Fecal Microbiota Transplants: Current Knowledge and Future Directions

  • Roxana Chis
  • Prameet M. Sheth
  • Elaine O. PetrofEmail author
Part of the Physiology in Health and Disease book series (PIHD)


The human gastrointestinal tract (GI) is home to an exceptionally diverse bacterial community, collectively referred to as the gut microbiota. These microbes play a pivotal role in modulating host physiology and immune response, in both gastrointestinal health and disease. There is evidence that alterations leading to an imbalance of the constituents of the gut microbiota, or dysbiosis, may contribute to several intestinal and extra-intestinal pathological states. These discoveries have led to exciting new microbe-based therapeutic developments, including reconstitution of bacterial communities, to reverse and correct dysbiosis. For instance, fecal microbiota transplantation (FMT), the process of infusing fecal matter from a healthy donor into a sick patient to restore a healthy microbiome in the recipient, has been used to treat recurrent Clostridium difficile infection (rCDI) and may hold promise for other gastrointestinal conditions. This chapter focuses on the key aspects of FMT, including methodology, physician and patient attitudes, safety and regulation, and its therapeutic potential for the treatment of rCDI and other gastrointestinal conditions, including inflammatory bowel disease, obesity, irritable bowel syndrome, and colorectal cancer.


  1. Abdelfatah M, Nayfe R, Nijim A, Enriquez K, Ali E, Watkins RR, Kandil H (2015) Factors predicting recurrence of Clostridium difficile infection (CDI) in hospitalized patients: retrospective study of more than 2000 patients. J Investig Med 63:747–751PubMedCrossRefGoogle Scholar
  2. Abt MC, McKenney PT, Pamer EG (2016) Clostridium difficile colitis: pathogenesis and host defence. Nat Rev Microbiol 14:609–620PubMedPubMedCentralCrossRefGoogle Scholar
  3. Agrawal M, Aroniadis OC, Brandt LJ, Kelly C, Freeman S, Surawicz C, Broussard E, Stollman N, Giovanelli A, Smith B, Yen E, Trivedi A, Hubble L, Kao D, Borody T, Finlayson S, Ray A, Smith R (2016) The long-term efficacy and safety of fecal microbiota transplant for recurrent, severe, and complicated Clostridium difficile infection in 146 elderly individuals. J Clin Gastroenterol 50:403–407PubMedGoogle Scholar
  4. Alang N, Kelly CR (2015) Weight gain after fecal microbiota transplantation. Open Forum Infect Dis 2:ofv004PubMedPubMedCentralCrossRefGoogle Scholar
  5. Aldeyab MA, Kearney MP, Scott MG, Aldiab MA, Alahmadi YM, Darwish Elhajji FW, Magee FA, McElnay JC (2012) An evaluation of the impact of antibiotic stewardship on reducing the use of high-risk antibiotics and its effect on the incidence of Clostridium difficile infection in hospital settings. J Antimicrob Chemother 67(12):2988–2996PubMedCrossRefGoogle Scholar
  6. Angelberger S, Reinisch W, Makristathis A, Lichtenberger C, Dejaco C, Papay P, Novacek G, Trauner M, Loy A, Berry D (2013) Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am J Gastroenterol 108:1620–1630PubMedCrossRefGoogle Scholar
  7. Barbut F, Richard A, Hamadi K, Chomette V, Burghoffer B, Petit JC (2000) Epidemiology of recurrences or reinfections of Clostridium difficile-associated diarrhea. J Clin Microbiol 38(6):2386–2388PubMedPubMedCentralGoogle Scholar
  8. Bakken JS (2009) Fecal bacteriotherapy for recurrent Clostridium difficile infection. Anaerobe 15:285–289PubMedCrossRefGoogle Scholar
  9. Bakken JS, Borody T, Brandt LJ, Brill JV, Demarco DC, Franzos MA, Kelly C, Khoruts A, Louie T, Martinelli LP, Moore TA, Russell G, Surawicz C (2011) Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol 9:1044–1049PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bartlett JG, Gerding DN (2008) Clinical recognition and diagnosis of Clostridium difficile infection. Clin Infect Dis 46(Suppl 1):S12–S18PubMedCrossRefGoogle Scholar
  11. Baxter M, Ahmad T, Colville A, Sheridan R (2015) Fatal aspiration pneumonia as a complication of fecal microbiota transplant. Clin Infect Dis 61:136–137PubMedCrossRefGoogle Scholar
  12. Bennet JD, Brinkman M (1989) Treatment of ulcerative colitis by implantation of normal colonic flora. Lancet 1:164PubMedCrossRefGoogle Scholar
  13. Bingham SA (2000) Diet and colorectal cancer prevention. Biochem Soc Trans 28:12–16PubMedCrossRefGoogle Scholar
  14. Bolino CM, Bercik P (2010) Pathogenic factors involved in the development of irritable bowel syndrome: focus on a microbial role. Infect Dis Clin North Am 24:961–975. ixPubMedCrossRefGoogle Scholar
  15. Borody TJ, George L, Andrews P, Brandl S, Noonan S, Cole P, Hyland L, Morgan A, Maysey J, Moore-Jones D (1989) Bowel-flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome? Med J Aust 150:604PubMedGoogle Scholar
  16. Borody TJ, Warren EF, Leis S, Surace R, Ashman O (2003) Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol 37:42–47PubMedCrossRefGoogle Scholar
  17. Boulange CL, Neves AL, Chilloux J, Nicholson JK, Dumas ME (2016) Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med 8:42PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brandt LJ, Aroniadis OC, Mellow M, Kanatzar A, Kelly C, Park T, Stollman N, Rohlke F, Surawicz C (2012) Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection. Am J Gastroenterol 107:1079–1087PubMedCrossRefGoogle Scholar
  19. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, Barnes R, Watson P, Allen-Vercoe E, Moore RA, Holt RA (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22:299–306PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB (2008) Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 197:435–438PubMedCrossRefGoogle Scholar
  21. Chow J, Tang H, Mazmanian SK (2011) Pathobionts of the gastrointestinal microbiota and inflammatory disease. Curr Opin Immunol 23:473–480PubMedPubMedCentralCrossRefGoogle Scholar
  22. Clinicaltrials.govGoogle Scholar
  23. Codling C, O’Mahony L, Shanahan F, Quigley EM, Marchesi JR (2010) A molecular analysis of fecal and mucosal bacterial communities in irritable bowel syndrome. Dig Dis Sci 55:392–397PubMedCrossRefGoogle Scholar
  24. Colman RJ, Rubin DT (2014) Fecal microbiota transplantation as therapy for inflammatory bowel disease: a systematic review and meta-analysis. J Crohns Colitis 8:1569–1581PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, Huang G, Liu Z, Wu P, Fan Z, Ji G, Wang X, Wu K, Fan D, Zhang F (2015) Fecal microbiota transplantation through mid-gut for refractory Crohn’s disease: safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol 30:51–58PubMedCrossRefGoogle Scholar
  26. De Leon LM, Watson JB, Kelly CR (2013) Transient flare of ulcerative colitis after fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol 11(1038):1036PubMedCrossRefGoogle Scholar
  27. Di Luccia B, Crescenzo R, Mazzoli A, Cigliano L, Venditti P, Walser JC, Widmer A, Baccigalupi L, Ricca E, Iossa S (2015) Rescue of fructose-induced metabolic syndrome by antibiotics or faecal transplantation in a rat model of obesity. PLoS One 10:e0134893PubMedPubMedCentralCrossRefGoogle Scholar
  28. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638PubMedPubMedCentralCrossRefGoogle Scholar
  29. Eiseman B, Silen W, Bascom GS, Kauvar AJ (1958) Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44:854–859PubMedGoogle Scholar
  30. Enck P, Aziz Q, Barbara G, Farmer AD, Fukudo S, Mayer EA, Niesler B, Quigley EMM, Rajilić-Stojanović M, Schemann M, Schwille-Kiuntke J, Simren M, Zipfel S, Spiller RC (2016) Irritable bowel syndrome. Nat Rev Dis Primers 2:16014PubMedPubMedCentralCrossRefGoogle Scholar
  31. Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y, Faust K, Kurilshikov A, Bonder MJ, Valles-Colomer M, Vandeputte D, Tito RY, Chaffron S, Rymenans L, Verspecht C, de Sutter L, Lima-Mendez G, D’Hoe K, Jonckheere K, Homola D, Garcia R, Tigchelaar EF, Eeckhaudt L, Fu J, Henckaerts L, Zhernakova A, Wijmenga C, Raes J (2016) Population-level analysis of gut microbiome variation. Science 352:560–564PubMedCrossRefGoogle Scholar
  32. Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TM, Comelli EM (2014) Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutr Diabetes 4:e121PubMedPubMedCentralCrossRefGoogle Scholar
  33. Figueroa I, Johnson S, Sambol SP, Goldstein EJ, Citron DM, Gerding DN (2012) Relapse versus reinfection: recurrent Clostridium difficile infection following treatment with fidaxomicin or vancomycin. Clin Infect Dis 55(Suppl 2):S104–S109PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fischer M, Kao D, Mehta SR, Martin T, Dimitry J, Keshteli AH, Cook GK, Phelps E, Sipe BW, Xu H, Kelly CR (2016) Predictors of early failure after fecal microbiota transplantation for the therapy of Clostridium difficile infection: a multicenter study. Am J Gastroenterol 111:1024–1031PubMedCrossRefGoogle Scholar
  35. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104:13780–13785PubMedPubMedCentralCrossRefGoogle Scholar
  36. Frank DN, Zhu W, Sartor RB, Li E (2011) Investigating the biological and clinical significance of human dysbioses. Trends Microbiol 19:427–434PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ge X, Tian H, Ding C, Gu L, Wei Y, Gong J, Zhu W, Li N, Li J (2016) Fecal microbiota transplantation in combination with soluble dietary fiber for treatment of slow transit constipation: a pilot study. Arch Med Res 47:236–242PubMedCrossRefGoogle Scholar
  38. Gerding DN, Meyer T, Lee C, Cohen SH, Murthy UK, Poirier A, Van Schooneveld TC, Pardi DS, Ramos A, Barron MA, Chen H, Villano S (2015) Administration of spores of nontoxigenic Clostridium difficile strain M3 for prevention of recurrent C. difficile infection: a randomized clinical trial. JAMA 313:1719–1727PubMedCrossRefGoogle Scholar
  39. Ghantoji SS, Sail K, Lairson DR, Dupont HL, Garey KW (2010) Economic healthcare costs of Clostridium difficile infection: a systematic review. J Hosp Infect 74:309–318PubMedCrossRefGoogle Scholar
  40. Gupta A, Khanna S (2014) Community-acquired Clostridium difficile infection: an increasing public health threat. Infect Drug Resist 7:63–72PubMedPubMedCentralGoogle Scholar
  41. Hahn MM, De Voer RM, Hoogerbrugge N, Ligtenberg MJ, Kuiper RP, Van Kessel AG (2016) The genetic heterogeneity of colorectal cancer predisposition – guidelines for gene discovery. Cell Oncol (Dordr) 39:491–510CrossRefGoogle Scholar
  42. Hansen J, Gulati A, Sartor RB (2010) The role of mucosal immunity and host genetics in defining intestinal commensal bacteria. Curr Opin Gastroenterol 26:564–571PubMedPubMedCentralCrossRefGoogle Scholar
  43. HealthCanada (2016) Fecal microbiota therapy for Clostridium difficile infection: OHTAC recommendation [Online]. Available: [Accessed]
  44. HealthqualityOntario (2016) Fecal microbiota therapy for Clostridium difficile infection: OHTAC recommendation [Online]. Available: [Accessed]
  45. Hensgens MP, Goorhuis A, Dekkers OM, Van Benthem BH, Kuijper EJ (2013) All-cause and disease-specific mortality in hospitalized patients with Clostridium difficile infection: a multicenter cohort study. Clin Infect Dis 56:1108–1116PubMedCrossRefGoogle Scholar
  46. Hope ME, Hold GL, Kain R, El-Omar EM (2005) Sporadic colorectal cancer—role of the commensal microbiota. FEMS Microbiol Lett 244:1–7PubMedCrossRefGoogle Scholar
  47. IDSA (2016) Fecal microbiota transplantation: investigational new drug protocol [Online]. Available: [Accessed]
  48. Im GY, Modayil RJ, Lin CT, Geier SJ, Katz DS, Feuerman M, Grendell JH (2011) The appendix may protect against Clostridium difficile recurrence. Clin Gastroenterol Hepatol 9:1072–1077PubMedCrossRefGoogle Scholar
  49. Jeffery IB, O’Toole PW, Ohman L, Claesson MJ, Deane J, Quigley EM, Simren M (2012) An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut 61:997–1006PubMedCrossRefGoogle Scholar
  50. Kahn SA, Vachon A, Rodriquez D, Goeppinger S, Surma B, Marks J, Rubin DT (2013) Patient perceptions of fecal microbiota transplantation for ulcerative colitis. Inflamm Bowel Dis 19:1506–1513PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kao D, Hotte N, Gillevet P, Madsen K (2014) Fecal microbiota transplantation inducing remission in Crohn’s colitis and the associated changes in fecal microbial profile. J Clin Gastroenterol 48:625–628PubMedCrossRefGoogle Scholar
  52. Kassam Z, Lee CH, Yuan Y, Hunt RH (2013) Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol 108:500–508PubMedCrossRefGoogle Scholar
  53. Kelly CR, Ihunnah C, Fischer M, Khoruts A, Surawicz C, Afzali A, Aroniadis O, Barto A, Borody T, Giovanelli A, Gordon S, Gluck M, Hohmann EL, Kao D, Kao JY, McQuillen DP, Mellow M, Rank KM, Rao K, Ray A, Schwartz MA, Singh N, Stollman N, Suskind DL, Vindigni SM, Youngster I, Brandt L (2014) Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol 109:1065–1071PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kelly CR, Khoruts A, Staley C, Sadowsky MJ, Abd M, Alani M, Bakow B, Curran P, McKenney J, Tisch A, Reinert SE, Machan JT, Brandt LJ (2016) Effect of fecal microbiota transplantation on recurrence in multiply recurrent Clostridium difficile infection: a randomized trial. Ann Intern Med 165:609–616PubMedCrossRefGoogle Scholar
  55. Khanna S, Pardi DS, Kelly CR, Kraft CS, Dhere T, Henn MR, Lombardo MJ, Vulic M, Ohsumi T, Winkler J, Pindar C, McGovern BH, Pomerantz RJ, Aunins JG, Cook DN, Hohmann EL (2016) A novel microbiome therapeutic increases gut microbial diversity and prevents recurrent Clostridium difficile infection. J Infect Dis 214:173–181PubMedCrossRefGoogle Scholar
  56. Khoruts A, Rank KM, Newman KM, Viskocil K, Vaughn BP, Hamilton MJ, Sadowsky MJ (2016) Inflammatory bowel disease affects the outcome of fecal microbiota transplantation for recurrent Clostridium difficile infection. Clin Gastroenterol Hepatol 14:1433–1438PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, El-Omar EM, Brenner D, Fuchs CS, Meyerson M, Garrett WS (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14:207–215PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kump PK, Grochenig HP, Lackner S, Trajanoski S, Reicht G, Hoffmann KM, Deutschmann A, Wenzl HH, Petritsch W, Krejs GJ, Gorkiewicz G, Hogenauer C (2013) Alteration of intestinal dysbiosis by fecal microbiota transplantation does not induce remission in patients with chronic active ulcerative colitis. Inflamm Bowel Dis 19:2155–2165PubMedCrossRefGoogle Scholar
  59. Kyne L, Warny M, Qamar A, Kelly CP (2001) Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet 357:189–193PubMedCrossRefGoogle Scholar
  60. Lee CH, Steiner T, Petrof EO, Smieja M, Roscoe D, Nematallah A, Weese JS, Collins S, Moayyedi P, Crowther M, Ropeleski MJ, Jayaratne P, Higgins D, Li Y, Rau NV, Kim PT (2016) Frozen vs fresh fecal microbiota transplantation and clinical resolution of diarrhea in patients with recurrent Clostridium difficile infection: a randomized clinical trial. JAMA 315:142–149PubMedCrossRefGoogle Scholar
  61. Leong C, Zelenitsky S (2013) Treatment strategies for recurrent Clostridium difficile Infection. Can J Hosp Pharm 66:361–368PubMedPubMedCentralGoogle Scholar
  62. Lepage P, Hasler R, Spehlmann ME, Rehman A, Zvirbliene A, Begun A, Ott S, Kupcinskas L, Dore J, Raedler A, Schreiber S (2011) Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 141:227–236PubMedCrossRefGoogle Scholar
  63. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444:1022–1023PubMedCrossRefGoogle Scholar
  64. Li SS, Zhu A, Benes V, Costea PI, Hercog R, Hildebrand F, Huerta-Cepas J, Nieuwdorp M, Salojarvi J, Voigt AY, Zeller G, Sunagawa S, De Vos WM, Bork P (2016) Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science 352:586–589PubMedCrossRefGoogle Scholar
  65. Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K (2000) Environmental and heritable factors in the causation of cancer—analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med 343:78–85PubMedCrossRefGoogle Scholar
  66. Lin HV, Frassetto A, Kowalik EJ Jr, Nawrocki AR, Lu MM, Kosinski JR, Hubert JA, Szeto D, Yao X, Forrest G, Marsh DJ (2012) Butyrate and propionate protect against diet-induced obesity and regulate gut hormones via free fatty acid receptor 3-independent mechanisms. PLoS One:7, e35240Google Scholar
  67. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230PubMedPubMedCentralCrossRefGoogle Scholar
  68. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55:205–211PubMedPubMedCentralCrossRefGoogle Scholar
  69. McFarland LV, Elmer GW, Surawicz CM (2002) Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 97:1769–1775PubMedCrossRefGoogle Scholar
  70. Merenstein D, El-Nachef N, Lynch SV (2014) Fecal microbial therapy: promises and pitfalls. J Pediatr Gastroenterol Nutr 59:157–161PubMedPubMedCentralCrossRefGoogle Scholar
  71. Moayyedi P, Surette MG, Kim PT, Libertucci J, Wolfe M, Onischi C, Armstrong D, Marshall JK, Kassam Z, Reinisch W, Lee CH (2015) Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149:102–109.e6PubMedCrossRefGoogle Scholar
  72. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, Leleiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C (2012) Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13:R79PubMedPubMedCentralCrossRefGoogle Scholar
  73. Nugent JL, McCoy AN, Addamo CJ, Jia W, Sandler RS, Keku TO (2014) Altered tissue metabolites correlate with microbial dysbiosis in colorectal adenomas. J Proteome Res 13:1921–1929PubMedPubMedCentralCrossRefGoogle Scholar
  74. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Folsch UR, Timmis KN, Schreiber S (2004) Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 53:685–693PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ott SJ, Plamondon S, Hart A, Begun A, Rehman A, Kamm MA, Schreiber S (2008) Dynamics of the mucosa-associated flora in ulcerative colitis patients during remission and clinical relapse. J Clin Microbiol 46:3510–3513PubMedPubMedCentralCrossRefGoogle Scholar
  76. Paramsothy SEA (2016) Multi donor intense faecal microbiota transplantation is an effective treatment for resistant ulcerative colitis: a randomised placebo-controlled trial. Gastroenterology 150:s122–s123CrossRefGoogle Scholar
  77. Peng Z, Xiang J, He Z, Zhang T, Xu L, Cui B, Li P, Huang G, Ji G, Nie Y, Wu K, Fan D, Zhang F (2016) Colonic transendoscopic enteral tubing: a novel way of transplanting fecal microbiota. Endosc Int Open 4:E610–E613PubMedPubMedCentralCrossRefGoogle Scholar
  78. Petrof EO, Gloor GB, Vanner SJ, Weese SJ, Carter D, Daigneault MC, Brown EM, Schroeter K, Allen-Vercoe E (2013) Stool substitute transplant therapy for the eradication of Clostridium difficile infection: ‘RePOOPulating’ the gut. Microbiome 1:3PubMedPubMedCentralCrossRefGoogle Scholar
  79. Pinn DM, Aroniadis OC, Brandt LJ (2014) Is fecal microbiota transplantation the answer for irritable bowel syndrome? A single-center experience. Am J Gastroenterol 109:1831–1832PubMedCrossRefGoogle Scholar
  80. Preidis GA, Versalovic J (2009) Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 136:2015–2031PubMedPubMedCentralCrossRefGoogle Scholar
  81. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, Meta HITC, Bork P, Ehrlich SD, Wang J (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65PubMedPubMedCentralCrossRefGoogle Scholar
  82. Quera R, Espinoza R, Estay C, Rivera D (2014) Bacteremia as an adverse event of fecal microbiota transplantation in a patient with Crohn’s disease and recurrent Clostridium difficile infection. J Crohns Colitis 8:252–253PubMedCrossRefGoogle Scholar
  83. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, Griffin NW, Lombard V, Henrissat B, Bain JR, Muehlbauer MJ, Ilkayeva O, Semenkovich CF, Funai K, Hayashi DK, Lyle BJ, Martini MC, Ursell LK, Clemente JC, Van Treuren W, Walters WA, Knight R, Newgard CB, Heath AC, Gordon JI (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214PubMedCrossRefGoogle Scholar
  84. Rossen NG, Fuentes S, Van der Spek MJ, Tijssen JG, Hartman JH, Duflou A, Lowenberg M, Van den Brink GR, Mathus-Vliegen EM, De Vos WM, Zoetendal EG, D’Haens GR, Ponsioen CY (2015) Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 149:110–118.e4PubMedCrossRefGoogle Scholar
  85. Sandler RS, Everhart JE, Donowitz M, Adams E, Cronin K, Goodman C, Gemmen E, Shah S, Avdic A, Rubin R (2002) The burden of selected digestive diseases in the United States. Gastroenterology 122:1500–1511PubMedCrossRefGoogle Scholar
  86. Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134:577–594PubMedCrossRefGoogle Scholar
  87. Schwartz M, Gluck M, Koon S (2013) Norovirus gastroenteritis after fecal microbiota transplantation for treatment of Clostridium difficile infection despite asymptomatic donors and lack of sick contacts. Am J Gastroenterol 108:1367PubMedCrossRefGoogle Scholar
  88. Seekatz AM, Aas J, Gessert CE, Rubin TA, Saman DM, Bakken JS, Young VB (2014) Recovery of the gut microbiome following fecal microbiota transplantation. MBio 5:e00893–e00814PubMedPubMedCentralCrossRefGoogle Scholar
  89. Shi Y, Dong Y, Huang W, Zhu D, Mao H, Su P (2016) Fecal microbiota transplantation for ulcerative colitis: a systematic review and meta-analysis. PLoS One 11:e0157259PubMedPubMedCentralCrossRefGoogle Scholar
  90. Sobhani I, Tap J, Roudot-Thoraval F, Roperch JP, Letulle S, Langella P, Corthier G, Tran Van Nhieu J, Furet JP (2011) Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One 6:e16393PubMedPubMedCentralCrossRefGoogle Scholar
  91. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105:16731–16736PubMedPubMedCentralCrossRefGoogle Scholar
  92. Song LL, Li YM (2016) Current noninvasive tests for colorectal cancer screening: an overview of colorectal cancer screening tests. World J Gastrointest Oncol 8:793–800PubMedPubMedCentralCrossRefGoogle Scholar
  93. Surawicz CM, McFarland LV, Greenberg RN, Rubin M, Fekety R, Mulligan ME, Garcia RJ, Brandmarker S, Bowen K, Borjal D, Elmer GW (2000) The search for a better treatment for recurrent Clostridium difficile disease: use of high-dose vancomycin combined with Saccharomyces boulardii. Clin Infect Dis 31:1012–1017PubMedCrossRefGoogle Scholar
  94. Surawicz CM, Brandt LJ, Binion DG, Ananthakrishnan AN, Curry SR, Gilligan PH, McFarland LV, Mellow M, Zuckerbraun BS (2013) Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 108:478–498. quiz 499PubMedCrossRefGoogle Scholar
  95. Suskind DL, Brittnacher MJ, Wahbeh G, Shaffer ML, Hayden HS, Qin X, Singh N, Damman CJ, Hager KR, Nielson H, Miller SI (2015) Fecal microbial transplant effect on clinical outcomes and fecal microbiome in active Crohn’s disease. Inflamm Bowel Dis 21:556–563PubMedPubMedCentralCrossRefGoogle Scholar
  96. Theriot CM, Koenigsknecht MJ, Carlson PE Jr, Hatton GE, Nelson AM, Li B, Huffnagle GB, Li JZ, Young VB (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5:3114PubMedPubMedCentralCrossRefGoogle Scholar
  97. Tjalsma H, Boleij A, Marchesi JR, Dutilh BE (2012) A bacterial driver-passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol 10:575–582PubMedCrossRefGoogle Scholar
  98. Tojo R, Suarez A, Clemente MG, De Los Reyes-Gavilan CG, Margolles A, Gueimonde M, Ruas-Madiedo P (2014) Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J Gastroenterol 20:15163–15176PubMedPubMedCentralCrossRefGoogle Scholar
  99. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027–1031PubMedCrossRefGoogle Scholar
  100. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484PubMedCrossRefGoogle Scholar
  101. Tvede M, Rask-Madsen J (1989) Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet 1:1156–1160PubMedCrossRefGoogle Scholar
  102. Van Nood E, Vrieze A, Nieuwdorp M, Fuentes S, Zoetendal EG, De Vos WM, Visser CE, Kuijper EJ, Bartelsman JF, Tijssen JG, Speelman P, Dijkgraaf MG, Keller JJ (2013) Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med 368:407–415PubMedCrossRefGoogle Scholar
  103. Varela E, Manichanh C, Gallart M, Torrejon A, Borruel N, Casellas F, Guarner F, Antolin M (2013) Colonisation by Faecalibacterium prausnitzii and maintenance of clinical remission in patients with ulcerative colitis. Aliment Pharmacol Ther 38:151–161PubMedCrossRefGoogle Scholar
  104. Villanueva-Millan MJ, Perez-Matute P, Oteo JA (2015) Gut microbiota: a key player in health and disease. A review focused on obesity. J Physiol Biochem 71:509–525PubMedCrossRefGoogle Scholar
  105. Vipperla K, O’Keefe SJ (2016) Diet, microbiota, and dysbiosis: a ‘recipe’ for colorectal cancer. Food Funct 7:1731–1740PubMedCrossRefGoogle Scholar
  106. Vrieze A, Van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, Dallinga-Thie GM, Ackermans MT, Serlie MJ, Oozeer R, Derrien M, Druesne A, Van Hylckama Vlieg JE, Bloks VW, Groen AK, Heilig HG, Zoetendal EG, Stroes ES, De Vos WM, Hoekstra JB, Nieuwdorp M (2012) Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143:913–916.e7PubMedCrossRefGoogle Scholar
  107. Wilcox MH, Mooney L, Bendall R, Settle CD, Fawley WN (2008) A case-control study of community-associated Clostridium difficile infection. J Antimicrob Chemother 62:388–396PubMedCrossRefGoogle Scholar
  108. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Jarnerot G, Tysk C, Jansson JK, Engstrand L (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139:1844–1854.e1PubMedCrossRefGoogle Scholar
  109. Wu N, Yang X, Zhang R, Li J, Xiao X, Hu Y, Chen Y, Yang F, Lu N, Wang Z, Luan C, Liu Y, Wang B, Xiang C, Wang Y, Zhao F, Gao GF, Wang S, Li L, Zhang H, Zhu B (2013) Dysbiosis signature of fecal microbiota in colorectal cancer patients. Microb Ecol 66:462–470PubMedCrossRefGoogle Scholar
  110. Xu L, Zhang T, Cui B, He Z, Xiang J, Long C, Peng Z, Li P, Huang G, Ji G, Zhang F (2016) Clinical efficacy maintains patients’ positive attitudes toward fecal microbiota transplantation. Medicine (Baltimore) 95:e4055CrossRefGoogle Scholar
  111. Youngster I, Sauk J, Pindar C, Wilson RG, Kaplan JL, Smith MB, Alm EJ, Gevers D, Russell GH, Hohmann EL (2014) 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 58:1515–1522PubMedPubMedCentralCrossRefGoogle Scholar
  112. Youngster I, Mahabamunuge J, Systrom HK, Sauk J, Khalili H, Levin J, Kaplan JL, Hohmann EL (2016) Oral, frozen fecal microbiota transplant (FMT) capsules for recurrent Clostridium difficile infection. BMC Med 14:134PubMedPubMedCentralCrossRefGoogle Scholar
  113. Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, Schloss PD (2013) The gut microbiome modulates colon tumorigenesis. MBio 4:e00692-13PubMedPubMedCentralCrossRefGoogle Scholar
  114. Zenlea T, Peppercorn MA (2014) Immunosuppressive therapies for inflammatory bowel disease. World J Gastroenterol 20:3146–3152PubMedPubMedCentralCrossRefGoogle Scholar
  115. Zhang F, Luo W, Shi Y, Fan Z, Ji G (2012) Should we standardize the 1,700-year-old fecal microbiota transplantation? Am J Gastroenterol 107:1755–1756PubMedCrossRefGoogle Scholar
  116. Zhang YZ, Li YY (2014) Inflammatory bowel disease: pathogenesis. World J Gastroenterol 20:91–99PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zipursky JS, Sidorsky TI, Freedman CA, Sidorsky MN, Kirkland KB (2014) Physician attitudes toward the use of fecal microbiota transplantation for the treatment of recurrent Clostridium difficile infection. Can J Gastroenterol Hepatol 28:319–324PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© The American Physiological Society 2018

Authors and Affiliations

  • Roxana Chis
    • 1
  • Prameet M. Sheth
    • 2
  • Elaine O. Petrof
    • 3
    Email author
  1. 1.Department of Internal Medicine, Kingston General HospitalQueen’s UniversityKingstonCanada
  2. 2.Department of Pathology and Molecular Medicine, Kingston General HospitalQueen’s UniversityKingstonCanada
  3. 3.Division of Infectious Diseases/GI Diseases Research Unit, Department of Medicine, Kingston General HospitalQueen’s UniversityKingstonCanada

Personalised recommendations