The microbiome and inflammatory bowel disease: Is there a therapeutic role for fecal microbiota transplantation

American Journal of Gastroenterology

Volumn 107, Issue 10, 2012, Pages 1452-1459

  Damman, Christopher J ^a   Miller, Samuel I ^b   Surawicz, Christina M ^a   Zisman, Timothy L ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOSALICYLIC ACID; ANTIBIOTIC AGENT; AZATHIOPRINE; CYCLOSPORIN; ENEMA; MACROGOL; MESALAZINE; METRONIDAZOLE; PREDNISONE; PROBIOTIC AGENT; RIFAMPICIN; STEROID; SULFALAZINE; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTEROIDES FRAGILIS; CAMPYLOBACTER; CLINICAL EFFECTIVENESS; CLINICAL TRIAL (TOPIC); CLOSTRIDIUM DIFFICILE INFECTION; CROHN DISEASE; ENTERITIS; ESCHERICHIA COLI; FAECALIBACTERIUM PRAUSNITZII; FAUNA; FECES MICROFLORA; FECES MICROFLORA THERAPY; FIRMICUTES; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HUMAN; MICROBIOME; MYCOBACTERIUM AVIUM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); THERAPY; ULCERATIVE COLITIS; UNSPECIFIED SIDE EFFECT;

ANIMALS; DISEASE MODELS, ANIMAL; ENEMA; FECES; GASTROINTESTINAL TRACT; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMATORY BOWEL DISEASES; LIVING DONORS; METAGENOME; MICE; PROBIOTICS; TRANSPLANTATION; TREATMENT OUTCOME;

EID: 84867057848     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2012.93     Document Type: Article

References (102)

1. Turnbaugh PJ, Ley RE, Hamady M et al. The human microbiome project. Nature 2007;449:804-10.
2. Proctor LM. The Human Microbiome Project in 2011 and beyond. Cell Host Microbe 2011;10:287-91.
3. Gill SR, Pop M, Deboy RT et al. Metagenomic analysis of the human distal gut microbiome. Science 2006;312:1355-9.
4. Qin J, Li R, Raes J et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65.
5. Bäckhed F, Ley RE, Sonnenburg JL et al. Host-bacterial mutualism in the human intestine. Science 2005;307:1915-20.
6. Eckburg PB, Bik EM, Bernstein CN et al. Diversity of the human intestinal microbial flora. Science 2005;308:1635-8.
7. Ley RE, Bäckhed F, Turnbaugh P et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005;102:11070-5.
8. Dinis JM, Barton DE, Ghadiri J et al. In search of an uncultured humanassociated TM7 bacterium in the environment. PLoS One [online] 2011;6:e21280.
9. Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 2008;57:1605-15.
10. Tap J, Mondot S, Levenez F et al. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 2009;11:2574-84.
11. Turnbaugh PJ, Hamady M, Yatsunenko T et al. A core gut microbiome in obese and lean twins. Nature 2009;457:480-4.
12. Arumugam M, Raes J, Pelletier E et al. Enterotypes of the human gut microbiome. Nature 2011;473:174-80.
13. Wu GD, Chen J, Hoffmann C et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105-8.
14. Spor A, Koren O, Ley RE. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 2011;9:279-90.
15. Palmer C, Bik EM, DiGiulio DB et al. Development of the human infant intestinal microbiota. PLoS Biol [online] 2007;5:e177.
16. Marques TM, Wall R, Ross RP et al. Programming infant gut microbiota: influence of dietary and environmental factors. Curr Opin Biotechnol 2010;21:149-56.
17. Mariat D, Firmesse O, Levenez F et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol [online] 2009;9:123.
18. Turnbaugh PJ, Ridaura VK, Faith JJ et al. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Science Transl Med 2009;1:6ra14, doi:10.1126/scitranslmed.3000322.
19. Willing BP, Russell SL, Finlay BB. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nature Rev Microbiol 2011;9:233-43.
20. Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci USA 2011;108(Suppl):4554-61.
21. Costello EK, Lauber CL, Hamady M et al. Bacterial community variation in human body habitats across space and time. Science 2009;326:1694-7.
22. Sekirov I, Russell SL, Antunes LCM et al. Gut microbiota in health and disease. Physiol Rev 2010;90:859-904.
23. Penders J, Stobberingh EE, van den Brandt PA et al. The role of the intestinal microbiota in the development of atopic disorders. Allergy 2007;62:1223-36.
24. McLoughlin RM, Mills KHG. Influence of gastrointestinal commensal bacteria on the immune responses that mediate allergy and asthma. J Allergy Clin Immunol 2011;127:1097-1107.
25. Kau AL, Ahern PP, Griffin NW et al. Human nutrition, the gut microbiome and the immune system. Nature 2011;474:327-36.
26. Kootte RS, Vrieze A, Holleman F et al. Thetherapeutic potential of manipulating gut microbiota in obesity and type 2 diabetes mellitus. Diabetes Obes Metab 2012;14:112-20.
27. Arthur JC, Jobin C. The struggle within: microbial influences on colorectal cancer. Inflamm Bowel Dis 2011;17:396-409.
28. Greer JB, O'Keefe SJ. Microbial induction of immunity, inflammation, and cancer. Front Physiol 2011;1:168.
29. Wardwell LH, Huttenhower C, Garrett WS. Current concepts of the intestinal microbiota and the pathogenesis of infection. Curr Infect Dis Rep 2011;13:28-34.
30. Salonen A, de Vos WM, Palva A. Gastrointestinal microbiota in irritable bowel syndrome: present state and perspectives. Microbiology 2010;156:3205-15.
31. Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 2012;18:968-84.
32. Tannock GW. The bowel microbiota and inflammatory bowel diseases. Int J Inflam [online] 2010;2010:954051.
33. Sartor RB. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008;134:577-94.
34. Metzker ML. Sequencing technologies: the next generation. Nature Rev Genet 2010;11:31-46.
35. Rajili-Stojanovi M, Smidt H, de Vos WM. Diversity of the human gastrointestinal tract microbiota revisited. Environ Microbiol 2007;9:2125-36.
36. Kuczynski J, Lauber CL, Walters WA et al. Experimental and analytical tools for studying the human microbiome. Nat Rev Genet 2011;13:47-58.
37. Faith JJ, Rey FE, O'Donnell D et al. Creating and characterizing communities of human gut microbes in gnotobiotic mice. ISME J 2010;4:1094-8.
38. Liévin-Le Moal V, Servin AL. Potential mechanisms of enteric cytoprotection by probiotics: lessons from cultured human intestinal cells. In: Malago JJ, Koninkx JFJG, Marinsek-Logar R et al. (eds). Probiotic Bacteria and Enteric Infections. Springer: The Netherlands, 2011, pp 375-97.
39. Lakhdari O, Tap J, Béguet-Crespel F et al. Identification of NF-?B modulation capabilities within human intestinal commensal bacteria. J Biomed Biotechnol 2011;2011:282356, doi:10.1155/2011/282356.
40. Reading NC, Kasper DL. The starting lineup: key microbial players in intestinal immunity and homeostasis. Front Microbiol 2011;2:148.
41. Young VB, Britton RA, Schmidt TM. The human microbiome and infectious diseases: beyond Koch. Interdiscip Perspect Infect Dis 2008;2008:296873, doi:10.1155/2008/296873.
42. Kappelman MD, Rifas-Shiman SL, Kleinman K et al. The prevalence and geographic distribution of Crohn's disease and ulcerative colitis in the United States. Clin Gastroenterol Hepatol 2007;5:1424-9.
43. Halme L, Paavola-Sakki P, Turunen U et al. Family and twin studies in inflammatory bowel disease. World J Gastroenterol 2006;12:3668-72.
44. Cho JH, Brant SR. Recent insights into the genetics of inflammatory bowel disease. Gastroenterology 2011;140:1704-12.
45. Cho JH. The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 2008;8:458-66.
46. Anderson CA, Boucher G, Lees CW et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet 2011;43:246-52.
47. Franke A, McGovern DPB, Barrett JC et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet 2010;42:1118-25.
48. Talley NJ, Abreu MT, Achkar J-P et al. An evidence-based systematic review on medical therapies for inflammatory bowel disease. Am J Gastroenterol 2011;106(Suppl):S2-25.
49. Saleh M, Elson CO. Experimental inflammatory bowel disease: insights into the host-microbiota dialog. Immunity 2011;34:293-302.
50. Nell S, Suerbaum S, Josenhans C. The impact of the microbiota on the pathogenesis of IBD: lessons from mouse infection models. Nat Rev Microbiol 2010;8:564-77.
51. Rutgeerts P, Peeters M, Hiele M et al. Effect of faecal stream diversion on recurrence of Crohn's disease in the neoterminal ileum. Lancet 1991;338:771-4.
52. Meijer BJ, Dieleman LA. Probiotics in thetreatment of human inflammatory bowel diseases: update 2011. J Clin Gastroenterol 2011;45(Suppl):S139-44.
53. Guslandi M. Rifaximin in thetreatment of inflammatory bowel disease. World J Gastroenterology 2011;17:4643-6.
54. Ohkusa T, Kato K, Terao S et al. Newly developed antibiotic combination therapy for ulcerative colitis: a double-blind placebo-controlled multicenter trial. Am J Gastroenterol 2010;105:1820-9.
55. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 2004;126:1620-33.
56. Khan KJ, Ullman TA, Ford AC et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol 2011;106:661-73.
57. Frank DN, St Amand AL, Feldman RA et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007;104:13780-5.
58. Mann EA, Saeed SA. Gastrointestinal infection as a trigger for inflammatory bowel disease. Curr Opin Gastroenterol 2011;28:24-9.
59. Chassaing B, Darfeuille-Michaud A. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology 2011;140:1720-8.
60. Swidsinski A, Loening-Baucke V, Verstraelen H et al. Biostructure of fecal microbiota in healthy subjects and patients with chronic idiopathic diarrhea. Gastroenterology 2008;135:568-79.
61. Swidsinski A, Loening-Baucke V, Vaneechoutte M et al. Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm Bowel Dis 2008;14:147-61.
62. Round JL, Lee SM, Li J et al. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011;332:974-7.
63. Atarashi K, Tanoue T, Shima T et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011;331:337-41.
64. Sokol H, Pigneur B, Watterlot L et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008;105:16731-6.
65. Sokol H, Seksik P, Furet JP et al. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009;15:1183-9.
66. Tannock G, Munro K, Harmsen H et al. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl Environ Microbiol 2000;66:2578-88.
67. Grehan MJ, Borody TJ, Leis SM et al. Durable alteration of the colonic microbiota by the administration of donor fecal flora. J Clin Gastroenterol 2010;44:551-61.
68. Klein W, Müller R. Das einweibminimum, die zymogene symbiose und die erzeugung von mikrobeneiweib im pansen aus stickstoffverbindungen nicht eiweibartiger nature (ein beitrag zur biologie des widerkäuers). Zeitschrift für Tierzüchtung und Züchtungsbiologie 1941;48:255-76.
69. Ebino KY. Studies on coprophagy in experimental animals. Jikken Dobutsu 1993;42:1-9.
70. Lewin RA. More on merde. Perspect Biol Med 2001;44:594-607.
71. Eiseman B, Silen W, Bascom G et al. Fecal enema as an adjunct in thetreatment of pseudomembranous enterocolitis. Surgery 1958;44:854.
72. Bowden T Jr, Mansberger A Jr, Lykins L et al. Pseudomembraneous enterocolitis: mechanism of restoring floral homeostasis. Am Surg 1981;47:178.
73. Schwan A, Sjölin S, Trottestam U et al. Relapsing clostridium difficile enterocolitis cured by rectal infusion of homologous faeces. Lancet 1983;8:845.
74. Borody TJ, Khoruts A. Fecal microbiota transplantation and emerging applications. Nat Rev Gastroenterol Hepatol 2011;9:88-96.
75. Bakken JS, Borody T, Brandt LJ et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol 2011;9:1044-9.
76. Mattila E, Uusitalo-Seppälä R, Wuorela M et al. Fecal transplantation, through colonoscopy, is effectivetherapy for recurrent Clostridium difficile infection. Gastroenterology 2012;142:490-6.
77. van Nood E, Speelman P, Kuijper EJ et al. Struggling with recurrent Clostridium difficile infections: is donor faeces the solution? Euro Surveill 2009;14:316.
78. Borody T, George L, Andrews P et al. Bowel-flora alteration: a potential cure for inflammatory bowel disease and irritable bowel syndrome? Med J Aust 1989;150:604.
79. Gustafsson A, Berstad A, Lund-Tonnesen S et al. The effect of faecal enema on five microflora-associated characteristics in patients with antibiotic-associated diarrhoea. Scand J Gastroenterol 1999;34:580-6.
80. Vrieze A. Metabolic effects of transplanting gut microbiota from lean donors to subjects with metabolic syndrome. Diabetologia 2010;53:S44.
81. Bennet JD, Brinkman M. Treatment of ulcerative colitis by implantation of normal colonic flora. Lancet 1989;1:164.
82. Borody TJ, Warren EF, Leis S et al. Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol 2003;37:42-7.
83. Borody TJ, Campbell J. Fecal microbiota transplantation: current status and future directions. Exp Rev Gastroenterol Hepatol 2011;5:653-5.
84. Lin J, Hackam DJ. Worms, flies and four-legged friends: the applicability of biological models to the understanding of intestinal inflammatory diseases. Dis Model Mech 2011;4:447-56.
85. Elson CO, Cong Y, McCracken VJ et al. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol Rev 2005;206:260-76.
86. Gootenberg DB, Turnbaugh PJ. Companion animals symposium: humanized animal models of the microbiome. J Anim Sci 2011;89:1531-7.
87. Rawls JF, Mahowald MA, Ley RE et al. Reciprocal gut microbiota transplants from zebrafish and miceto germ-free recipients reveal host habitat selection. Cell 2006;127:423-33.
88. Alpert C, Sczesny S, Gruhl B et al. Long-term stability of the human gut microbiota in two different rat strains. Curr Issues Mol Biol 2008;10:17-24.
89. Vijay-Kumar M, Aitken JD, Carvalho FA et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010;328:228-31.
90. Manichanh C, Reeder J, Gibert P et al. Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res 2010;20:1411-9.
91. Garrett WS, Lord GM, Punit S et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007;131:33-45.
92. Garrett WS, Gallini CA, Yatsunenko T et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010;8:292-300.
93. Elinav E, Strowig T, Kau AL et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011;145:745-57.
94. Ivanov II, Frutos RDL, Manel N et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008;4:337-49.
95. Ivanov II, Atarashi K, Manel N et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009;139:485-98.
96. Willing BP, Vacharaksa A, Croxen M et al. Altering host resistanceto infections through microbial transplantation. PLoS One [online] 2011;6:e26988.
97. Ghosh S, Dai C, Brown K et al. Colonic microbiota alters host susceptibility to infectious colitis by modulating inflammation, redox status, and ion transporter gene expression. Am J Physiol Gastrointest Liver Physiol 2011;301:G39-49.
98. Stecher B, Chaffron S, Käppeli R et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog [online] 2010;6:e1000711.
99. Endt K, Stecher B, Chaffron S et al. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog [online] 2010;6:e1001097.
100. Burns DA, Heap JT, Minton NP. Clostridium difficile spore germination: an update. Res Microbiol 2010;161:730-4.
101. Khoruts A, Dicksved J, Jansson JK et al. Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea. J Clin Gastroenterol 2010;44:354-60.
102. Kahn SA, Gorawara-Bhat R, Rubin DT. Fecal bacteriotherapy for ulcerative colitis: patients are ready, are we? Inflamm Bowel Dis 2012;18:676-84.