PPI61667073MELD Model for End-Stage Liver Diseasew74hepatic encephalopathyvie72HERe71ulcerative colitisor69UC:F68proton pump inhibitorial67MRSA methicillin-resistant Staphylococcus aureusnt65vancomycin-resistant 3https://mc.manuscriptcentral.com/gut
GutPage 6 of 454HIS/ BSG FMT Guideline: Main Document, Gut version.821. Abstract:83Interest in the therapeutic potential of faecal microbiota transplant (FMT) has been increasing84globally in recent years, particularly as a result of randomised studies in which it has been used as an85intervention. The main focus of these studies has been the treatment of recurrent or refractory86Clostridium difficile infection (CDI), but there is also an emerging evidence base regarding potential87applications in non-CDI settings. The key clinical stakeholders for the provision and governance of88FMT services in the United Kingdom (UK) have tended to be in two major specialty areas:89gastroenterology and microbiology/infectious diseases. Whilst the National Institute for Health and90Care Excellence (NICE) guidance (2014) for use of FMT for recurrent or refractory CDI has become91accepted in the UK, clear evidence-based UK guidelines for FMT have been lacking. This resulted in92discussions between the British Society of Gastroenterology (BSG) and Healthcare Infection Society93(HIS), and a joint BSG/HIS FMT working group was established. This guideline document is the94culmination of that joint dialogue.95ialntidenfCo962. Executive summary:972.1.98The remit of the British Society of Gastroenterology (BSG)/ Healthcare Infection Society (HIS)99working group was to provide recommendations as to best practice in the provision of a faecal100microbiota transplant (FMT) service. This guideline considers the use of FMT for the treatment of101Clostridium difficile infection (CDI) – as well as for potential non-CDI indications – in adults. The102working group have primarily targeted their report at clinicians involved in the use and provision of103FMT services, but have also aimed it to be of interest to patients and their relatives.Overview:or:FwvieRe1041052.2.Summary of recommendations:1062.2.1. Which patients with Clostridium difficile infection should be considered for faecal107microbiota transplant, and how should they be followed up after treatment?Prior to faecal microbiota transplant. Patient 84950515253545556575859601082.2.1.1.1092.2.1.1.1. Recurrent Clostridium difficile infection:110We recommend that FMT should be offered to patients with recurrent CDI who have had at111least two recurrences, or those who have had one recurrence and have risk factors for112further episodes, including severe and severe-complicated CDI (GRADE of evidence: high;113strength of recommendation: strong).4https://mc.manuscriptcentral.com/gut
Page 7 of 454GutHIS/ BSG FMT Guideline: Main Document, Gut version.1141152.2.1.1.2. Refractory Clostridium difficile infection:116We recommend that FMT should be considered in cases of refractory CDI (GRADE of117evidence: moderate; strength of recommendation: strong).118Co1192.2.1.1.3. FMT as initial therapy for Clostridium difficile infection:120We recommend that FMT should not be administered as initial treatment for CDI (GRADE of121evidence: low; strength of recommendation: strong).idenf122nt1232.2.1.1.4. Antimicrobial/ antitoxin therapy prior to considering FMT for patients with CDI:124i.We recommend that FMT for recurrent CDI should only be considered afterial125recurrence of symptoms following resolution of an episode of CDI that was treated126with appropriate antimicrobials for at least 10 days (GRADE of evidence: low;127strength of recommendation: strong).ii.or128:FWe recommend consideration of treatment with extended/ pulsed vancomycin129and/or fidaxomicin before considering FMT as treatment for recurrent CDI (GRADE130of evidence: low; strength of recommendation: strong).131iii.ReFor those with severe or complicated CDI, which appears to be associated withvie132reduced cure rates, we recommend that consideration should be given to offering133patients treatment with medications which are associated with reduced risk of134recurrence (e.g. fidaxomicin and bezlotoxumab), before offering FMT (GRADE of135evidence: low; strength of recommendation: strong).w1361372.2.1.2.1382.2.1.2.1. Management of FMT failure:139We recommend that FMT should be offered after initial FMT failure (GRADE of evidence:140high; strength of recommendation: strong).1411422.2.1.2.2. General approach to follow-up st-FMT follow-up, outcomes and adverse 51525354555657585960
GutPage 8 of 454HIS/ BSG FMT Guideline: Main Document, Gut version.143We recommend that all FMT recipients should routinely receive follow-up. Clinicians should144follow-up FMT recipients for long enough to fully establish efficacy/adverse events, and for145at least eight weeks in total (GRADE of evidence: low; strength of recommendation: strong).146Co1472.2.1.2.3. Management of the FMT recipient:148i.We recommend that immediate management after endoscopic administration ofnf149FMT should be as per endoscopy unit protocol (GRADE of evidence: very low:150strength of recommendation: strong).151ii.ideWe recommend that patients should be warned about short term adverse events, in152particular the possibility of self-limiting GI symptoms. They should be advised that153serious adverse events are rare (GRADE of evidence: very low; strength of154recommendation: strong).iii.ial155ntAfter enteral tube administration, we recommend that patients may have the tube156removed and oral water given from 30 minutes post-administration (GRADE of157evidence: very low; strength of recommendation: strong).or:F1581592.2.1.2.4. Definition of cure post-FMT for CDI:160We recommend that a decision regarding cure/remission from CDI should be recorded161during follow-up. However, this has no uniformly-agreed definition, and should be decided162on a case-by-case basis (GRADE of evidence: very low; strength of recommendation: strong).163wvieRe1642.2.1.2.5. Definition of treatment failure post-FMT for CDI:165We recommend that treatment failure/recurrence should be defined on a case-by-case166basis.167appropriate to consider in the case of persistent CDI symptoms/suspected relapse (GRADE168of evidence: low; strength of recommendation: strong).OnRoutine testing for C. difficile toxin after FMT is not recommended, but it 3545556575859601691701711722.2.2. What recipient factors influence the outcome of faecal microbiota transplant whentreating people with Clostridium difficile infection?2.2.2.1.General approach to co-morbidities and FMT:6https://mc.manuscriptcentral.com/gut
Page 9 of 454GutHIS/ BSG FMT Guideline: Main Document, Gut version.173i.(GRADE of evidence: very low; strength of recommendation: strong).174175We recommend that FMT should be avoided in those with anaphylactic food allergyii.We suggest that FMT should be offered with caution to patients with CDI and176decompensated chronic liver disease (GRADE of evidence: very low; strength of177recommendation: weak).178Co1792.2.2.2.180i.Immunosuppression and FMT:nfWe recommend that FMT should be offered with caution to immunosuppressed181patients, in whom FMT appears efficacious without significant additional adverse182effects (GRADE of evidence: moderate; strength of recommendation: strong).183ii.ideWe recommend that immunosuppressed FMT recipients at risk of severe infection ifnt184exposed to EBV or CMV should only receive FMT from donors negative for EBV and185CMV (GRADE of evidence: very low; strength of recommendation: strong).1861872.2.2.3.188i.:FialOther comorbidities and FMT:We recommend that FMT should be offered to those with recurrent CDI andor189inflammatory bowel disease, but patients should be counselled about a small but190recognised risk of exacerbation of IBD (GRADE of evidence: moderate; strength of191recommendation: strong).ii.We recommend that FMT should be considered for appropriate patients withvie192Re193recurrent CDI regardless of other comorbidities (GRADE of evidence: moderate;194strength of recommendation: strong).1951972.2.3. What donor factors influence the outcome of faecal microbiota transplant whentreating people with Clostridium difficile infection?1982.2.3.1.199We recommend that related or unrelated donors should both be considered acceptable.200However, where possible, FMT is best sourced from a centralised stool bank, from a healthy201unrelated donor (GRADE of evidence: low; strength of recommendation: strong).2022032.2.3.2.Age and BMI restrictions for potential ral approach to donor 748495051525354555657585960
GutPage 10 of 454HIS/ BSG FMT Guideline: Main Document, Gut version.204We suggest that people should only be considered as potential FMT donors if they are 18205and 60 years old, and have a BMI of 18 and 30 kg/m2 (GRADE of evidence: low; strength206of recommendation: weak).207Co2082.2.3.3.General approach to the donor screening assessment:209It is mandatory to screen potential donors by questionnaire and personal interview, to210establish risk factors for transmissible diseases and factors influencing the gut microbiota211(Table 1) (GRADE of evidence: low; strength of recommendation: strong).212idenf2132.2.3.4.Laboratory screening of potential donors:214Blood and stool screening of donors is mandatory (Tables 2 and 3) (GRADE of evidence: low;215strength of recommendation: strong).ialnt2162.2.3.5.218i.Repeat donor checks, and donation pathway:or217:FIn centres using frozen FMT, before FMT may be used clinically, we recommend that219donors should have successfully completed a donor health questionnaire and laboratory220screening assays both before and after the period of stool donation.221preferred means of donor screening (GRADE of evidence: low; strength of222recommendation: strong).This is thevieRe223ii. In centres using fresh FMT, we recommend that a repeat health questionnaire should be224assessed at the time of each stool donation. To ensure ongoing suitability for inclusion225as a donor, the donor health questionnaire and laboratory screening should be repeated226regularly (GRADE of evidence: low; strength of recommendation: 7484950515253545556575859602282.2.4. What factors related to the preparation of the transplant influence the outcome of229faecal microbiota transplant when treating people with Clostridium difficile230infection?2312.2.4.1.General principles of FMT preparation:8https://mc.manuscriptcentral.com/gut
Page 11 of 454GutHIS/ BSG FMT Guideline: Main Document, Gut version.232i.evidence: low; strength of recommendation: strong).233234ii.237238iii.We recommend that both aerobically and anaerobically prepared FMT treatmentsshould be considered suitable when preparing FMT for the treatment of recurrentCDI (GRADE of evidence: moderate; strength of recommendation: strong).iv.nf239We recommend that donor stool should be processed within 6 hours of defaecation(GRADE of evidence: low; strength of recommendation: strong).235236We recommend that stool collection should follow a standard protocol (GRADE ofCoWe recommend that sterile 0.9% saline should be considered as an appropriate240diluent for FMT production, and cryoprotectant such as glycerol should be added for241frozen FMT (GRADE of evidence: moderate: strength of recommendation: strong).242v.ntWe suggest that stool should be mixed 1:5 with diluent to make the initial faecalialvi.emulsion (GRADE of evidence: low; strength of recommendation: weak).245vii.:F246We recommend using 50g of stool in each FMT preparation (GRADE of evidence:moderate: strength of recommendation: strong).243244ideWe suggest that homogenisation and filtration of FMT should be undertaken in a247closed disposable system (GRADE of evidence: low; strength of recommendation:248weak).or249Fresh vs frozen FMT:Re2502.2.4.2.251We recommend that the use of banked frozen FMT material should be considered252preferable to fresh preparations for CDI (GRADE of evidence: high; strength of253recommendation: strong).wvie2542552.2.4.3.256i.Use of frozen FMT:OnWe recommend that FMT material stored frozen at -80oC should be regarded as having 54555657585960257maximum shelf life of six months from preparation (GRADE of evidence: low; strength of258recommendation: strong).259ii. We suggest consideration of thawing frozen FMT at ambient temperature, and using260within six hours of thawing (GRADE of evidence: low; strength of ral.com/gut
GutPage 12 of 454HIS/ BSG FMT Guideline: Mai
40 Keywords: microbiota; faecal transplant; Clostridium difficile; inflammatory bowel disease 41 42 Word count: 16301 43 44 Abbreviations: FMT faecal microbiota transplant 45 CDI Clostridium difficile infection
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