3,868
Views
11
CrossRef citations to date
0
Altmetric
Original Article

Danish national guideline for the treatment of Clostridioides difficile infection and use of faecal microbiota transplantation (FMT)

ORCID Icon, , , , , , , ORCID Icon, , ORCID Icon, & ORCID Icon show all
Pages 1056-1077 | Received 03 Mar 2021, Accepted 20 Apr 2021, Published online: 14 Jul 2021

References

  • Leffler DA, Lamont JT. Clostridium difficile infection. N Engl J Med. 2015;372(16):1539–1548.
  • Redelings MD, Sorvillo F, Mascola L. Increase in Clostridium difficile-related mortality rates, United States, 1999–2004. Emerg Infect Dis. 2007;13(9):1417–1419.
  • Le Monnier A, , Duburcq A, Zahar JR, GMC Study Group, et al. Hospital cost of Clostridium difficile infection including the contribution of recurrences in French acute-care hospitals. J Hosp Infect. 2015;91(2):117–122.
  • Magee G, Strauss ME, Thomas SM, et al. Impact of Clostridium difficile-associated diarrhea on acute care length of stay, hospital costs, and readmission: a multicenter retrospective study of inpatients, 2009-2011. Am J Infect Control. 2015;43(11):1148–1153.
  • Zhang S, Palazuelos-Munoz S, Balsells EM, et al. Cost of hospital management of Clostridium difficile infection in United States-a meta-analysis and modelling study. BMC Infect Dis. 2016;16(1):447.
  • Allegretti JR, Mullish BH, Kelly C, et al. The evolution of the use of faecal microbiota transplantation and emerging therapeutic indications. Lancet. 2019;394(10196):420–431.
  • Eiseman B, Silen W, Bascom GS, et al. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44(5):854–859.
  • Garborg K, Waagsbo B, Stallemo A, et al. Results of faecal donor instillation therapy for recurrent Clostridium difficile-associated diarrhoea. Scand J Infect Dis. 2010;42(11–12):857–861.
  • 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(7):1079–1087.
  • 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(2):145–149.
  • Mattila E, Uusitalo-Seppala R, Wuorela M, et al. Fecal transplantation, through colonoscopy, is effective therapy for recurrent Clostridium difficile infection. Gastroenterology. 2012;142(3):490–496.
  • Rubin TA, Gessert CE, Aas J, et al. Fecal microbiome transplantation for recurrent Clostridium difficile infection: report on a case series. Anaerobe. 2013;19:22–26.
  • 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(11):1515–1522.
  • van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–415.
  • 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(9):835–843.
  • 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(9):609–616.
  • 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 Pharmacol Ther. 2017;45(7):899–908.
  • 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(2):142–149.
  • Hvas CL, Jørgensen SMD, Jørgensen SP, et al. Fecal microbiota transplantation is superior to fidaxomicin for treatment of recurrent Clostridium difficile infection. Gastroenterology. 2019;156(5):1324–1332.
  • Teasley DG, Gerding DN, Olson MM, et al. Prospective randomised trial of metronidazole versus vancomycin for Clostridium-difficile-associated diarrhoea and colitis. Lancet. 1983;2(8358):1043–1046.
  • Wenisch C, Parschalk B, Hasenhundl M, et al. Comparison of vancomycin, teicoplanin, metronidazole, and fusidic acid for the treatment of Clostridium difficile-associated diarrhea. Clin Infect Dis. 1996;22(5):813–818.
  • Fekety R. Guidelines for the diagnosis and management of Clostridium difficile-associated diarrhea and colitis. American College of Gastroenterology, Practice Parameters Committee. Am J Gastroenterol. 1997;92(5):739–750.
  • Zar FA, Bakkanagari SR, Moorthi KM, et al. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis. 2007;45(3):302–307.
  • Johnson S, Louie TJ, Gerding DN, for the Polymer Alternative for CDI Treatment (PACT) investigators, et al. Vancomycin, metronidazole, or tolevamer for Clostridium difficile infection: results from two multinational, randomized, controlled trials. Clin Infect Dis. 2014;59(3):345–354.
  • Stevens VW, Nelson RE, Schwab-Daugherty EM, et al. Comparative effectiveness of vancomycin and metronidazole for the prevention of recurrence and death in patients with Clostridium difficile infection. JAMA Intern Med. 2017;177(4):546–553.
  • Fekety R, Silva J, Kauffman C, et al. Treatment of antibiotic-associated Clostridium difficile colitis with oral vancomycin: comparison of two dosage regimens. Am J Med. 1989;86(1):15–19.
  • Lam SW, Bass SN, Neuner EA, et al. Effect of vancomycin dose on treatment outcomes in severe Clostridium difficile infection. Int J Antimicrob Agents. 2013;42(6):553–558.
  • Rokas KE, Johnson JW, Beardsley JR, et al. The addition of intravenous metronidazole to oral vancomycin is associated with improved mortality in critically ill patients with Clostridium difficile infection. Clin Infect Dis. 2015;61(6):934–941.
  • Wang Y, Schluger A, Li J, et al. Does addition of intravenous metronidazole to oral vancomycin improve outcomes in Clostridioides difficile infection? Clin Infect Dis. 2020;71(9):2414–2420.
  • 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(5):440–447.
  • Cornely OA, Crook DW, Esposito R, OPT-80-004 Clinical Study Group, et al. Fidaxomicin versus vancomycin for infection with Clostridium difficile in Europe, Canada, and the USA: a double-blind, non-inferiority, randomised controlled trial. Lancet Infect Dis. 2012;12(4):281–289.
  • Guery B, Menichetti F, Anttila VJ, et al. Extended-pulsed fidaxomicin versus vancomycin for Clostridium difficile infection in patients 60 years and older (EXTEND): a randomised, controlled, open-label, phase 3b/4 trial. Lancet Infect Dis. 2018;18(3):296–307.
  • Sirbu BD, Soriano MM, Manzo C, Lum J, et al. Vancomycin taper and pulse regimen with careful follow-up for patients Wwth recurrent Clostridium difficile infection. Clin Infect Dis. 2017;65(8):1396–1399.
  • Tedesco FJ, Gordon D, Fortson WC. Approach to patients with multiple relapses of antibiotic-associated pseudomembranous colitis. Am J Gastroenterol. 1985;80(11):867–868.
  • Gentry CA, Giancola SE, Thind S, et al. 2nd: A propensity-matched analysis between standard versus tapered oral vancomycin courses for themanagement of recurrent Clostridium difficile infection. Open Forum Infect Dis. 2017;4:ofx235.
  • Murphy MM, Patatanian E, Gales MA. Extended duration vancomycin in recurrent Clostridium difficile infection: a systematic review. Ther Adv Infect Dis. 2018;5(6):111–119.
  • Okumura H, Fukushima A, Taieb V, et al. Fidaxomicin compared with vancomycin and metronidazole for the treatment of Clostridioides (Clostridium) difficile infection: a network meta-analysis. J Infect Chemother. 2020;26(1):43–50.
  • Debast SB, Bauer MP, Kuijper EJ. European Society of Clinical Microbiology and Infectious Diseases: update of the treatment guidance document for Clostridium difficile infection. Clin Microbiol Infect. 2014;20(2):1–26.
  • Nelson RL, Suda KJ, Evans CT. Antibiotic treatment for Clostridium difficile-associated diarrhoea in adults. Cochrane Database Syst Rev. 2017;3:CD004610.
  • McDonald LC, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis. 2018;66(7):987–994.
  • Guery B, Galperine T, Barbut F. Clostridioides difficile: diagnosis and treatments. BMJ. 2019;366:l4609.
  • Cheng YW, Fischer M. Clinical management of severe, fulminant, and refractory Clostridioides difficile infection. Expert Rev anti Infect Ther. 2020;18(4):323–333.
  • Musher DM, Logan N, Bressler AM, et al. Nitazoxanide versus vancomycin in Clostridium difficile infection: a randomized, double-blind study. Clin Infect Dis. 2009;48(4):e41-6–e46.
  • Boero M, Berti E, Morgando A, et al. Treatement of pseudomembranous colitis: a randomized controlled trial with rifaximine vs. vancomycin. Microbiologia Medica. 1990;5:74–77.
  • Ng QX, Loke W, Foo NX, et al. A systematic review of the use of rifaximin for Clostridium difficile infections. Anaerobe. 2019;55:35–39.
  • de Lalla F, Nicolin R, Rinaldi E, et al. Prospective study of oral teicoplanin versus oral vancomycin for therapy of pseudomembranous colitis and Clostridium difficile-associated diarrhea. Antimicrob Agents Chemother. 1992;36(10):2192–2196.
  • Popovic N, Korac M, Nesic Z, et al. Oral teicoplanin versus oral vancomycin for the treatment of severe Clostridium difficile infection: a prospective observational study. Eur J Clin Microbiol Infect Dis. 2018;37(4):745–754.
  • Wilcox MH, Gerding DN, Poxton IR, et al. Bezlotoxumab for prevention of recurrent Clostridium difficile infection. N Engl J Med. 2017;376(4):305–317.
  • Carignan A, Poulin S, Martin P, et al. Efficacy of secondary prophylaxis with vancomycin for preventing recurrent Clostridium difficile infections. Am J Gastroenterol. 2016;111(12):1834–1840.
  • Van Hise NW, Bryant AM, Hennessey EK, et al. Efficacy of oral vancomycin in preventing recurrent Clostridium difficile infection in patients treated with systemic antimicrobial agents. Clin Infect Dis. 2016;63(5):651–653.
  • Brown CC, Manis MM, Bohm NM, et al. Oral vancomycin for secondary prophylaxis of Clostridium difficile infection. Ann Pharmacother. 2019;53(4):396–401.
  • Zhang K, Beckett P, Abouanaser S, et al. Prolonged oral vancomycin for secondary prophylaxis of relapsing Clostridium difficile infection. BMC Infect Dis. 2019;19(1):51.
  • Hota SS, Sales V, Tomlinson G, Salpeter MJ, 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(3):265–271.
  • Rode AA, Chehri M, Krogsgaard L, et al. Cure of recurrent Clostridium difficile infection with a mix of 12 gut bacteria, faecal microbiota transplantation or oral vancomycin: results from an open-label multicentre randomised controlled trial. Aliment Pharmacol Ther. 2021;53(9):999–1009.
  • Juul FE, Garborg K, Bretthauer M, et al. Fecal microbiota transplantation for primary Clostridium difficileinfection. N Engl J Med. 2018;378(26):2535–2536.
  • Camacho-Ortiz A, Gutierrez-Delgado EM, Garcia-Mazcorro JF, et al. Randomized clinical trial to evaluate the effect of fecal microbiota transplant for initial Clostridium difficile infection in intestinal microbiome. PLOS One. 2017;12(12):e0189768.
  • Fischer M, Sipe B, Cheng YW, et al. Fecal microbiota transplant in severe and severe-complicated Clostridium difficile: a promising treatment approach. Gut Microbes. 2017;8(3):289–302.
  • Hocquart M, Lagier JC, Cassir N, et al. Early fecal microbiota transplantation improves survival in severe Clostridium difficile infections. Clin Infect Dis. 2018;66(5):645–650.
  • Tixier EN, Verheyen E, Ungaro RC, et al. Faecal microbiota transplant decreases mortality in severe and fulminant Clostridioides difficile infection in critically ill patients. Aliment Pharmacol Ther. 2019;50(10):1094–1099.
  • Cheng YW, Phelps E, Nemes S, et al. Fecal microbiota transplant decreases mortality in patients with refractory severe or fulminant Clostridioides difficile infection. Clin Gastroenterol Hepatol. 2020;18(10):2234–2243.
  • Petrof EO, Gloor GB, Vanner SJ, et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome. 2013;1(1):3.
  • Tvede M, Rask-Madsen J. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet. 1989;1(8648):1156–1160.
  • Tvede M, Tinggaard M, Helms M. Rectal bacteriotherapy for recurrent Clostridium difficile-associated diarrhoea: results from a case series of 55 patients in Denmark 2000–2012. Clin Microbiol Infect. 2015;21(1):48–53.
  • Bhangu S, Bhangu A, Nightingale P, et al. Mortality and risk stratification in patients with Clostridium difficile-associated diarrhoea. Colorectal Dis. 2010;12(3):241–246.
  • Lamontagne F, Labbe AC, Haeck O, et al. Impact of emergency colectomy on survival of patients with fulminant Clostridium difficile colitis during an epidemic caused by a hypervirulent strain. Ann Surg. 2007;245(2):267–272.
  • Neal MD, Alverdy JC, Hall DE, et al. Diverting loop ileostomy and colonic lavage: an alternative to total abdominal colectomy for the treatment of severe, complicated Clostridium difficile associated disease. Ann Surg. 2011;254(3):423–427.
  • Ferrada P, Callcut R, Zielinski MD, EAST Multi-Institutional Trials Committee, et al. Loop ileostomy versus total colectomy as surgical treatment for Clostridium difficile-associated disease: an Eastern Association for the surgery of trauma multicenter trial. J Trauma Acute Care Surg. 2017;83(1):36–40.
  • Kulaylat AS, Kassam Z, Hollenbeak CS, et al. Surgical Clostridium-associated risk of death score predicts mortality after colectomy for Clostridium difficile. Dis Colon Rectum. 2017;60(12):1285–1290.
  • McKechnie T, Lee Y, Springer JE, et al. Diverting loop ileostomy with colonic lavage as an alternative to colectomy for fulminant Clostridioides difficile: a systematic review and meta-analysis. Int J Colorectal Dis. 2020;35(1):1–8.
  • Vely A, Ferrada P. Role of surgery in Clostridium difficile infection. Clin Colon Rectal Surg. 2020;33(2):87–91.
  • Juo YY, Sanaiha Y, Jabaji Z, et al. Trends in diverting loop ileostomy vs total abdominal colectomy as surgical management for Clostridium difficile colitis. JAMA Surg. 2019;154(10):899–906.
  • Bowman JA, Utter GH. Evolving strategies to manage Clostridium difficile colitis. J Gastrointest Surg. 2020;24(2):484–491.
  • Green DA, Stotler B, Jackman D, et al. Clinical characteristics of patients who test positive for Clostridium difficile by repeat PCR. J Clin Microbiol. 2014;52(11):3853–3855.
  • Sunkesula VC, Kundrapu S, Muganda C, et al. Does empirical Clostridium difficile infection (CDI) therapy result in false-negative CDI diagnostic test results? Clin Infect Dis. 2013;57(4):494–500.
  • Aichinger E, Schleck CD, Harmsen WS, et al. Nonutility of repeat laboratory testing for detection of Clostridium difficile by use of PCR or enzyme immunoassay. J Clin Microbiol. 2008;46(11):3795–3797.
  • 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(6):576–582.
  • Svendsen AT, Bytzer P, Engsbro AL. Systematic review with meta-analyses: does the pathogen matter in post-infectious irritable bowel syndrome? Scand J Gastroenterol. 2019;54(5):546–562.
  • Costello SP, Hughes PA, Waters O, et al. Effect of fecal microbiota transplantation on 8-week remission in patients with ulcerative colitis: a randomized clinical trial. JAMA. 2019;321(2):156–164.
  • 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(1):102–109.
  • Paramsothy S, Kamm MA, Kaakoush NO, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017;389(10075):1218–1228.
  • Rossen NG, Fuentes S, van der Spek MJ, et al. Findings rom a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology. 2015;149(1):110–118.
  • Sokol H, Landman C, Seksik P, Saint-Antoine IBD Network, et al. Fecal microbiota transplantation to maintain remission in Crohn’s disease: a pilot randomized controlled study. Microbiome. 2020;8(1):12.
  • Halkjaer SI, Christensen AH, Lo BZS, et al. Faecal microbiota transplantation alters gut microbiota in patients with irritable bowel syndrome: results from a randomised, double-blind placebo-controlled study. Gut. 2018;67(12):2107–2115.
  • Johnsen PH, Hilpusch F, Cavanagh JP, et al. Faecal microbiota transplantation versus placebo for moderate-to-severe irritable bowel syndrome: a double-blind, randomised, placebo-controlled, parallel-group, single-centre trial. Lancet Gastroenterol Hepatol. 2018;3(1):17–24.
  • Aroniadis OC, Brandt LJ, Oneto C, et al. Faecal microbiota transplantation for diarrhoea-predominant irritable bowel syndrome: a double-blind, randomised, placebo-controlled trial. Lancet Gastroenterol Hepatol. 2019;4(9):675–685.
  • El-Salhy M, Hatlebakk JG, Gilja OH, et al. Efficacy of faecal microbiota transplantation for patients with irritable bowel syndrome in a randomised, double-blind, placebo-controlled study. Gut. 2020;69(5):859–867.
  • Holster S, Lindqvist CM, Repsilber D, et al. The Effect of allogenic versus autologous fecal microbiota transfer on symptoms, visceral perception and fecal and mucosal microbiota in irritable bowel syndrome: a randomized controlled study. Clin Transl Gastroenterol. 2019;10(4):e00034.
  • Ianiro G, Eusebi LH, Black CJ, et al. Systematic review with meta-analysis: efficacy of faecal microbiota transplantation for the treatment of irritable bowel syndrome. Aliment Pharmacol Ther. 2019;50(3):240–248.
  • Manges AR, Steiner TS, Wright AJ. Fecal microbiota transplantation for the intestinal decolonization of extensively antimicrobial-resistant opportunistic pathogens: a review. Infect Dis. 2016;48(8):587–592.
  • Stalenhoef JE, Terveer EM, Knetsch CW, et al. Fecal microbiota transfer for multidrug-resistant Gram-negatives: a clinical success combined with microbiological failure. Open Forum Infect Dis. 2017;4(2):ofx047.
  • Singh R, de Groot PF, Geerlings SE, et al. Fecal microbiota transplantation against intestinal colonization by extended spectrum beta-lactamase producing Enterobacteriaceae: a proof of principle study. BMC Res Notes. 2018;11(1):190.
  • Grosen AK, Povlsen JV, Lemming L, et al. Faecal microbiota transplantation eradicated extended-spectrum beta-lactamase-producing Klebsiella pneumoniae from a renal transplant recipient with recurrent urinary tract infections. Case Rep Nephrol Dial. 2019;9(2):102–107.
  • Huttner BD, de Lastours V, Wassenberg M, et al. A five-day course of oral antibiotics followed by faecal transplantation to eradicate carriage of multidrug-resistant Enterobacteriaceae: a randomized clinical trial. Clin Microbiol Infect. 2019;25(7):830–838.
  • Bajaj JS, Kassam Z, Fagan A, et al. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: a randomized clinical trial. Hepatology. 2017;66(6):1727–1738.
  • Landy J, Walker AW, Li JV, et al. Variable alterations of the microbiota, without metabolic or immunological change, following faecal microbiota transplantation in patients with chronic pouchitis. Sci Rep. 2015;5:12955.
  • Fang S, Kraft CS, Dhere T, et al. Successful treatment of chronic Pouchitis utilizing fecal microbiota transplantation (FMT): a case report. Int J Colorectal Dis. 2016;31(5):1093–1094.
  • Herfarth H, Barnes EL, Long MD, et al. Combined endoscopic and oral fecal microbiota transplantation in patients with antibiotic-dependent pouchitis: low clinical efficacy due to low donor microbial engraftment. Inflamm Intest Dis. 2019;4(1):1–6.
  • Nishida A, Imaeda H, Inatomi O, et al. The efficacy of fecal microbiota transplantation for patients with chronic pouchitis: a case series. Clin Case Rep. 2019;7(4):782–788.
  • Selvig D, Piceno Y, Terdiman J, et al. Fecal microbiota transplantation in pouchitis: clinical, endoscopic, histologic, and microbiota results from a pilot study. Dig Dis Sci. 2020;65(4):1099–1106.
  • Kragsnaes MS, Kjeldsen J, Horn HC, et al. Efficacy and safety of faecal microbiota transplantation in patients with psoriatic arthritis: protocol for a 6-month, double-blind, randomised, placebo-controlled trial. BMJ Open. 2018;8(4):e019231.
  • Arora V, Kachroo S, Ghantoji SS, et al. High Horn’s index score predicts poor outcomes in patients with Clostridium difficile infection. J Hosp Infect. 2011;79(1):23–26.
  • Garey KW, Sethi S, Yadav Y, et al. Meta-analysis to assess risk factors for recurrent Clostridium difficile infection. J Hosp Infect. 2008;70(4):298–304.
  • Kyne L, Warny M, Qamar A, et al. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet. 2001;357(9251):189–193.
  • Surawicz CM, Brandt LJ, Binion DG, et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol. 2013;108(4):478–498.
  • Peri R, Aguilar RC, Tuffers K, German Clinical Microbiome Study Group (GCMSG), et al. The impact of technical and clinical factors on fecal microbiota transfer outcomes for the treatment of recurrent Clostridioides difficile infections in Germany. United Eur Gastroenterol J. 2019;7(5):716–722.
  • Ianiro G, Valerio L, Masucci L, et al. Predictors of failure after single faecal microbiota transplantation in patients with recurrent Clostridium difficile infection: results from a 3-year, single-centre cohort study. Clin Microbiol Infect. 2017;23(5):337.e1–e3.
  • Ianiro G, Maida M, Burisch J, et al. Efficacy of different faecal microbiota transplantation protocols for Clostridium difficile infection: a systematic review and meta-analysis. United Eur Gastroenterol J. 2018;6(8):1232–1244.
  • van Beurden YH, de Groot PF, van Nood E, et al. Goorhuis A: complications, effectiveness, and long term follow-up of fecal microbiota transfer by nasoduodenal tube for treatment of recurrent Clostridium difficile infection. United European Gastroenterol J. 2017;5(6):868–879.
  • 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. JAMA. 2017;318(20):1985–1993.
  • 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.
  • Youngster I, Mahabamunuge J, Systrom HK, et al. Oral, frozen fecal microbiota transplant (FMT) capsules for recurrent Clostridium difficile infection. BMC Med. 2016;14(1):134.
  • Iqbal U, Anwar H, Karim MA. Safety and efficacy of encapsulated fecal microbiota transplantation for recurrent Clostridium difficile infection: a systematic review. Eur J Gastroenterol Hepatol. 2018;30(7):730–734.
  • Ianiro G, Masucci L, Quaranta G, et al. Randomised clinical trial: faecal microbiota transplantation by colonoscopy plus vancomycin for the treatment of severe refractory Clostridium difficile infection-single versus multiple infusions. Aliment Pharmacol Ther. 2018;48(2):152–159.
  • Pringle PL, Soto MT, Chung RT, et al. Patients with cirrhosis require more fecal microbiota capsules to cure refractory and recurrent Clostridium difficile infections. Clin Gastroenterol Hepatol. 2019;17(4):791–793.
  • 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(6):940–947.
  • Satokari R, Mattila E, Kainulainen V, et al. 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(1):46–53.
  • Gough E, Shaikh H, Manges AR. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis. 2011;53(10):994–1002.
  • Costello SP, Tucker EC, La Brooy J, et al. Establishing a fecal microbiota transplant service for the treatment of Clostridium difficile infection. Clin Infect Dis. 2016;62(7):908–914.
  • 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(6):1672–1678.
  • Wang S, Xu M, Wang W, et al. Systematic review: adverse events of fecal microbiota transplantation. PLOS One. 2016;11(8):e0161174.
  • Baxter M, Colville A. Adverse events in faecal microbiota transplant: a review of the literature. J Hosp Infect. 2016;92(2):117–127.
  • Kelly CR, Kunde SS, Khoruts A. Guidance on preparing an investigational new drug application for fecal microbiota transplantation studies. Clin Gastroenterol Hepatol. 2014;12(2):283–288.
  • Cheng YW, Phelps E, Ganapini V, et al. Fecal microbiota transplantation for the treatment of recurrent and severe Clostridium difficile infection in solid organ transplant recipients: a multicenter experience. Am J Transplant. 2019;19(2):501–511.
  • Qazi T, Amaratunga T, Barnes EL, et al. The risk of inflammatory bowel disease flares after fecal microbiota transplantation: systematic review and meta-analysis. Gut Microbes. 2017;8(6):574–588.
  • Tabbaa OM, Aboelsoud MM, Mattar MC. Long-term safety and efficacy of fecal microbiota transplantation in the treatment of Clostridium difficile infection in patients with and without inflammatory bowel disease: a tertiary care center’s experience. Gastroenterol Res. 2018;11(6):397–403.
  • Hirten RP, Grinspan A, Fu SC, et al. Microbial engraftment and efficacy of fecal microbiota transplant for Clostridium difficile in patients with and without inflammatory bowel disease. Inflamm Bowel Dis. 2019;25(6):969–979.
  • Meighani A, Hart BR, Bourgi K, et al. Outcomes of fecal microbiota transplantation for Clostridium difficile infection in patients with inflammatory bowel disease. Dig Dis Sci. 2017;62(10):2870–2875.
  • Chen T, Zhou Q, Zhang D, et al. Effect of Faecal microbiota transplantation fortreatment of Clostridium difficile infection in patients with inflammatory bowel disease: a systematic review and meta-analysis of cohort studies. J Crohns Colitis. 2018;12(6):710–717.
  • Allegretti JR, Kelly CR, Grinspan A, et al. Outcomes of fecal microbiota transplantation in patients with inflammatory bowel diseases and recurrent Clostridioides difficile infection. Gastroenterology. 2020;159(5):1982–1984.
  • You JHS, Jiang X, Lee WH, et al. Cost-effectiveness analysis of fecal microbiota transplantation for recurrent Clostridium difficile infection in patients with inflammatory bowel disease. J Gastroenterol Hepatol. 2020;35(9):1515–1523.
  • 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(7):1065–1071.
  • Shogbesan O, Poudel DR, Victor S, et al. A systematic review of the efficacy and safety of fecal microbiota transplant for Clostridium difficile infection in immunocompromised patients. Can J Gastroenterol Hepatol. 2018; 2018:1–10.
  • Abu-Sbeih H, Ali FS, Wang Y. Clinical review on the utility of fecal microbiota transplantation in immunocompromised patients. Curr Gastroenterol Rep. 2019;21(4):8.
  • DeFilipp Z, Bloom PP, Torres Soto M, et al. Drug-resistant E. colibacteremia transmitted by fecal microbiota transplant. N Engl J Med. 2019;381(21):2043–2050.
  • Oppfeldt AM, Dahlerup JF, Christensen LA, et al. Faecal microbiota transplantation for recurring Clostridium difficile infection in a patient with Crohn’s disease and ileorectal anastomosis. BMJ Case Rep. 2016;217209.
  • Jørgensen SMD, Hansen MM, Erikstrup C, et al. Faecal microbiota transplantation: establishment of a clinical application framework. Eur J Gastroenterol Hepatol. 2017;29:36–45.
  • Cammarota G, Ianiro G, Tilg H, European FMT Working Group, et al. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66(4):569–580.
  • Cammarota G, Ianiro G, Kelly CR, et al. International consensus conference on stool banking for faecal microbiota transplantation in clinical practice. Gut. 2019;68(12):2111–2121.
  • Rode AA, Bytzer P, Pedersen OB, et al. Establishing a donor stool bank for faecal microbiota transplantation: methods and feasibility. Eur J Clin Microbiol Infect Dis. 2019;38(10):1837–1847.
  • Guide to the quality and safety of tissues and cells for human application. 4th ed. Strasbourg: European Directorate for the Quality of Medicines & HealthCare of the Council of Europe (EDQM); 2019.
  • Mullish BH, Quraishi MN, Segal JP, et al. The use of faecal microbiota transplant as treatment for recurrent or refractory Clostridium difficile infection and other potential indications: joint British Society of Gastroenterology (BSG) and Healthcare Infection Society (HIS) guidelines. Gut. 2018;67(11):1920–1941.
  • Competent Authorities on Substances of Human Origin Expert Group (CASoHO E01718). Meeting of the competent authorities for tissues and cells, 3–4 December 2014. Summary Report https://ec.europa.eu/health/sites/health/files/blood_tissues_organs/docs/ev_20141203_sr_en.pdf.
  • Directive 2004/23/ec of the European Parliament and of the Council of 31 March 2004 on setting standards of quality and safety for the donation, procurement, testing, preparation, preservation, storage and distribution of human tissues and cells. https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2004:102:0048:0058:en:PDF.
  • EU. EU directive relating to medicinal products for human use (2001/83/EC): European Union; 2001. https://ec.europa.eu/health/sites/default/files/files/eudralex/vol-1/dir_2001_83_consol_2012/dir_2001_83_cons_2012_en.pdf
  • Walsh JH, Purcell RH, Morrow AG, et al. Post transfusion hepatitis after open-heart operations. Incidence after the administration of blood from commercial and volunteer donor populations. JAMA. 1970;211(2):261–265.
  • Paramsothy S, Borody TJ, Lin E, et al. Donor recruitment for fecal microbiota transplantation. Inflamm Bowel Dis. 2015;21(7):1600–1606.
  • Terveer EM, van Beurden YH, Goorhuis A, et al. How to: establish and run a stool bank. Clin Microbiol Infect. 2017;23(12):924–930.
  • Kassam Z, Dubois N, Ramakrishna B, et al. Donor screening for fecal microbiota transplantation. N Engl J Med. 2019;381(21):2070–2072.
  • Kazerouni A, Burgess J, Burns LJ, et al. Optimal screening and donor management in a public stool bank. Microbiome. 2015;3(1):75.
  • Woodworth MH, Carpentieri C, Sitchenko KL, Kraft CS. Challenges in fecal donor selection and screening for fecal microbiota transplantation: a review. Gut Microbes. 2017;8(3):225–237.
  • Jørgensen SMD, Erikstrup C, Dinh KM, et al. Recruitment of feces donors among blood donors: Results from an observational cohort study. Gut Microbes. 2018;9(6):540–550.
  • Tariq R, Weatherly R, Kammer P, et al. Donor screening experience for fecal microbiota transplantation in patients with recurrent C. difficile infection. J Clin Gastroenterol. 2018;52(2):146–150.
  • Lai CY, Sung J, Cheng F, et al. Systematic review with meta-analysis: review of donor features, procedures and outcomes in 168 clinical studies of faecal microbiota transplantation. Aliment Pharmacol Ther. 2019;49(4):354–363.
  • Guo Y, Li SH, Kuang YS, He JR, et al. Effect of short-term room temperature storage on the microbial community in infant fecal samples. Sci Rep. 2016;6:26648.
  • Kragsnaes MS, Nilsson AC, Kjeldsen J, et al. How do I establish a stool bank for fecal microbiota transplantation within the blood- and tissue transplant service? Transfusion. 2020;60(6):1135–1141.
  • Ott SJ, Musfeldt M, Timmis KN, et al. In vitro alterations of intestinal bacterial microbiota in fecal samples during storage. Diagn Microbiol Infect Dis. 2004;50(4):237–245.
  • Hamilton MJ, Weingarden AR, Sadowsky MJ, et al. Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012;107(5):761–767.
  • Papanicolas LE, Choo JM, Wang Y, et al. Bacterial viability in faecal transplants: Which bacteria survive? EBioMedicine. 2019;41:509–516.
  • Browne HP, Forster SC, Anonye BO, et al. Culturing of ‘unculturable’ human microbiota reveals novel taxa and extensive sporulation. Nature. 2016;533(7604):543–546.
  • McCune VL, Quraishi MN, Manzoor S, et al. Results from the first English stool bank using faecal microbiota transplant as a medicinal product for the treatment of Clostridioides difficile infection. EClinical Medicine. 2020;20:100301.
  • Thornit DN, Sander B, la Cour M, et al. The effects of peroral glycerol on plasma osmolarity in diabetic patients and healthy individuals. Basic Clin Pharmacol Toxicol. 2009;105(5):289–293.
  • Liao CH, Shollenberger LM. Survivability and long-term preservation of bacteria in water and in phosphate-buffered saline. Lett Appl Microbiol. 2003;37(1):45–50.
  • Terveer EM, Vendrik KE, Ooijevaar RE, et al. Faecal microbiota transplantation for Clostridioides difficile infection: four years’ experience of the Netherlands Donor Feces Bank. United European Gastroenterol J. 2020;8(10):1236–1247.
  • Takahashi M, Ishikawa D, Sasaki T, et al. Faecal freezing preservation period influences colonization ability for faecal microbiota transplantation. J Appl Microbiol. 2019;126(3):973–984.
  • Detailed guidance on the collection, verification and presentation of adverse event/reaction reports arising from clinical trials on medicinal products for human use (‘CT-3’). https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:C:2011:172:0001:0013:EN:PDF
  • Sleight SC, Wigginton NS, Lenski RE. Increased susceptibility to repeated freeze-thaw cycles in Escherichia coli following long-term evolution in a benign environment. BMC Evol Biol. 2006;6(1):104.
  • Ianiro G, Mullish BH, Kelly CR, et al. Reorganisation of faecal microbiota transplant services during the covid-19 pandemic. Gut. 2020;69(9):1555–1563.