From stool transplants to next-generation microbiota therapeutics

Gastroenterology

Volumn 146, Issue 6, 2014, Pages 1573-1582

  Petrof, Elaine O ^a   Khoruts, Alexander ^b  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Defined Microbiota Ecosystems; Fecal Microbiota Transplantation; Full Spectrum Microbiota; Recurrent Clostridium difficile Infection

Indexed keywords

ARTICLE; CLINICAL PRACTICE; CLOSTRIDIUM DIFFICILE INFECTION; EPIDEMIC; FECES MICROFLORA; FETAL TISSUE TRANSPLANTATION; HISTORY OF MEDICINE; HUMAN; NONHUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC);

DEFINED MICROBIOTA ECOSYSTEMS; FECAL MICROBIOTA TRANSPLANTATION; FULL SPECTRUM MICROBIOTA; RECURRENT CLOSTRIDIUM DIFFICILE INFECTION;

ANIMALS; BIOLOGICAL THERAPY; CLOSTRIDIUM DIFFICILE; DYSBIOSIS; ENTEROCOLITIS, PSEUDOMEMBRANOUS; EPIDEMICS; FECES; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINES; MICROBIOTA; RECURRENCE; RISK FACTORS; TREATMENT OUTCOME;

EID: 84898778719     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2014.01.004     Document Type: Article

References (95)

1. M.J. Blaser, and S. Falkow What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 7 2009 887 894
2. J. Schrezenmeir, and M. de Vrese Probiotics, prebiotics, and synbiotics-approaching a definition Am J Clin Nutr 73 2001 361S 364S
3. M. de Vrese, and J. Schrezenmeir Probiotics, prebiotics, and synbiotics Adv Biochem Eng Biotechnol 111 2008 1 66
4. M.E. Sanders Probiotics: definition, sources, selection, and uses Clin Infect Dis 46 Suppl 2 2008 S58 S61 discussion S144-S151
5. D.E. Hoffmann, C.M. Fraser, and F.B. Palumbo et al. Science and regulation. Probiotics: finding the right regulatory balance Science 342 2013 314 315
6. T.J. Borody, and A. Khoruts Fecal microbiota transplantation and emerging applications Nat Rev Gastroenterol Hepatol 9 2011 88 96
7. Z. Kassam, C.H. Lee, and Y. Yuan et al. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis Am J Gastroenterol 108 2013 500 508
8. K.E. Burke, and J.T. Lamont Fecal transplantation for recurrent Clostridium difficile infection in older adults: a review J Am Geriatr Soc 61 2013 1394 1398
9. L.J. Brandt, and O.C. Aroniadis An overview of fecal microbiota transplantation: techniques, indications, and outcomes Gastrointest Endosc 78 2013 240 249
10. E. Gough, H. Shaikh, and A.R. Manges Systematic review of intestinal microbiota transplantation (fecal bacteriotherapy) for recurrent Clostridium difficile infection Clin Infect Dis 53 2011 994 1002
11. R.E. Ley, C.A. Lozupone, and M. Hamady et al. Worlds within worlds: evolution of the vertebrate gut microbiota Nat Rev Microbiol 6 2008 776 788
12. D.W. Hopkins, J.A. Chudek, and D.E. Bignell et al. Application of 13C NMR to investigate the transformations and biodegradation of organic materials by wood- and soil-feeding termites, and a coprophagous litter-dwelling dipteran larva Biodegradation 9 1998 423 431
13. P.R. Guy Coprophagy in the African elephant (Loxadonta africana Blumenbach) Afr J Ecol 15 1977 174
14. C.L.R. Payne, T.H. Webster, and K.D. Hunt Coprophagy by the semi-habituated chimpanzees of Semliki, Uganda Pan Africa News 15 2008 29 32
15. B.H. Jasmin, R.C. Boston, and R.B. Modesto et al. Perioperative ruminal pH changes in domestic sheep (Ovis aries) housed in a biomedical research setting J Am Assoc Lab Anim Sci 50 2011 27 32
16. K. McGovern Approach to the adult horse with chronic diarrhea Livestock 18 2013 189 194
17. E. Nurmi, and M. Rantala New aspects of Salmonella infection in broiler production Nature 241 1973 210 211
18. F. Zhang, W. Luo, and Y. Shi et al. Should we standardize the 1,700-year-old fecal microbiota transplantation? Am J Gastroenterol 107 2012 1755 author reply 6
19. S. Lehrer Duodenal infusion of feces for recurrent Clostridium difficile N Engl J Med 368 2013 2144
20. B. Eiseman, W. Silen, and G.S. Bascom et al. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis Surgery 44 1958 854 859
21. D.P. Levine Vancomycin: a history Clin Infect Dis 42 Suppl 1 2006 S5 S12
22. O.C. Aroniadis, and L.J. Brandt Fecal microbiota transplantation: past, present and future Curr Opin Gastroenterol 29 2013 79 84
23. M. Tvede, and J. Rask-Madsen Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients Lancet 1 1989 1156 1160
24. M. Dietrich, and T.M. Fliedner Gnotobiotic care of patients with immunologic deficiency diseases Transplant Proc 5 1973 1271 1277
25. D. van der Waaij, J.M. Vossen, and C.K. Altes et al. Reconventionalization following antibiotic decontamination in man and animals Am J Clin Nutr 30 1977 1887 1895
26. D. van der Waaij The ecology of the human intestine and its consequences for overgrowth by pathogens such as Clostridium difficile Annu Rev Microbiol 43 1989 69 87
27. W.M. de Vos Fame and future of faecal transplantations-developing next-generation therapies with synthetic microbiomes Microb Biotechnol 6 2013 316 325
28. A.N. Ananthakrishnan Clostridium difficile infection: epidemiology, risk factors and management Nat Rev Gastroenterol Hepatol 8 2011 17 26
29. M. He, F. Miyajima, and P. Roberts et al. Emergence and global spread of epidemic healthcare-associated Clostridium difficile Nat Genet 45 2013 109 113
30. M. Rupnik, M.H. Wilcox, and D.N. Gerding Clostridium difficile infection: new developments in epidemiology and pathogenesis Nat Rev Microbiol 7 2009 526 536
31. M. Merrigan, A. Venugopal, and M. Mallozzi et al. Human hypervirulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production J Bacteriol 192 2010 4904 4911
32. D.W. Eyre, M.L. Cule, and D.J. Wilson et al. Diverse sources of C. difficile infection identified on whole-genome sequencing N Engl J Med 369 2013 1195 1205
33. S. Khanna, D.S. Pardi, and S.L. Aronson et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study Am J Gastroenterol 107 2012 89 95
34. L. Lee, and S.H. Cohen Community-acquired Clostridium difficile infection: an emerging problem Curr Emerg Hosp Med Rep 1 2013 149 153
35. A.J. Hall, A.T. Curns, and L.C. McDonald et al. The roles of Clostridium difficile and norovirus among gastroenteritis-associated deaths in the United States, 1999-2007 Clin Infect Dis 55 2012 216 223
36. W.R. Jarvis, J. Schlosser, and A.A. Jarvis et al. National point prevalence of Clostridium difficile in US health care facility inpatients, 2008 Am J Infect Control 37 2009 263 270
37. A. Markelov, D. Livert, and H. Kohli Predictors of fatal outcome after colectomy for fulminant Clostridium difficile colitis: a 10-year experience Am Surg 77 2011 977 980
38. F. Lamontagne, A.C. Labbe, and O. Haeck et al. Impact of emergency colectomy on survival of patients with fulminant Clostridium difficile colitis during an epidemic caused by a hypervirulent strain Ann Surg 245 2007 267 272
39. L.J. Brandt, O.C. Aroniadis, and M. Mellow et al. Long-term follow-up of colonoscopic fecal microbiota transplant for recurrent Clostridium difficile infection Am J Gastroenterol 107 2012 1079 1087
40. M.J. Hamilton, A.R. Weingarden, and T. Unno et al. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria Gut Microbes 4 2013 125 135
41. E. van Nood, A. Vrieze, and M. Nieuwdorp et al. Duodenal infusion of donor feces for recurrent Clostridium difficile N Engl J Med 368 2013 407 415
42. M.S. Silverman, I. Davis, and D.R. Pillai Success of self-administered home fecal transplantation for chronic Clostridium difficile infection Clin Gastroenterol Hepatol 8 2010 471 473
43. J.S. Bakken, T. Borody, and L.J. Brandt et al. Treating Clostridium difficile infection with fecal microbiota transplantation Clin Gastroenterol Hepatol 9 2011 1044 1049
44. J.S. Bakken, P.M. Polgreen, and S.E. Beekmann et al. Treatment approaches including fecal microbiota transplantation for recurrent Clostridium difficile infection (RCDI) among infectious disease physicians Anaerobe 24 2013 20 24
45. J.G. Bartlett Clostridium difficile: progress and challenges Ann N Y Acad Sci 1213 2010 62 69
46. V. Stevens, G. Dumyati, and L.S. Fine et al. Cumulative antibiotic exposures over time and the risk of Clostridium difficile infection Clin Infect Dis 53 2011 42 48
47. J.Y. Chang, D.A. Antonopoulos, and A. Kalra et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea J Infect Dis 197 2008 435 438
48. A. Khoruts, J. Dicksved, and J.K. Jansson et al. Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea J Clin Gastroenterol 44 2010 354 360
49. M.M. Merrigan, S.P. Sambol, and S. Johnson et al. New approach to the management of Clostridium difficile infection: colonisation with non-toxigenic C. difficile during daily ampicillin or ceftriaxone administration Int J Antimicrob Agents 33 Suppl 1 2009 S46 S50
50. T.D. Lawley, S. Clare, and A.W. Walker et al. Targeted restoration of the intestinal microbiota with a simple, defined bacteriotherapy resolves relapsing Clostridium difficile disease in mice PLoS Pathog 8 2012 e1002995
51. E.O. Petrof, G.B. Gloor, and S.J. Vanner et al. Stool substitute transplant therapy for the eradication of Clostridium difficile infection: 'RePOOPulating' the gut Microbiome 1 2013 1 12
52. P. Banerjee, G.J. Merkel, and A.K. Bhunia Lactobacillus delbrueckii ssp. bulgaricus B-30892 can inhibit cytotoxic effects and adhesion of pathogenic Clostridium difficile to Caco-2 cells Gut Pathog 1 2009 8
53. M.C. Rea, A. Dobson, and O. O'Sullivan et al. Effect of broad- and narrow-spectrum antimicrobials on Clostridium difficile and microbial diversity in a model of the distal colon Proc Natl Acad Sci U S A 108 Suppl 1 2011 4639 4644
54. K.H. Wilson Efficiency of various bile salt preparations for stimulation of Clostridium difficile spore germination J Clin Microbiol 18 1983 1017 1019
55. J.A. Sorg, and A.L. Sonenshein Bile salts and glycine as cogerminants for Clostridium difficile spores J Bacteriol 190 2008 2505 2512
56. J.A. Sorg, and A.L. Sonenshein Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid J Bacteriol 192 2010 4983 4990
57. M.B. Francis, C.A. Allen, and R. Shrestha et al. Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection PLoS Pathog 9 2013 e1003356
58. J.L. Giel, J.A. Sorg, A.L. Sonenshein, and J. Zhu Metabolism of bile salts in mice influences spore germination in Clostridium difficile PLoS One 5 2010 e8740
59. A.R. Weingarden, C. Chen, and A. Bobr et al. Microbiota transplantation restores normal fecal bile acid composition in recurrent Clostridium difficile infection Am J Physiol Gastrointest Liver Physiol 306 2014 G310 G319
60. D. Kunimoto, and A.B. Thomson Recurrent Clostridium difficile-associated colitis responding to cholestyramine Digestion 33 1986 225 228
61. P. Pruksananonda, and K.R. Powell Multiple relapses of Clostridium difficile-associated diarrhea responding to an extended course of cholestyramine Pediatr Infect Dis J 8 1989 175 178
62. M.D. Moncino, and J.M. Falletta Multiple relapses of Clostridium difficile-associated diarrhea in a cancer patient. Successful control with long-term cholestyramine therapy Am J Pediatr Hematol Oncol 14 1992 361 364
63. C.D. Jolley, J.M. Dietschy, and S.D. Turley Induction of bile acid synthesis by cholesterol and cholestyramine feeding is unimpaired in mice deficient in apolipoprotein AI Hepatology 32 2000 1309 1316
64. C. Rust, G.H. Sauter, and M. Oswald et al. Effect of cholestyramine on bile acid pattern and synthesis during administration of ursodeoxycholic acid in man Eur J Clin Invest 30 2000 135 139
65. A. Pantosti, I. Luzzi, and R. Cardines et al. Comparison of the in vitro activities of teicoplanin and vancomycin against Clostridium difficile and their interactions with cholestyramine Antimicrob Agents Chemother 28 1985 847 848
66. S.H. Cohen, D.N. Gerding, and S. Johnson et al. 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 31 2010 431 455
67. S. Rakoff-Nahoum, J. Paglino, and F. Eslami-Varzaneh et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis Cell 118 2004 229 241
68. I. Jarchum, M. Liu, and C. Shi et al. Critical role for MyD88-mediated neutrophil recruitment during Clostridium difficile colitis Infect Immun 80 2012 2989 2996
69. A. Ryan, M. Lynch, and S.M. Smith et al. A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins PLoS Pathog 7 2011 e1002076
70. Y.P. Hung, H.J. Lin, and T.C. Wu et al. Risk factors of fecal toxigenic or non-toxigenic Clostridium difficile colonization: impact of Toll-like receptor polymorphisms and prior antibiotic exposure PLoS One 8 2013 e69577
71. I. Jarchum, M. Liu, and L. Lipuma et al. Toll-like receptor 5 stimulation protects mice from acute Clostridium difficile colitis Infect Immun 79 2011 1498 1503
72. A. Menendez, B.P. Willing, and M. Montero et al. Bacterial stimulation of the TLR-MyD88 pathway modulates the homeostatic expression of ileal Paneth cell alpha-defensins J Innate Immun 5 2013 39 49
73. T. Giesemann, G. Guttenberg, and K. Aktories Human alpha-defensins inhibit Clostridium difficile toxin B Gastroenterology 134 2008 2049 2058
74. B.A. Leav, B. Blair, and M. Leney et al. Serum anti-toxin B antibody correlates with protection from recurrent Clostridium difficile infection (CDI) Vaccine 28 2010 965 969
75. J.M. Miller, R. Astles, and T. Baszler et al. Guidelines for safe work practices in human and animal medical diagnostic laboratories. Recommendations of a CDC-convened, Biosafety Blue Ribbon Panel MMWR Surveill Summ 61 Suppl 2012 1 102
76. J.M. Starkey, J.L. MacPherson, and D.C. Bolgiano et al. Markers for transfusion-transmitted disease in different groups of blood donors JAMA 262 1989 3452 3454
77. L.P. Smits, K.E. Bouter, and W.M. de Vos et al. Therapeutic potential of fecal microbiota transplantation Gastroenterology 145 2013 946 953
78. E. Allen-Vercoe, G. Reid, and N. Viner et al. A Canadian Working Group report on fecal microbial therapy: microbial ecosystems therapeutics Can J Gastroenterol 26 2012 457 462
79. P.B. Reich, D. Tilman, and F. Isbell et al. Impacts of biodiversity loss escalate through time as redundancy fades Science 336 2012 589 592
80. E.O. Petrof, E.C. Claud, and G.B. Gloor et al. Microbial ecosystems therapeutics: a new paradigm in medicine? Benef Microbes 4 2013 53 65
81. T. Olszak, D. An, and S. Zeissig et al. Microbial exposure during early life has persistent effects on natural killer T cell function Science 336 2012 489 493
82. I. Cho, S. Yamanishi, and L. Cox et al. Antibiotics in early life alter the murine colonic microbiome and adiposity Nature 488 2012 621 626
83. R. Diaz Heijtz, S. Wang, and F. Anuar et al. Normal gut microbiota modulates brain development and behavior Proc Natl Acad Sci U S A 108 2011 3047 3052
84. P.R. Moore, and A. Evenson et al. Use of sulfasuxidine, streptothricin, and streptomycin in nutritional studies with the chick J Biol Chem 165 1946 437 441
85. T.H. Jukes, and W.L. Williams Nutritional effects of antibiotics Pharmacol Rev 5 1953 381 420
86. T.H. Haight, and W.E. Pierce Effect of prolonged antibiotic administration of the weight of healthy young males J Nutr 56 1955 151 161
87. F. Backhed, H. Ding, and T. Wang et al. The gut microbiota as an environmental factor that regulates fat storage Proc Natl Acad Sci U S A 101 2004 15718 15723
88. V.K. Ridaura, J.J. Faith, and F.E. Rey et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice Science 341 2013 1241214
89. M.I. Smith, T. Yatsunenko, and M.J. Manary et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor Science 339 2013 548 554
90. A. Vrieze, E. Van Nood, and F. Holleman et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome Gastroenterology 143 2012 913 916.e7
91. J.D. Bennet, and M. Brinkman Treatment of ulcerative colitis by implantation of normal colonic flora Lancet 1 1989 164
92. T.J. Borody, E.F. Warren, and S. Leis et al. Treatment of ulcerative colitis using fecal bacteriotherapy J Clin Gastroenterol 37 2003 42 47
93. S. Kunde, A. Pham, and S. Bonczyk et al. Safety, tolerability, and clinical response after fecal transplantation in children and young adults with ulcerative colitis J Pediatr Gastroenterol Nutr 56 2013 597 601
94. S. Angelberger, W. Reinisch, and A. Makristathis et al. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation Am J Gastroenterol 108 2013 1620 1630
95. P.K. Kump, H.P. Grochenig, and S. Lackner et al. Alteration of intestinal dysbiosis by fecal microbiota transplantation does not induce remission in patients with chronic active ulcerative colitis Inflamm Bowel Dis 19 2013 2155 2165