Intestinal microbiota and the efficacy of fecal microbiota transplantation in gastrointestinal disease

Gastroenterology and Hepatology

Volumn 10, Issue 4, 2014, Pages 230-237

  Aroniadis, Olga C ^a   Brandt, Lawrence J ^a,b  

^a MONTEFIORE MEDICAL CENTER   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Clostridium difficile; Fecal microbiota transplantation; Inflammatory bowel disease; Irritable bowel syndrome

Indexed keywords

CLINICAL OBSERVATION; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; FECAL MICROBIOTA TRANSPLANTATION; FECES; FECES MICROFLORA; GASTROINTESTINAL DISEASE; GASTROINTESTINAL TRACT; HOMEOSTASIS; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; IRRITABLE COLON; MICROBIOME; MICROORGANISM; NONHUMAN; RECURRENT INFECTION; REVIEW; SAFETY; TRANSPLANTATION;

EID: 84901624964     PISSN: 15547914     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. Zhang F, Luo W, Shi Y, Fan Z, Ji G. Should we standardize the 1,700-year-old fecal microbiota transplantation? Am J Gastroenterol. 2012;107(11):1755, author reply 1755-1756.
2. Borody TJ, Warren EF, Leis SM, Surace R, Ashman O, Siarakas S. Bacteriotherapy using fecal flora: toying with human motions. J Clin Gastroenterol. 2004;38(6):475-483. (Pubitemid 38808419)
3. Eiseman B, Silen W, Bascom GS, Kauvar AJ. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery. 1958;44(5):854-859.
4. Schwan A, Sjolin S, Trottestam U, Aronsson B. Relapsing Clostridium difficile enterocolitis cured by rectal infusion of homologous faeces. Lancet. 1983;2(8354):845.
5. Bakken JS, Borody T, Brandt LJ, et al Fecal Microbiota Transplantation Workgroup. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9(12):1044-1049.
6. Aas J, Gessert CE, Bakken JS. Recurrent Clostridium difficile colitis: case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin Infect Dis. 2003;36(5):580-585. (Pubitemid 36259562)
7. Persky SE, Brandt LJ. Treatment of recurrent Clostridium difficile-associated diarrhea by administration of donated stool directly through a colonoscope. Am J Gastroenterol. 2000;95(11):3283-3285.
8. Silverman MS, Davis I, Pillai DR. Success of self-administered home fecal transplantation for chronic Clostridium difficile infection. Clin Gastroenterol Hepatol. 2010;8(5):471-473.
9. Brandt LJ, Reddy SS. Fecal microbiota transplantation for recurrent Clostridium difficile infection. J Clin Gastroenterol. 2011;45(suppl):S159-S167.
10. 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.
11. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859-904.
12. Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635-1638. (Pubitemid 40807514)
13. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837-848. (Pubitemid 43261456)
14. Brandt LJ. American Journal of Gastroenterology Lecture: intestinal microbiota and the role of fecal microbiota transplant (FMT) in treatment of C. difficile infection. Am J Gastroenterol. 2013;108(2):177-185.
15. Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol. 2013;13(5):321-335.
16. Momose Y, Hirayama K, Itoh K. Competition for proline between indigenous Escherichia coli and E. coli O157:H7 in gnotobiotic mice associated with infant intestinal microbiota and its contribution to the colonization resistance against E. coli O157:H7. Antonie Van Leeuwenhoek. 2008;94(2):165-171.
17. Leatham MP, Banerjee S, Autieri SM, Mercado-Lubo R, Conway T, Cohen PS. Precolonized human commensal Escherichia coli strains serve as a barrier to E. coli O157:H7 growth in the streptomycin-treated mouse intestine. Infect Immun. 2009;77(7):2876-2886.
18. Kamada N, Kim YG, Sham HP, et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science. 2012;336(6086):1325-1329.
19. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A. 2008;105(39):15064-15069.
20. Bergstrom KS, Kissoon-Singh V, Gibson DL, et al. Muc2 protects against lethal infectious colitis by disassociating pathogenic and commensal bacteria from the colonic mucosa. PLoS Pathog. 2010;6(5):e1000902.
21. Petersson J, Schreiber O, Hansson GC, et al. Importance and regulation of the colonic mucus barrier in a mouse model of colitis. Am J Physiol Gastrointest Liver Physiol. 2011;300(2):G327-G333.
22. Fukuda S, Toh H, Hase K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature. 2011;469(7331):543-547.
23. Satoh-Takayama N, Vosshenrich CA, Lesjean-Pottier S, et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity. 2008;29(6):958-970.
24. Franchi L, Kamada N, Nakamura Y, et al. NLRC4-driven production of IL-1•• discriminates between pathogenic and commensal bacteria and promotes host intestinal defense. Nat Immunol. 2012;13(5):449-456.
25. Zeuthen LH, Fink LN, Frokiaer H. Epithelial cells prime the immune response to an array of gut-derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor-beta. Immunology. 2008;123(2):197-208.
26. Kelly D, Campbell JI, King TP, et al. Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol. 2004;5(1):104-112. (Pubitemid 38081475)
27. Bates JM, Akerlund J, Mittge E, Guillemin K. Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe. 2007;2(6):371-382. (Pubitemid 350215326)
28. Chang JY, Antonopoulos DA, Kalra A, et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197(3):435-438. (Pubitemid 351263426)
29. Kyne L, Farrell RJ, Kelly CP. Clostridium difficile. Gastroenterol Clin North Am. 2001;30(3):753-777, ix-x. (Pubitemid 32880451)
30. Grehan MJ, Borody TJ, Leis SM, Campbell J, Mitchell H, Wettstein A. Durable alteration of the colonic microbiota by the administration of donor fecal flora. J Clin Gastroenterol. 2010;44(8):551-561.
31. Hamilton MJ, Weingarden AR, Unno T, Khoruts A, Sadowsky MJ. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes. 2013;4(2):125-135.
32. 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.
33. Khoruts A. Why could fecal transplantation be effective? Presented at: Digestive Disease Week; Orlando, FL; May 19-21, 2013.
34. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996-2003. Emerg Infect Dis. 2006;12(3):409-415.
35. Zilberberg MD, Shorr AF, Kollef MH. Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000-2005. Emerg Infect Dis. 2008;14(6):929-931. (Pubitemid 351838602)
36. Cohen SH, Gerding DN, Johnson S, et al Society for Healthcare Epidemiology of America; Infectious Diseases Society of America. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31(5):431-455.
37. 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; quiz 499.
38. Bakken JS. Fecal bacteriotherapy for recurrent Clostridium difficile infection. Anaerobe. 2009;15(6):285-289.
39. Lund-Tønnesen S, Berstad A, Schreiner A, Midtvedt T. Clostridium difficile-associated diarrhea treated with homologous feces [in Norwegian]. Tidsskr Nor Laegeforen. 1998;118(7):1027-1030. (Pubitemid 28135942)
40. Huebner ES, Surawicz CM. Treatment of recurrent Clostrium difficile diarrrhea. Gastroenterol Hepatol. 2006;2(3):203-208. (Pubitemid 46050747)
41. Yoon SS, Brandt LJ. Treatment of refractory/recurrent C. difficile-associated disease by donated stool transplanted via colonoscopy: a case series of 12 patients. J Clin Gastroenterol. 2010;44(8):562-566.
42. Rohlke F, Surawicz CM, Stollman N. Fecal flora reconstitution for recurrent Clostridium difficile infection: results and methodology. J Clin Gastroenterol. 2010;44(8):567-570.
43. MacConnachie AA, Fox R, Kennedy DR, Seaton RA. Faecal transplant for recurrent Clostridium difficile-associated diarrhoea: a UK case series. QJM. 2009;102(11):781-784.
44. Rubin TA, Gessert CE, Aas J. Stool transplantation for older patients with Clostridium difficile infection. J Am Geriatr Soc. 2009;57(12):2386-2387.
45. Russell G, Kaplan J, Ferraro M, Michelow IC. Fecal bacteriotherapy for relapsing Clostridium difficile infection in a child: a proposed treatment protocol. Pediatrics. 2010;126(1):e239-e242.
46. Tvede M, Rask-Madsen J. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet. 1989;1(8648):1156-1160. (Pubitemid 19138849)
47. Paterson DL, Iredell J, Whitby M. Putting back the bugs: bacterial treatment relieves chronic diarrhoea. Med J Aust. 1994;160(4):232-233. (Pubitemid 24057461)
48. You DM, Franzos MA, Holman RP. Successful treatment of fulminant Clostridium difficile infection with fecal bacteriotherapy. Ann Intern Med. 2008;148(8):632-633. (Pubitemid 351669152)
49. Kassam Z, Hundal R, Marshall JK, Lee CH. Fecal transplantation via retention enemas is effective for recurrent or refractory Clostridium difficile-associated diarrhea. Gastroenterology. 2010;138(5):S207-S208.
50. Sofi A, Nawras A, Sodeman T, et al. Fecal bacteriotherapy works for Clostridium difficile infection: a meta-analysis. Presented at: American College of Gastroenterology Annual Meeting; Washington, DC; October 28-November 2, 2011.
51. 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.
52. Aroniadis OC, Brandt LJ, Greenberg A, et al. Long-term follow-up study of fecal microbiota transplantation (FMT) for severe or complicated Clostridium difficile infection (CDI). Gastroenterology. 2013;144(5):S185.
53. Kamada N, Hisamatsu T, Okamoto S, et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J Clin Invest. 2008;118(6):2269-2280. (Pubitemid 351872344)
54. Sartor RB, Mazmanian SK. Intestinal microbes in inflammatory bowel disease. Am J Gastroenterol Suppl. 2012;1(1):15-21.
55. Sokol H, Seksik P, Furet JP, et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009;15(8):1183-1189.
56. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34):13780-13785. (Pubitemid 350003397)
57. Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics and new diagnoses of Crohn's disease and ulcerative colitis. Am J Gastroenterol. 2011;106(12):2133-2142.
58. Borody TJ, Leis S, McGrath K, et al. Treatment of chronic constipation and colitis using human probiotic infusions. Presented at: Probiotics, Prebiotics and New Foods Conference; Rome, Italy; September 2-4, 2001.
59. Borody TJ, Warren EF, Leis S, Surace R, Ashman O. Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol. 2003;37(1):42-47. (Pubitemid 36734332)
60. Borody TJ, George L, Andrews P, et al. Bowel-flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome? Med J Aust. 1989;150(10):604.
61. Greenberg A, Aroniadis O, Shelton C, Brandt LJ. Long-term follow-up study of fecal microbiota transplantation (FMT) for inflammatory bowel disease. Am J Gastroenterol. 2013;108(suppl 1):A1791.
62. Ringel Y, Maharshak N. Intestinal microbiota and immune function in the pathogenesis of irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2013;305(8):G529-G541.
63. Bercik P, Wang L, Verdu EF, et al. Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology. 2004;127(1):179-187. (Pubitemid 38962286)
64. Caenepeel P, Janssens J, Vantrappen G, Eyssen H, Coremans G. Interdigestive myoelectric complex in germ-free rats. Dig Dis Sci. 1989;34(8):1180-1184. (Pubitemid 19202111)
65. Collins S, Verdu E, Denou E, Bercik P. The role of pathogenic microbes and commensal bacteria in irritable bowel syndrome. Dig Dis . 2009;27(suppl 1):85-89.
66. Dunlop SP, Jenkins D, Neal KR, Spiller RC. Relative importance of enterochromaffin cell hyperplasia, anxiety, and depression in postinfectious IBS. Gastroenterology. 2003;125(6):1651-1659. (Pubitemid 37500429)
67. Collins SM, Chang C, Mearin F. Postinfectious chronic gut dysfunction: from bench to bedside. Am J Gastroenterol Suppl. 2012;1(1):2-8.
68. Ringel Y, Quigley EMM, Lin H. Using probiotics in gastrointestinal disorders. Am J Gastroenterol Suppl. 2012;1(1):34-40.
69. Halvorson HA, Schlett CD, Riddle MS. Postinfectious irritable bowel syndrome - a meta-analysis. Am J Gastroenterol. 2006;101(8):1894-1899, quiz 1942.
70. Schwille-Kiuntke J, Enck P, Zendler C, et al. Postinfectious irritable bowel syndrome: follow-up of a patient cohort of confirmed cases of bacterial infection with Salmonella or Campylobacter. Neurogastroenterol Motil. 2011;23(11):e479-e488.
71. Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26(4):535-544. (Pubitemid 47174284)
72. Pimentel M, Chang C, Lembo A, et al. Anti-vinculin antibodies: multicenter validation of diagnostic blood test for irritable bowel syndrome (IBS). Am J Gastroenterol. 2013;108(suppl 1):A1887.
73. Pimentel M, Soffer EE, Chow EJ, Kong Y, Lin HC. Lower frequency of MMC is found in IBS subjects with abnormal lactulose breath test, suggesting bacterial overgrowth. Dig Dis Sci. 2002;47(12):2639-2643. (Pubitemid 35471599)
74. Salonen A, de Vos WM, Palva A. Gastrointestinal microbiota in irritable bowel syndrome: present state and perspectives. Microbiology. 2010;156(pt 11):3205-3215.
75. Ringel Y, Carroll IM. Alterations in the intestinal microbiota and functional bowel symptoms. Gastrointest Endosc Clin N Am. 2009;19(1):141-150, vii.
76. Chassard C, Dapoigny M, Scott KP, et al. Functional dysbiosis within the gut microbiota of patients with constipated-irritable bowel syndrome. Aliment Pharmacol Ther. 2012;35(7):828-838.
77. Kim G, Deepinder F, Morales W, et al. Methanobrevibacter smithii is the predominant methanogen in patients with constipation-predominant IBS and methane on breath. Dig Dis Sci. 2012;57(12):3213-3218.
78. Foxx-Orenstein AE, Chey W. Manipulation of the gut microbiota as a novel treatment strategy for gastrointestinal disorders. Am J Gastroenterol Suppl. 2012;1(1):41-46.
79. Andrews P, Borody TJ, Shortis NP, Thompson S. Bacteriotherapy for chronic constipation - long term follow-up. Gastroenterology. 1995;108(4):A563.
80. Pinn DM, Aroniadis OC, Brandt LJ. Follow-up study of fecal microbiota transplantation (FMT) for the treatment of refractory irritable bowel syndrome (IBS). Presented at: American College of Gastroenterology Annual Meeting; San Diego, CA; October 11-16, 2013.
81. Ihunnah C, Kelly C, Hohmann E, et al. Fecal microbiota transplantation (FMT) for treatment of Clostridium difficile infection (CDI) in immunocompromised patients. Am J Gastroenterol. 2013;108(2):S179.
82. Brandt LJ, Aroniadis OC, Greenberg A, et al. Safety of fecal microbiota transplantation (FMT) in immunocompromised (Ic) patients with inflammatory bowel disease (IBD). Am J Gastroenterol. 2013;108(suppl 1):A1840.
83. Lawley TD, Clare S, Walker AW, et al. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice. PLoS Pathog. 2012;8(10):e1002995.
84. 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):1-12.
85. Graham D, Attumi T, Opekun A, et al. Triple Bacteriodes fecal replacement therapy for relapsing Clostridium difficile diarrhea (fecal transplantation sans feces). Am J Gastroenterol. 2013;108(2):S170.
86. Louie T, Cannon K, O'Grady H, et al. Fecal microbiome transplantation (FMT) via oral fecal microbial capsules for recurrent Clostridium difficile infection (rCDI). Presented at: ID Week; San Francisco, CA; October 2-6, 2013.