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Review article: Medical guidelines

Vol. 153 No. 8 (2023)

Swiss expert opinion: current approaches in faecal microbiota transplantation in daily practice

  • Laura Rossier
  • Christoph Matter
  • Emanuel Burri
  • Tatiana Galperine
  • Petr Hrúz
  • Pascal Juillerat
  • Alain Schoepfer
  • Stephan R. Vavricka
  • Nadine Zahnd
  • Natalie Décosterd
  • Frank Seibold
DOI
https://doi.org/10.57187/smw.2023.40100
Cite this as:
Swiss Med Wkly. 2023;153:40100
Published
25.08.2023

Summary

INTRODUCTION: Faecal microbiota transplantation (FMT) is an established therapy for recurrent C. difficile infection, and recent studies have reported encouraging results of FMT in patients with ulcerative colitis. Few international consensus guidelines exist for this therapy, and thus FMT policies and practices differ among European countries. As of 2019, stool transplants are considered a non-standardised medicinal product in Switzerland, and a standardised production process requires authorisation by the Swiss Agency for Therapeutic Products. This authorisation leads to prolonged administrative procedures and increasing costs, which reduces treatment accessibility. In particular, patients with ulcerative colitis in Switzerland can only benefit from FMT off-label, even though it is a valid therapeutic option. Therefore, this study summarised the available data on FMT and established a framework for the standardised use of FMT.

METHODS: A panel of Swiss gastroenterologists with a special interest in inflammatory bowel disease was established to identify the current key issues of FMT. After a comprehensive review of the literature, statements were formulated about FMT indications, donor screening, stool transplant preparation and administration, and safety aspects. The panel then voted on the statements following the Delphi process; the statements were reformulated and revoted until a consensus was reached. The manuscript was then reviewed by an infectiologist (the head of Lausanne’s FMT centre).

RESULTS: The established statements are summarised in the supplementary tables in the appendix to this paper. The working group hopes these will help standardise FMT practice in Switzerland and contribute to making faecal microbiota transplantation a safe and accessible treatment for patients with recurrent C. difficile infections and selected patients with ulcerative colitis, as well as other indications in the future.

References

  1. Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013 Apr;108(4):500–8. 10.1038/ajg.2013.59 DOI: https://doi.org/10.1038/ajg.2013.59
  2. van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, de Vos WM, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013 Jan;368(5):407–15. 10.1056/NEJMoa1205037 DOI: https://doi.org/10.1056/NEJMoa1205037
  3. Lawson PA, Citron DM, Tyrrell KL, Finegold SM. Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prévot 1938. Anaerobe. 2016 Aug;40:95–9. 10.1016/j.anaerobe.2016.06.008 DOI: https://doi.org/10.1016/j.anaerobe.2016.06.008
  4. D Goldenberg S, Merrick B; D. Goldenberg S. The role of faecal microbiota transplantation: looking beyond Clostridioides difficile infection. Ther Adv Infect Dis. 2021 Jan;8:2049936120981526. 10.1177/2049936120981526 DOI: https://doi.org/10.1177/2049936120981526
  5. Tilg H, Kaser A. Gut microbiome, obesity, and metabolic dysfunction. J Clin Invest. 2011 Jun;121(6):2126–32. 10.1172/JCI58109 DOI: https://doi.org/10.1172/JCI58109
  6. De Luca F, Shoenfeld Y. The microbiome in autoimmune diseases. Clin Exp Immunol. 2019 Jan;195(1):74–85. 10.1111/cei.13158 DOI: https://doi.org/10.1111/cei.13158
  7. Najafi S, Majidpoor J, Mortezaee K. The impact of microbiota on PD-1/PD-L1 inhibitor therapy outcomes: A focus on solid tumors. Life Sci. 2022 Dec;310:121138. 10.1016/j.lfs.2022.121138 DOI: https://doi.org/10.1016/j.lfs.2022.121138
  8. Fehily SR, Basnayake C, Wright EK, Kamm MA. Fecal microbiota transplantation therapy in Crohn’s disease: systematic review. J Gastroenterol Hepatol. 2021 Oct;36(10):2672–86. 10.1111/jgh.15598 DOI: https://doi.org/10.1111/jgh.15598
  9. Tan P, Li X, Shen J, Feng Q. Fecal Microbiota Transplantation for the Treatment of Inflammatory Bowel Disease: an Update. Front Pharmacol. 2020 Sep;11:574533. 10.3389/fphar.2020.574533 DOI: https://doi.org/10.3389/fphar.2020.574533
  10. Borody TJ, Paramsothy S, Agrawal G. Fecal microbiota transplantation: indications, methods, evidence, and future directions. Curr Gastroenterol Rep. 2013 Aug;15(8):337. 10.1007/s11894-013-0337-1 DOI: https://doi.org/10.1007/s11894-013-0337-1
  11. Terveer EM, van Beurden YH, Goorhuis A, Seegers JF, Bauer MP, van Nood E, et al. How to: establish and run a stool bank. Clin Microbiol Infect. 2017 Dec;23(12):924–30. 10.1016/j.cmi.2017.05.015 DOI: https://doi.org/10.1016/j.cmi.2017.05.015
  12. Transplantation de microbiote fécal : de l’évidence aux réalités du terrain. Rev Med Suisse n.d. https://www.revmed.ch/revue-medicale-suisse/2021/revue-medicale-suisse-734/transplantation-de-microbiote-fecal-de-l-evidence-aux-realites-du-terrain (accessed July 22, 2022).
  13. Keller JJ, Ooijevaar RE, Hvas CL, Terveer EM, Lieberknecht SC, Högenauer C, et al. A standardised model for stool banking for faecal microbiota transplantation: a consensus report from a multidisciplinary UEG working group. United European Gastroenterol J. 2021 Mar;9(2):229–47. 10.1177/2050640620967898 DOI: https://doi.org/10.1177/2050640620967898
  14. Keller JJ, Vehreschild MJ, Hvas CL, Jørgensen SM, Kupciskas J, Link A, et al.; UEG working group of the Standards and Guidelines initiative Stool banking for FMT. Stool for fecal microbiota transplantation should be classified as a transplant product and not as a drug. United European Gastroenterol J. 2019 Dec;7(10):1408–10. 10.1177/2050640619887579 DOI: https://doi.org/10.1177/2050640619887579
  15. Evaluation of the EU legislation on blood, tissues and cells n.d. https://health.ec.europa.eu/blood-tissues-cells-and-organs/overview/evaluation-eu-legislation-blood-tissues-and-cells_en (accessed November 6, 2022).
  16. Revision of the EU legislation on blood, tissues and cells n.d. https://health.ec.europa.eu/blood-tissues-cells-and-organs/overview/revision-eu-legislation-blood-tissues-and-cells_en (accessed November 6, 2022).
  17. European Directorate for the Quality of Medicines & HealthCare. Guide to the quality and safety of tissues and cells for human application. vol. 5th ed. EDQM Council of Europe; 2022.
  18. Swissmedic 2019 © Copyright. Advanced Therapy Medicinal Products, transplants and procedures n.d. https://www.swissmedic.ch/swissmedic/en/home/services/documents/transplantatprodukte.html (accessed July 22, 2022).
  19. Kelly CR, Fischer M, Allegretti JR, LaPlante K, Stewart DB, Limketkai BN, et al. ACG Clinical Guidelines: Prevention, Diagnosis, and Treatment of Clostridioides difficile Infections. Am J Gastroenterol. 2021 Jun;116(6):1124–47. 10.14309/ajg.0000000000001278 DOI: https://doi.org/10.14309/ajg.0000000000001278
  20. van Prehn J, Reigadas E, Vogelzang EH, Bouza E, Hristea A, Guery B, et al.; Guideline Committee of the European Study Group on Clostridioides difficile. European Society of Clinical Microbiology and Infectious Diseases: 2021 update on the treatment guidance document for Clostridioides difficile infection in adults. Clin Microbiol Infect. 2021 Dec;27 Suppl 2:S1–21. 10.1016/j.cmi.2021.09.038 DOI: https://doi.org/10.1016/j.cmi.2021.09.038
  21. Allegretti JR, Marcus J, Storm M, Sitko J, Kennedy K, Gerber GK, et al. Clinical Predictors of Recurrence After Primary Clostridioides difficile Infection: A Prospective Cohort Study. Dig Dis Sci. 2020 Jun;65(6):1761–6. 10.1007/s10620-019-05900-3 DOI: https://doi.org/10.1007/s10620-019-05900-3
  22. Johnson S, Louie TJ, Gerding DN, Cornely OA, Chasan-Taber S, Fitts D, et al.; Polymer Alternative for CDI Treatment (PACT) investigators. Vancomycin, metronidazole, or tolevamer for Clostridium difficile infection: results from two multinational, randomized, controlled trials. Clin Infect Dis. 2014 Aug;59(3):345–54. 10.1093/cid/ciu313 DOI: https://doi.org/10.1093/cid/ciu313
  23. Infection à Clostridioides difficile : approches thérapeutiques diverses. Rev Med Suisse n.d. https://www.revmed.ch/revue-medicale-suisse/2022/revue-medicale-suisse-799/infection-a-clostridioides-difficile-approches-therapeutiques-diverses (accessed October 17, 2022).
  24. Johnson S, Lavergne V, Skinner AM, Gonzales-Luna AJ, Garey KW, Kelly CP, et al. Clinical Practice Guideline by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA): 2021 Focused Update Guidelines on Management of Clostridioides difficile Infection in Adults. Clin Infect Dis. 2021 Sep;73(5):e1029–44. 10.1093/cid/ciab549 DOI: https://doi.org/10.1093/cid/ciab549
  25. Kelly CR, Khoruts A, Staley C, Sadowsky MJ, Abd M, Alani M, et al. Effect of Fecal Microbiota Transplantation on Recurrence in Multiply Recurrent Clostridium difficile Infection: A Randomized Trial. Ann Intern Med. 2016 Nov;165(9):609–16. 10.7326/M16-0271 DOI: https://doi.org/10.7326/M16-0271
  26. Cammarota G, Ianiro G, Kelly CR, Mullish BH, Allegretti JR, Kassam Z, et al. International consensus conference on stool banking for faecal microbiota transplantation in clinical practice. Gut. 2019 Dec;68(12):2111–21. 10.1136/gutjnl-2019-319548 DOI: https://doi.org/10.1136/gutjnl-2019-319548
  27. Cammarota G, Ianiro G, Tilg H, Rajilić-Stojanović M, Kump P, Satokari R, et al.; European FMT Working Group. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017 Apr;66(4):569–80. 10.1136/gutjnl-2016-313017 DOI: https://doi.org/10.1136/gutjnl-2016-313017
  28. Hvas CL, Dahl Jørgensen SM, Jørgensen SP, Storgaard M, Lemming L, Hansen MM, et al. Fecal Microbiota Transplantation Is Superior to Fidaxomicin for Treatment of Recurrent Clostridium difficile Infection. Gastroenterology. 2019 Apr;156(5):1324–1332.e3. 10.1053/j.gastro.2018.12.019 DOI: https://doi.org/10.1053/j.gastro.2018.12.019
  29. Kelly CR, Yen EF, Grinspan AM, Kahn SA, Atreja A, Lewis JD, et al. Fecal Microbiota Transplantation Is Highly Effective in Real-World Practice: Initial Results From the FMT National Registry. Gastroenterology. 2021 Jan;160(1):183–192.e3. 10.1053/j.gastro.2020.09.038 DOI: https://doi.org/10.1053/j.gastro.2020.09.038
  30. Cammarota G, Masucci L, Ianiro G, Bibbò S, Dinoi G, Costamagna 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 May;41(9):835–43. 10.1111/apt.13144 DOI: https://doi.org/10.1111/apt.13144
  31. Shaffer SR, Witt J, Targownik LE, Kao D, Lee C, Smieliauskas F, et al. Cost-effectiveness analysis of a fecal microbiota transplant center for treating recurrent C.difficile infection. J Infect. 2020 Nov;81(5):758–65. 10.1016/j.jinf.2020.09.025 DOI: https://doi.org/10.1016/j.jinf.2020.09.025
  32. Roshan N, Clancy AK, Borody TJ. Faecal Microbiota Transplantation is Effective for the Initial Treatment of Clostridium difficile Infection: A Retrospective Clinical Review. Infect Dis Ther. 2020 Dec;9(4):935–42. 10.1007/s40121-020-00339-w DOI: https://doi.org/10.1007/s40121-020-00339-w
  33. Baunwall SM, Andreasen SE, Hansen MM, Kelsen J, Høyer KL, Rågård N, et al. Faecal microbiota transplantation for first or second Clostridioides difficile infection (EarlyFMT): a randomised, double-blind, placebo-controlled trial. Lancet Gastroenterol Hepatol. 2022 Dec;7(12):1083–91. 10.1016/S2468-1253(22)00276-X DOI: https://doi.org/10.1016/S2468-1253(22)00276-X
  34. Quraishi MN, Widlak M, Bhala N, Moore D, Price M, Sharma 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 Pharmacol Ther. 2017 Sep;46(5):479–93. 10.1111/apt.14201 DOI: https://doi.org/10.1111/apt.14201
  35. Song YN, Yang DY, Veldhuyzen van Zanten S, Wong K, McArthur E, Song CZ, et al. Fecal Microbiota Transplantation for Severe or Fulminant Clostridioides difficile Infection: Systematic Review and Meta-analysis. J Can Assoc Gastroenterol. 2021 Jul;5(1):e1–11. 10.1093/jcag/gwab023 DOI: https://doi.org/10.1093/jcag/gwab023
  36. Tariq R, Syed T, Yadav D, Prokop LJ, Singh S, Loftus EV, et al. Outcomes of Fecal Microbiota Transplantation for C. difficile Infection in Inflammatory Bowel Disease: A Systematic Review and Meta-analysis. J Clin Gastroenterol. 2021;•••: 10.1097/MCG.0000000000001633 DOI: https://doi.org/10.1097/MCG.0000000000001633
  37. Allegretti JR, Kelly CR, Grinspan A, Mullish BH, Hurtado J, Carrellas M, et al. Inflammatory Bowel Disease Outcomes Following Fecal Microbiota Transplantation for Recurrent C. difficile Infection. Inflamm Bowel Dis. 2021 Aug;27(9):1371–8. 10.1093/ibd/izaa283 DOI: https://doi.org/10.1093/ibd/izaa283
  38. Qazi T, Amaratunga T, Barnes EL, Fischer M, Kassam Z, Allegretti JR. The risk of inflammatory bowel disease flares after fecal microbiota transplantation: systematic review and meta-analysis. Gut Microbes. 2017 Nov;8(6):574–88. 10.1080/19490976.2017.1353848 DOI: https://doi.org/10.1080/19490976.2017.1353848
  39. Březina J, Bajer L, Wohl P, Ďuricová D, Hrabák P, Novotný A, et al. Fecal Microbial Transplantation versus Mesalamine Enema for Treatment of Active Left-Sided Ulcerative Colitis-Results of a Randomized Controlled Trial. J Clin Med. 2021 Jun;10(13):2753. 10.3390/jcm10132753 DOI: https://doi.org/10.3390/jcm10132753
  40. Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, et al. Fecal Microbiota Transplantation Induces Remission in Patients With Active Ulcerative Colitis in a Randomized Controlled Trial. Gastroenterology. 2015 Jul;149(1):102–109.e6. 10.1053/j.gastro.2015.04.001 DOI: https://doi.org/10.1053/j.gastro.2015.04.001
  41. Haifer C, Paramsothy S, Kaakoush NO, Saikal A, Ghaly S, Yang T, et al. Lyophilised oral faecal microbiota transplantation for ulcerative colitis (LOTUS): a randomised, double-blind, placebo-controlled trial. Lancet Gastroenterol Hepatol. 2022 Feb;7(2):141–51. 10.1016/S2468-1253(21)00400-3 DOI: https://doi.org/10.1016/S2468-1253(21)00400-3
  42. Rossen NG, Fuentes S, van der Spek MJ, Tijssen JG, Hartman JH, Duflou A, et al. Findings From a Randomized Controlled Trial of Fecal Transplantation for Patients With Ulcerative Colitis. Gastroenterology. 2015 Jul;149(1):110–118.e4. 10.1053/j.gastro.2015.03.045 DOI: https://doi.org/10.1053/j.gastro.2015.03.045
  43. Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomised placebo-controlled trial. Lancet. 2017 Mar;389(10075):1218–28. 10.1016/S0140-6736(17)30182-4 DOI: https://doi.org/10.1016/S0140-6736(17)30182-4
  44. Costello SP, Hughes PA, Waters O, Bryant RV, Vincent AD, Blatchford P, et al. Effect of Fecal Microbiota Transplantation on 8-Week Remission in Patients With Ulcerative Colitis: A Randomized Clinical Trial. JAMA. 2019 Jan;321(2):156–64. 10.1001/jama.2018.20046 DOI: https://doi.org/10.1001/jama.2018.20046
  45. Costello S, Waters O, Bryant R, Katsikeros R, Makanyanga J, Schoeman M, et al. OP036 Short duration, low intensity pooled faecal microbiota transplantation induces remission in patients with mild-moderately active ulcerative colitis: a randomised controlled trial. J Crohn’s Colitis. 2017;11 suppl_1:S23. 10.1093/ecco-jcc/jjx002.035 DOI: https://doi.org/10.1093/ecco-jcc/jjx002.035
  46. Lavelle A, Sokol H. Understanding and predicting the efficacy of FMT. Nat Med. 2022 Sep;28(9):1759–60. 10.1038/s41591-022-01991-0 DOI: https://doi.org/10.1038/s41591-022-01991-0
  47. Herrlinger KR, Stange EF. Twenty-five years of biologicals in IBD: what´s all the hype about? J Intern Med. 2021 Oct;290(4):806–25. 10.1111/joim.13345 DOI: https://doi.org/10.1111/joim.13345
  48. Sood A, Mahajan R, Singh A, Midha V, Mehta V, Narang V, et al. Role of Faecal Microbiota Transplantation for Maintenance of Remission in Patients With Ulcerative Colitis: A Pilot Study. J Crohn’s Colitis. 2019 Sep;13(10):1311–7. 10.1093/ecco-jcc/jjz060 DOI: https://doi.org/10.1093/ecco-jcc/jjz060
  49. Vaughn BP, Vatanen T, Allegretti JR, Bai A, Xavier RJ, Korzenik J, et al. Increased Intestinal Microbial Diversity Following Fecal Microbiota Transplant for Active Crohn’s Disease. Inflamm Bowel Dis. 2016 Sep;22(9):2182–90. 10.1097/MIB.0000000000000893 DOI: https://doi.org/10.1097/MIB.0000000000000893
  50. Suskind DL, Brittnacher MJ, Wahbeh G, Shaffer ML, Hayden HS, Qin X, et al. Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis. 2015 Mar;21(3):556–63. 10.1097/MIB.0000000000000307 DOI: https://doi.org/10.1097/MIB.0000000000000307
  51. Gutin L, Piceno Y, Fadrosh D, Lynch K, Zydek M, Kassam Z, et al. Fecal microbiota transplant for Crohn disease: A study evaluating safety, efficacy, and microbiome profile. United European Gastroenterol J. 2019 Jul;7(6):807–14. 10.1177/2050640619845986 DOI: https://doi.org/10.1177/2050640619845986
  52. Xiang L, Ding X, Li Q, Wu X, Dai M, Long C, et al. Efficacy of faecal microbiota transplantation in Crohn’s disease: a new target treatment? Microb Biotechnol. 2020 May;13(3):760–9. 10.1111/1751-7915.13536 DOI: https://doi.org/10.1111/1751-7915.13536
  53. Yang Z, Bu C, Yuan W, Shen Z, Quan Y, Wu S, et al. Fecal Microbiota Transplant via Endoscopic Delivering Through Small Intestine and Colon: No Difference for Crohn’s Disease. Dig Dis Sci. 2020 Jan;65(1):150–7. 10.1007/s10620-019-05751-y DOI: https://doi.org/10.1007/s10620-019-05751-y
  54. Sokol H, Landman C, Seksik P, Berard L, Montil M, Nion-Larmurier I, et al.; Saint-Antoine IBD Network. Fecal microbiota transplantation to maintain remission in Crohn’s disease: a pilot randomized controlled study. Microbiome. 2020 Feb;8(1):12. 10.1186/s40168-020-0792-5 DOI: https://doi.org/10.1186/s40168-020-0792-5
  55. Johnsen PH, Hilpüsch F, Valle PC, Goll R. The effect of fecal microbiota transplantation on IBS related quality of life and fatigue in moderate to severe non-constipated irritable bowel: secondary endpoints of a double blind, randomized, placebo-controlled trial. EBioMedicine. 2020 Jan;51:102562. 10.1016/j.ebiom.2019.11.023 DOI: https://doi.org/10.1016/j.ebiom.2019.11.023
  56. Ooijevaar RE, Terveer EM, Verspaget HW, Kuijper EJ, Keller JJ. Clinical Application and Potential of Fecal Microbiota Transplantation. Annu Rev Med. 2019 Jan;70(1):335–51. 10.1146/annurev-med-111717-122956 DOI: https://doi.org/10.1146/annurev-med-111717-122956
  57. Yu EW, Gao L, Stastka P, Cheney MC, Mahabamunuge J, Torres Soto M, et al. Fecal microbiota transplantation for the improvement of metabolism in obesity: the FMT-TRIM double-blind placebo-controlled pilot trial. PLoS Med. 2020 Mar;17(3):e1003051. 10.1371/journal.pmed.1003051 DOI: https://doi.org/10.1371/journal.pmed.1003051
  58. Vendrik KE, Ooijevaar RE, de Jong PR, Laman JD, van Oosten BW, van Hilten JJ, et al. Fecal Microbiota Transplantation in Neurological Disorders. Front Cell Infect Microbiol. 2020 Mar;10:98. 10.3389/fcimb.2020.00098 DOI: https://doi.org/10.3389/fcimb.2020.00098
  59. El-Salhy M, Hatlebakk JG, Gilja OH, Bråthen Kristoffersen A, Hausken T. Efficacy of faecal microbiota transplantation for patients with irritable bowel syndrome in a randomised, double-blind, placebo-controlled study. Gut. 2020 May;69(5):859–67. 10.1136/gutjnl-2019-319630 DOI: https://doi.org/10.1136/gutjnl-2019-319630
  60. El-Salhy M, Winkel R, Casen C, Hausken T, Gilja OH, Hatlebakk JG. Efficacy of Fecal Microbiota Transplantation for Patients With Irritable Bowel Syndrome at 3 Years After Transplantation. Gastroenterology. 2022 Oct;163(4):982–994.e14. 10.1053/j.gastro.2022.06.020 DOI: https://doi.org/10.1053/j.gastro.2022.06.020
  61. FMT in IBS. “We’ve Been Targeting Wrong Part of the Intestine.” Medscape n.d. https://www.medscape.com/viewarticle/982505 (accessed October 22, 2022).
  62. Xu F, Li N, Wang C, Xing H, Chen D, Wei Y. Clinical efficacy of fecal microbiota transplantation for patients with small intestinal bacterial overgrowth: a randomized, placebo-controlled clinic study. BMC Gastroenterol. 2021 Feb;21(1):54. 10.1186/s12876-021-01630-x DOI: https://doi.org/10.1186/s12876-021-01630-x
  63. Commission Directive 2006/17/EC of 8 February 2006 implementing Directive 2004/23/EC of the European Parliament and of the Council as regards certain technical requirements for the donation, procurement and testing of human tissues and cells (Text with EEA relevance). vol. 038. 2006.
  64. Sokol H, Galperine T, Kapel N, Bourlioux P, Seksik P, Barbut F, et al.; French Group of Faecal microbiota Transplantation (FGFT). Faecal microbiota transplantation in recurrent Clostridium difficile infection: Recommendations from the French Group of Faecal microbiota Transplantation. Dig Liver Dis. 2016 Mar;48(3):242–7. 10.1016/j.dld.2015.08.017 DOI: https://doi.org/10.1016/j.dld.2015.08.017
  65. Gweon TG, Lee YJ, Kim KO, Yim SK, Soh JS, Kim SY, et al.; Gut Microbiota and Therapy Research Group Under the Korean Society of Neurogastroenterology and Motility. Clinical Practice Guidelines for Fecal Microbiota Transplantation in Korea. J Neurogastroenterol Motil. 2022 Jan;28(1):28–42. 10.5056/jnm21221 DOI: https://doi.org/10.5056/jnm21221
  66. Commissioner O of the. Fecal Microbiota for Transplantation: Safety Alert - Risk of Serious Adverse Events Likely Due to Transmission of Pathogenic Organisms. FDA; 2020.
  67. Terveer EM, van Gool T, Ooijevaar RE, Sanders IM, Boeije-Koppenol E, Keller JJ, et al.; Netherlands Donor Feces Bank (NDFB) Study Group. Human Transmission of Blastocystis by Fecal Microbiota Transplantation Without Development of Gastrointestinal Symptoms in Recipients. Clin Infect Dis. 2020 Dec;71(10):2630–6. 10.1093/cid/ciz1122 DOI: https://doi.org/10.1093/cid/ciz1122
  68. Aykur M, Calıskan Kurt C, Dirim Erdogan D, Biray Avcı C, Vardar R, Aydemir S, et al. Investigation of Dientamoeba fragilis Prevalence and Evaluation of Sociodemographic and Clinical Features in Patients with Gastrointestinal Symptoms. Acta Parasitol. 2019 Mar;64(1):162–70. 10.2478/s11686-018-00017-5 DOI: https://doi.org/10.2478/s11686-018-00017-5
  69. Chou A, Austin RL. Entamoeba Histolytica. StatPearls. Treasure Island (FL): StatPearls Publishing; 2022.
  70. Mehta N, Wang T, Friedman-Moraco RJ, Carpentieri C, Mehta AK, Rouphael N, et al. Fecal Microbiota Transplantation Donor Screening Updates and Research Gaps for Solid Organ Transplant Recipients. J Clin Microbiol. 2022 Feb;60(2):e0016121. 10.1128/JCM.00161-21 DOI: https://doi.org/10.1128/JCM.00161-21
  71. DeFilipp Z, Bloom PP, Torres Soto M, Mansour MK, Sater MR, Huntley MH, et al. Drug-Resistant E. coli Bacteremia Transmitted by Fecal Microbiota Transplant. N Engl J Med. 2019 Nov;381(21):2043–50. 10.1056/NEJMoa1910437 DOI: https://doi.org/10.1056/NEJMoa1910437
  72. Vendrik KE, Terveer EM, Kuijper EJ, Nooij S, Boeije-Koppenol E, Sanders IM, et al.; Netherlands Donor Faeces Bank Study Group. Periodic screening of donor faeces with a quarantine period to prevent transmission of multidrug-resistant organisms during faecal microbiota transplantation: a retrospective cohort study. Lancet Infect Dis. 2021 May;21(5):711–21. 10.1016/S1473-3099(20)30473-4 DOI: https://doi.org/10.1016/S1473-3099(20)30473-4
  73. Hohmann EL. Faecal microbiota transplantation: more screening for old and new pathogens. Lancet Infect Dis. 2021 May;21(5):587–9. 10.1016/S1473-3099(20)30850-1 DOI: https://doi.org/10.1016/S1473-3099(20)30850-1
  74. Ianiro G, Mullish BH, Kelly CR, Kassam Z, Kuijper EJ, Ng SC, et al. Reorganisation of faecal microbiota transplant services during the COVID-19 pandemic. Gut. 2020 Sep;69(9):1555–63. 10.1136/gutjnl-2020-321829 DOI: https://doi.org/10.1136/gutjnl-2020-321829
  75. Manzoor SE, Zaman S, Whalley C, Inglis D, Bosworth A, Kidd M, et al. Multi-modality detection of SARS-CoV-2 in faecal donor samples for transplantation and in asymptomatic emergency surgical admissions. F1000 Res. 2021 May;10:373. 10.12688/f1000research.52178.1 DOI: https://doi.org/10.12688/f1000research.52178.1
  76. Bastiaanssen TF, Cowan CS, Claesson MJ, Dinan TG, Cryan JF. Making Sense of … the Microbiome in Psychiatry. Int J Neuropsychopharmacol. 2019 Jan;22(1):37–52. 10.1093/ijnp/pyy067 DOI: https://doi.org/10.1093/ijnp/pyy067
  77. Glassner KL, Abraham BP, Quigley EM. The microbiome and inflammatory bowel disease. J Allergy Clin Immunol. 2020 Jan;145(1):16–27. 10.1016/j.jaci.2019.11.003 DOI: https://doi.org/10.1016/j.jaci.2019.11.003
  78. Inoue Y, Shimojo N. Microbiome/microbiota and allergies. Semin Immunopathol. 2015 Jan;37(1):57–64. 10.1007/s00281-014-0453-5 DOI: https://doi.org/10.1007/s00281-014-0453-5
  79. Ruusunen A, Rocks T, Jacka F, Loughman A. The gut microbiome in anorexia nervosa: relevance for nutritional rehabilitation. Psychopharmacology (Berl). 2019 May;236(5):1545–58. 10.1007/s00213-018-5159-2 DOI: https://doi.org/10.1007/s00213-018-5159-2
  80. Hensgens MP, Goorhuis A, Dekkers OM, Kuijper EJ. Time interval of increased risk for Clostridium difficile infection after exposure to antibiotics. J Antimicrob Chemother. 2012 Mar;67(3):742–8. 10.1093/jac/dkr508 DOI: https://doi.org/10.1093/jac/dkr508
  81. Becattini S, Taur Y, Pamer EG. Antibiotic-Induced Changes in the Intestinal Microbiota and Disease. Trends Mol Med. 2016 Jun;22(6):458–78. 10.1016/j.molmed.2016.04.003 DOI: https://doi.org/10.1016/j.molmed.2016.04.003
  82. Stefura T, Zapała B, Gosiewski T, Skomarovska O, Pędziwiatr M, Major P. Changes in the Composition of Oral and Intestinal Microbiota After Sleeve Gastrectomy and Roux-En-Y Gastric Bypass and Their Impact on Outcomes of Bariatric Surgery. Obes Surg. 2022 May;32(5):1439–50. 10.1007/s11695-022-05954-9 DOI: https://doi.org/10.1007/s11695-022-05954-9
  83. Mangiola F, Nicoletti A, Gasbarrini A, Ponziani FR. Gut microbiota and aging. Eur Rev Med Pharmacol Sci. 2018 Nov;22(21):7404–13. 10.26355/eurrev_201811_16280
  84. Steele SR, Park GE, Johnson EK, Martin MJ, Stojadinovic A, Maykel JA, et al. The impact of age on colorectal cancer incidence, treatment, and outcomes in an equal-access health care system. Dis Colon Rectum. 2014 Mar;57(3):303–10. 10.1097/DCR.0b013e3182a586e7 DOI: https://doi.org/10.1097/DCR.0b013e3182a586e7
  85. Bénard MV, de Bruijn CM, Fenneman AC, Wortelboer K, Zeevenhoven J, Rethans B, et al. Challenges and costs of donor screening for fecal microbiota transplantations. PLoS One. 2022 Oct;17(10):e0276323. 10.1371/journal.pone.0276323 DOI: https://doi.org/10.1371/journal.pone.0276323
  86. Gough E, Shaikh H, Manges AR. Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection. Clin Infect Dis. 2011 Nov;53(10):994–1002. 10.1093/cid/cir632 DOI: https://doi.org/10.1093/cid/cir632
  87. Ianiro G, Maida M, Burisch J, Simonelli C, Hold G, Ventimiglia M, et al. Efficacy of different faecal microbiota transplantation protocols for Clostridium difficile infection: A systematic review and meta-analysis. United European Gastroenterol J. 2018 Oct;6(8):1232–44. 10.1177/2050640618780762 DOI: https://doi.org/10.1177/2050640618780762
  88. Osman M, Budree S, Kelly CR, Panchal P, Allegretti JR, Kassam Z, et al.; OpenBiome Collaborators. Effectiveness and Safety of Fecal Microbiota Transplantation for Clostridioides Difficile Infection: Results From a 5344-Patient Cohort Study. Gastroenterology. 2022 Jul;163(1):319–22. 10.1053/j.gastro.2022.03.051 DOI: https://doi.org/10.1053/j.gastro.2022.03.051
  89. Satokari R, Mattila E, Kainulainen V, Arkkila PE. 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 Jan;41(1):46–53. 10.1111/apt.13009 DOI: https://doi.org/10.1111/apt.13009
  90. Nicco C, Paule A, Konturek P, Edeas M. From Donor to Patient: Collection, Preparation and Cryopreservation of Fecal Samples for Fecal Microbiota Transplantation. Diseases. 2020 Apr;8(2):E9. 10.3390/diseases8020009 DOI: https://doi.org/10.3390/diseases8020009
  91. 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 Microbiol Infect Dis. 2017 Aug;88(4):322–9. 10.1016/j.diagmicrobio.2017.05.007 DOI: https://doi.org/10.1016/j.diagmicrobio.2017.05.007
  92. Lee CH, Steiner T, Petrof EO, Smieja M, Roscoe D, Nematallah A, 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 Jan;315(2):142–9. 10.1001/jama.2015.18098 DOI: https://doi.org/10.1001/jama.2015.18098
  93. Fadda HM. The Route to Palatable Fecal Microbiota Transplantation. AAPS PharmSciTech. 2020 Apr;21(3):114. 10.1208/s12249-020-1637-z DOI: https://doi.org/10.1208/s12249-020-1637-z
  94. Jiang ZD, Ajami NJ, Petrosino JF, Jun G, Hanis CL, Shah M, 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 Apr;45(7):899–908. 10.1111/apt.13969 DOI: https://doi.org/10.1111/apt.13969
  95. Jiang ZD, Jenq RR, Ajami NJ, Petrosino JF, Alexander AA, Ke S, et al. Safety and preliminary efficacy of orally administered lyophilized fecal microbiota product compared with frozen product given by enema for recurrent Clostridium difficile infection: A randomized clinical trial. PLoS One. 2018 Nov;13(11):e0205064. 10.1371/journal.pone.0205064 DOI: https://doi.org/10.1371/journal.pone.0205064
  96. Jalanka J, Salonen A, Salojärvi J, Ritari J, Immonen O, Marciani L, et al. Effects of bowel cleansing on the intestinal microbiota. Gut. 2015 Oct;64(10):1562–8. 10.1136/gutjnl-2014-307240 DOI: https://doi.org/10.1136/gutjnl-2014-307240
  97. Kao D, Roach B, Silva M, Beck P, Rioux K, Kaplan GG, et al. Effect of Oral Capsule- vs Colonoscopy-Delivered Fecal Microbiota Transplantation on Recurrent Clostridium difficile Infection: A Randomized Clinical Trial. JAMA. 2017 Nov;318(20):1985–93. 10.1001/jama.2017.17077 DOI: https://doi.org/10.1001/jama.2017.17077
  98. Tariq R, Hayat M, Pardi D, Khanna S. Predictors of failure after fecal microbiota transplantation for recurrent Clostridioides difficile infection: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis. 2021 Jul;40(7):1383–92. 10.1007/s10096-021-04163-z DOI: https://doi.org/10.1007/s10096-021-04163-z
  99. Chen QY, Tian HL, Yang B, Lin ZL, Zhao D, Ye C, et al. [Effect of intestinal preparation on the efficacy and safety of fecal microbiota transplantation treatment]. Zhonghua Wei Chang Wai Ke Za Zhi. 2020 Jul;23 Z1:48–55. 10.3760/cma.j.cn.441530-20200418-00225
  100. Fischer M, Sipe B, Cheng YW, Phelps E, Rogers N, Sagi S, et al. Fecal microbiota transplant in severe and severe-complicated Clostridium difficile: A promising treatment approach. Gut Microbes. 2017 May;8(3):289–302. 10.1080/19490976.2016.1273998 DOI: https://doi.org/10.1080/19490976.2016.1273998
  101. Smith BJ, Piceno Y, Zydek M, Zhang B, Syriani LA, Terdiman JP, et al. Strain-resolved analysis in a randomized trial of antibiotic pretreatment and maintenance dose delivery mode with fecal microbiota transplant for ulcerative colitis. Sci Rep. 2022 Apr;12(1):5517. 10.1038/s41598-022-09307-5 DOI: https://doi.org/10.1038/s41598-022-09307-5
  102. Abujamel T, Cadnum JL, Jury LA, Sunkesula VC, Kundrapu S, Jump RL, et al. Defining the vulnerable period for re-establishment of Clostridium difficile colonization after treatment of C. difficile infection with oral vancomycin or metronidazole. PLoS One. 2013 Oct;8(10):e76269. 10.1371/journal.pone.0076269 DOI: https://doi.org/10.1371/journal.pone.0076269
  103. Cammarota G, Ianiro G, Gasbarrini A. Fecal microbiota transplantation for the treatment of Clostridium difficile infection: a systematic review. J Clin Gastroenterol. 2014 Sep;48(8):693–702. 10.1097/MCG.0000000000000046 DOI: https://doi.org/10.1097/MCG.0000000000000046
  104. Baunwall SM, Terveer EM, Dahlerup JF, Erikstrup C, Arkkila P, Vehreschild MJ, et al. The use of Faecal Microbiota Transplantation (FMT) in Europe: A Europe-wide survey. Lancet Reg Health Eur. 2021 Jul;9:100181. 10.1016/j.lanepe.2021.100181 DOI: https://doi.org/10.1016/j.lanepe.2021.100181
  105. Mullish BH, Quraishi MN, Segal JP, McCune VL, Baxter M, Marsden GL, 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. J Hosp Infect. 2018 Sep;100 Suppl 1:S1–31. 10.1016/j.jhin.2018.07.037 DOI: https://doi.org/10.1016/j.jhin.2018.07.037
  106. Ramai D, Zakhia K, Fields PJ, Ofosu A, Patel G, Shahnazarian V, 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. 2021 Feb;66(2):369–80. 10.1007/s10620-020-06185-7 DOI: https://doi.org/10.1007/s10620-020-06185-7
  107. Lee CH, Belanger JE, Kassam Z, Smieja M, Higgins D, Broukhanski G, 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 Infect Dis. 2014 Aug;33(8):1425–8. 10.1007/s10096-014-2088-9 DOI: https://doi.org/10.1007/s10096-014-2088-9
  108. Oral Vancomycin Followed by Fecal Transplantation Versus Tapering Oral Vancomycin Treatment for Recurrent Clostridium difficile Infection: An Open-Label, Randomized Controlled Trial - PubMed n.d. https://pubmed.ncbi.nlm.nih.gov/28011612/ (accessed August 19, 2022).
  109. Du C, Luo Y, Walsh S, Grinspan A. Oral Fecal Microbiota Transplant Capsules Are Safe and Effective for Recurrent Clostridioides difficile Infection: A Systematic Review and Meta-Analysis. J Clin Gastroenterol. 2021 Apr;55(4):300–8. 10.1097/MCG.0000000000001495 DOI: https://doi.org/10.1097/MCG.0000000000001495
  110. Terveer EM, van Beurden YH, van Dorp S, Keller JJ, Kuijper EJ. Is the Lower Gastrointestinal Route Really Preferred Over the Upper Gastrointestinal Route for Fecal Microbiota Transfer? J Clin Gastroenterol. 2016;50(10):895. 10.1097/MCG.0000000000000595 DOI: https://doi.org/10.1097/MCG.0000000000000595
  111. Youngster I, Sauk J, Pindar C, Wilson RG, Kaplan JL, Smith MB, 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 Jun;58(11):1515–22. 10.1093/cid/ciu135 DOI: https://doi.org/10.1093/cid/ciu135
  112. Furuya-Kanamori L, Doi SA, Paterson DL, Helms SK, Yakob L, McKenzie SJ, et al. Upper Versus Lower Gastrointestinal Delivery for Transplantation of Fecal Microbiota in Recurrent or Refractory Clostridium difficile Infection: A Collaborative Analysis of Individual Patient Data From 14 Studies. J Clin Gastroenterol. 2017 Feb;51(2):145–50. 10.1097/MCG.0000000000000511 DOI: https://doi.org/10.1097/MCG.0000000000000511
  113. van Beurden YH, de Groot PF, van Nood E, Nieuwdorp M, Keller JJ, 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 Oct;5(6):868–79. 10.1177/2050640616678099 DOI: https://doi.org/10.1177/2050640616678099
  114. Zipursky JS, Sidorsky TI, Freedman CA, Sidorsky MN, Kirkland KB. Patient attitudes toward the use of fecal microbiota transplantation in the treatment of recurrent Clostridium difficile infection. Clin Infect Dis. 2012 Dec;55(12):1652–8. 10.1093/cid/cis809 DOI: https://doi.org/10.1093/cid/cis809
  115. Hong AS, Yu WY, Hong JM, Cross CL, Azab M, Ohning G, et al. Proton pump inhibitor in upper gastrointestinal fecal microbiota transplant: A systematic review and analysis. J Gastroenterol Hepatol. 2020 Jun;35(6):932–40. 10.1111/jgh.14958 DOI: https://doi.org/10.1111/jgh.14958
  116. Weingarden AR, Hamilton MJ, Sadowsky MJ, Khoruts A. Resolution of severe Clostridium difficile infection following sequential fecal microbiota transplantation. J Clin Gastroenterol. 2013 Sep;47(8):735–7. 10.1097/MCG.0b013e31829004ae DOI: https://doi.org/10.1097/MCG.0b013e31829004ae
  117. Ianiro G, Masucci L, Quaranta G, Simonelli C, Lopetuso LR, Sanguinetti M, 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 Jul;48(2):152–9. 10.1111/apt.14816 DOI: https://doi.org/10.1111/apt.14816
  118. Danne C, Rolhion N, Sokol H. Recipient factors in faecal microbiota transplantation: one stool does not fit all. Nat Rev Gastroenterol Hepatol. 2021 Jul;18(7):503–13. 10.1038/s41575-021-00441-5 DOI: https://doi.org/10.1038/s41575-021-00441-5
  119. Stallmach A, Lange K, Buening J, Sina C, Vital M, Pieper DH. Fecal Microbiota Transfer in Patients With Chronic Antibiotic-Refractory Pouchitis. Am J Gastroenterol. 2016 Mar;111(3):441–3. 10.1038/ajg.2015.436 DOI: https://doi.org/10.1038/ajg.2015.436
  120. Selvig D, Piceno Y, Terdiman J, Zydek M, Umetsu SE, Balitzer D, et al. Fecal Microbiota Transplantation in Pouchitis: Clinical, Endoscopic, Histologic, and Microbiota Results from a Pilot Study. Dig Dis Sci. 2020 Apr;65(4):1099–106. 10.1007/s10620-019-05715-2 DOI: https://doi.org/10.1007/s10620-019-05715-2
  121. Park SY, Seo GS. Fecal Microbiota Transplantation: Is It Safe? Clin Endosc. 2021 Mar;54(2):157–60. 10.5946/ce.2021.072 DOI: https://doi.org/10.5946/ce.2021.072
  122. Wang S, Xu M, Wang W, Cao X, Piao M, Khan S, et al. Systematic Review: Adverse Events of Fecal Microbiota Transplantation. PLoS One. 2016 Aug;11(8):e0161174. 10.1371/journal.pone.0161174 DOI: https://doi.org/10.1371/journal.pone.0161174
  123. Baxter M, Colville A. Adverse events in faecal microbiota transplant: a review of the literature. J Hosp Infect. 2016 Feb;92(2):117–27. 10.1016/j.jhin.2015.10.024 DOI: https://doi.org/10.1016/j.jhin.2015.10.024
  124. Marcella C, Cui B, Kelly CR, Ianiro G, Cammarota G, Zhang F. Systematic review: the global incidence of faecal microbiota transplantation-related adverse events from 2000 to 2020. Aliment Pharmacol Ther. 2021 Jan;53(1):33–42. 10.1111/apt.16148 DOI: https://doi.org/10.1111/apt.16148
  125. Baxter M, Ahmad T, Colville A, Sheridan R. Fatal Aspiration Pneumonia as a Complication of Fecal Microbiota Transplant. Clin Infect Dis. 2015 Jul;61(1):136–7. 10.1093/cid/civ247 DOI: https://doi.org/10.1093/cid/civ247
  126. Research C for BE and. Safety Alert Regarding Use of Fecal Microbiota for Transplantation and Additional Safety Protections Pertaining to Monkeypox Virus. FDA; 2022.
  127. Drewes JL, Corona A, Sanchez U, Fan Y, Hourigan SK, Weidner M, et al. Transmission and clearance of potential procarcinogenic bacteria during fecal microbiota transplantation for recurrent Clostridioides difficile. JCI Insight. 2019 Oct;4(19):e130848. 10.1172/jci.insight.130848 DOI: https://doi.org/10.1172/jci.insight.130848
  128. Alang N, Kelly CR. Weight gain after fecal microbiota transplantation. Open Forum Infect Dis. 2015 Feb;2(1):ofv004. 10.1093/ofid/ofv004 DOI: https://doi.org/10.1093/ofid/ofv004
  129. Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, et al. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol. 2012 Jul;107(7):1079–87. 10.1038/ajg.2012.60 DOI: https://doi.org/10.1038/ajg.2012.60
  130. Dawwas GK, Brensinger CM, Vajravelu RK, Wu Q, Kelly CR, Laine L, et al. Long-term Outcomes Following Multiply Recurrent Clostridioides difficile Infection and Fecal Microbiota Transplantation. Clin Gastroenterol Hepatol. 2022 Apr;20(4):806–816.e6. 10.1016/j.cgh.2020.12.004 DOI: https://doi.org/10.1016/j.cgh.2020.12.004
  131. De Leon LM, Watson JB, Kelly CR. Transient flare of ulcerative colitis after fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol. 2013 Aug;11(8):1036–8. 10.1016/j.cgh.2013.04.045 DOI: https://doi.org/10.1016/j.cgh.2013.04.045

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