Therapeutic modulation of intestinal dysbiosis

Pharmacological Research

Volumn 69, Issue 1, 2013, Pages 75-86

  Walker, Alan W ^a   Lawley, Trevor D ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Dysbiosis; Faecal transplantation; Intestinal homeostasis; Intestinal microbiota; Prebiotics; Probiotics

Indexed keywords

ACETIC ACID; ANTIBIOTIC AGENT; BUTYRIC ACID; FIDAXOMICIN; FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INULIN; POLYSACCHARIDE; PREBIOTIC AGENT; PROBIOTIC AGENT; PROPIONIC ACID; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; VANCOMYCIN; XYLOSE OLIGOSACCHARIDE;

ACTINOBACTERIA; ANTIBACTERIAL ACTIVITY; ATOPY; BACTEROIDETES; BIFIDOBACTERIUM BREVE; BIOLOGICAL THERAPY; CLOSTRIDIUM DIFFICILE INFECTION; COLITIS; COLORECTAL CANCER; CROHN DISEASE; DIABETES MELLITUS; DIARRHEA; DIETARY FIBER; DRUG EFFICACY; DRUG TARGETING; DYSBIOSIS; ENTERITIS; FECAL TRANSPLANTATION; FIRMICUTES; GASTROINTESTINAL INFECTION; HUMAN; ILEITIS; INTESTINE FLORA; METABOLIC SYNDROME X; NECROTIZING ENTEROCOLITIS; NONHUMAN; ORGANISMAL INTERACTION; PRIORITY JOURNAL; PROTEOBACTERIA; PSEUDOMEMBRANOUS COLITIS; REVIEW; ULCERATIVE COLITIS;

GASTROINTESTINAL DISEASES; HUMANS; INTESTINES; METAGENOME;

EID: 84873718952     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2012.09.008     Document Type: Review

References (177)

1. T.D. Leser, and L. Mølbak Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host Environmental Microbiology 11 2009 2194 2206
2. W.B. Whitman, D.C. Coleman, and W.J. Wiebe Prokaryotes: the unseen majority Proceedings of the National Academy of Sciences of the United States of America 95 1998 6578 6583
3. J. Qin, R. Li, J. Raes, M. Arumugam, K.S. Burgdorf, and C. Manichanh A human gut microbial gene catalogue established by metagenomic sequencing Nature 464 2010 59 65
4. E.A. Grice, and J.A. Segre The human microbiome: our second genome Annual Review of Genomics and Human Genetics 2012 10.1146/annurev-genom-090711-163814 [Epub ahead of print]
5. T. Feng, L. Wang, T.R. Schoeb, C.O. Elson, and Y. Cong Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis Journal of Experimental Medicine 207 2010 1321 1332
6. C.P. Tamboli, C. Neut, P. Desreumaux, and J.F. Colombel Dysbiosis in inflammatory bowel disease Gut 53 2004 1 4
7. A.W. DuPont, and H.L. DuPont The intestinal microbiota and chronic disorders of the gut Nature Reviews Gastroenterology & Hepatology 8 2011 523 531
8. E. Holmes, J. Kinross, G.R. Gibson, R. Burcelin, W. Jia, and S. Pettersson Therapeutic modulation of microbiota-host metabolic interactions Science Translational Medicine 4 137 2012 rv6
9. W. Jia, H. Li, L. Zhao, and J.K. Nicholson Gut microbiota: a potential new territory for drug targeting Nature Reviews Drug Discovery 7 2008 123 129
10. E. Metchnikoff The prolongation of life: optimistic studies 1908 G.P. Putnam's Sons New York
11. R.I. Mackie, A. Sghir, and H.R. Gaskins Developmental microbial ecology of the neonatal gastrointestinal tract American Journal of Clinical Nutrition 69 1999 1035S 1045S
12. M.G. Dominguez-Bello, E.K. Costello, M. Contreras, M. Magris, G. Hidalgo, and N. Fierer Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns Proceedings of the National Academy of Sciences of the United States of America 107 2010 11971 11975
13. H.J. Harmsen, A.C. Wildeboer-Veloo, G.C. Raangs, A.A. Wagendorp, N. Klijn, and J.G. Bindels Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods Journal of Pediatric Gastroenterology and Nutrition 30 2000 61 67
14. D.A. Sela, and D.A. Mills Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides Trends in Microbiology 18 2010 298 307
15. L. Duijts, M.K. Ramadhani, and H.A. Moll Breastfeeding protects against infectious diseases during infancy in industrialized countries. A systematic review Maternal & Child Nutrition 5 2009 199 210
16. J.M. Hascoët, C. Hubert, F. Rochat, H. Legagneur, S. Gaga, and S. Emady-Azar Effect of formula composition on the development of infant gut microbiota Journal of Pediatric Gastroenterology and Nutrition 52 2011 756 762
17. A.L. Kozyrskyj, P. Ernst, and A.B. Becker Increased risk of childhood asthma from antibiotic use in early life Chest 131 2007 1753 1759
18. S.L. Russell, M.J. Gold, M. Hartmann, B.P. Willing, L. Thorson, and M. Wlodarska Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma EMBO Reports 13 2012 440 447
19. A. Hviid, H. Svanström, and M. Frisch Antibiotic use and inflammatory bowel diseases in childhood Gut 60 2011 49 54
20. J.E. Koenig, A. Spor, N. Scalfone, A.D. Fricker, J. Stombaugh, and R. Knight Succession of microbial consortia in the developing infant gut microbiome Proceedings of the National Academy of Sciences of the United States of America 108 Suppl. 1 2011 4578 4585
21. T. Yatsunenko, F.E. Rey, M.J. Manary, I. Trehan, M.G. Dominguez-Bello, and M. Contreras Human gut microbiome viewed across age and geography Nature 486 2012 222 227
22. M. Rajilić-Stojanović, H. Smidt, and W.M. de Vos Diversity of the human gastrointestinal tract microbiota revisited Environmental Microbiology 9 2007 2125 2136
23. Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
24. P.J. Turnbaugh, M. Hamady, T. Yatsunenko, B.L. Cantarel, A. Duncan, and R.E. Ley A core gut microbiome in obese and lean twins Nature 457 2009 480 484
25. E.G. Zoetendal, A.D.L. Akkermans, and W.M. de Vos Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria Applied and Environment Microbiology 64 1998 3854 3859
26. J.G. Caporaso, C.L. Lauber, E.K. Costello, D. Berg-Lyons, A. Gonzalez, and J. Stombaugh Moving pictures of the human microbiome Genome Biology 12 2011 R50
27. S.H. Duncan, A. Belenguer, G. Holtrop, A.M. Johnstone, H.J. Flint, and G.E. Lobley Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces Applied and Environment Microbiology 73 2007 1073 1078
28. A.W. Walker, J. Ince, S.H. Duncan, L.M. Webster, G. Holtrop, and X. Ze Dominant and diet-responsive groups of bacteria within the human colonic microbiota The ISME Journal 5 2011 220 230
29. G.D. Wu, J. Chen, C. Hoffmann, K. Bittinger, Y.Y. Chen, and S.A. Keilbaugh Linking long-term dietary patterns with gut microbial enterotypes Science 334 2011 105 108
30. M. Wilson Microbial inhabitants of humans: their ecology and role in health and disease 1st ed. 2005 Cambridge University Press New York
31. P.B. Eckburg, E.M. Bik, C.N. Bernstein, E. Purdom, L. Dethlefsen, and M. Sargent Diversity of the human intestinal microbial flora Science 308 2005 1635 1638
32. J. Tap, S. Mondot, F. Levenez, E. Pelletier, C. Caron, and J.P. Furet Towards the human intestinal microbiota phylogenetic core Environmental Microbiology 11 2009 2574 2584
33. A.M. Stephen, and J.H. Cummings The microbial contribution to human faecal mass Journal of Medical Microbiology 13 1980 45 56
34. M. Breitbart, M. Haynes, S. Kelley, F. Angly, R.A. Edwards, and B. Felts Viral diversity and dynamics in an infant gut Research in Microbiology 159 2008 367 373
35. A. Reyes, M. Haynes, N. Hanson, F.E. Angly, A.C. Heath, and F. Rohwer Viruses in the faecal microbiota of monozygotic twins and their mothers Nature 466 2010 334 338
36. K. Cadwell, K.K. Patel, N.S. Maloney, T.C. Liu, A.C. Ng, and C.E. Storer Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine Cell 141 2010 1135 1145
37. P.D. Scanlan, and J.R. Marchesi Micro-eukaryotic diversity of the human distal gut microbiota: qualitative assessment using culture-dependent and -independent analysis of faeces The ISME Journal 2 2008 1183 1193
38. I.D. Iliev, V.A. Funari, K.D. Taylor, Q. Nguyen, C.N. Reyes, and S.P. Strom Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis Science 336 2012 1314 1317
39. N. Nakamura, H.C. Lin, C.S. McSweeney, R.I. Mackie, and H.R. Gaskins Mechanisms of microbial hydrogen disposal in the human colon and implications for health and disease Annual Review of Food Science and Technology 1 2010 363 395
40. R. Blumberg, and F. Powrie Microbiota, disease, and back to health: a metastable journey Science Translational Medicine 4 137 2012 rv7
41. L.V. Hooper, T. Midtvedt, and J.I. Gordon How host-microbial interactions shape the nutrient environment of the mammalian intestine Annual Review of Nutrition 22 2002 283 307
42. P.B. Mortensen, and M.R. Clausen Short-chain fatty acids in the human colon: relation to gastrointestinal health and disease Scandinavian Journal of Gastroenterology: Supplement 216 1996 132 148
43. H. Ruppin, S. Bar-Meir, K.H. Soergel, C.M. Wood, and M.G. Schmitt Jr. Absorption of short-chain fatty acids by the colon Gastroenterology 78 1980 1500 1507
44. W.E. Roediger Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man Gut 21 1980 793 798
45. H. Ashida, M. Ogawa, M. Kim, H. Mimuro, and C. Sasakawa Bacteria and host interactions in the gut epithelial barrier Nature Chemical Biology 8 2011 36 45
46. J.P. Segain, D. Raingeard de la Blétière, A. Bourreille, V. Leray, N. Gervois, and C. Rosales Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn's disease Gut 47 2000 397 403
47. R.B. Canani, M.D. Costanzo, L. Leone, M. Pedata, R. Meli, and A. Calignano Potential beneficial effects of butyrate in intestinal and extraintestinal diseases World Journal of Gastroenterology 17 2011 1519 1528
48. A. Barcenilla, S.E. Pryde, J.C. Martin, S.H. Duncan, C.S. Stewart, and C. Henderson Phylogenetic relationships of butyrate-producing bacteria from the human gut Applied and Environment Microbiology 66 2000 1654 1661
49. F. Van Immerseel, R. Ducatelle, M. De Vos, N. Boon, T. Van De Wiele, and K. Verbeke Butyric acid-producing anaerobic bacteria as a novel probiotic treatment approach for inflammatory bowel disease Journal of Medical Microbiology 59 2010 141 143
50. K.M. Maslowski, A.T. Vieira, A. Ng, J. Kranich, F. Sierro, and D. Yu Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43 Nature 461 2009 1282 1286
51. S. Rakoff-Nahoum, J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis Cell 118 2004 229 241
52. H. Chung, S.J. Pamp, J.A. Hill, N.K. Surana, S.M. Edelman, and E.B. Troy Gut immune maturation depends on colonization with a host-specific microbiota Cell 149 2012 1578 1593
53. J.L. Round, and S.K. Mazmanian Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota Proceedings of the National Academy of Sciences of the United States of America 107 2010 12204 12209
54. K. Atarashi, T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, and Y. Momose Induction of colonic regulatory T cells by indigenous Clostridium species Science 331 2011 337 341
55. Lawley TD, Walker AW. Intestinal colonization resistance. Immunology, in press.
56. H. Kato, H. Kita, T. Karasawa, T. Maegawa, Y. Koino, and H. Takakuwa Colonisation and transmission of Clostridium difficile in healthy individuals examined by PCR ribotyping and pulsed-field gel electrophoresis Journal of Medical Microbiology 50 2001 720 727
57. M.J. Hill Intestinal flora and endogenous vitamin synthesis European Journal of Cancer Prevention 6 Suppl. 1 1997 S43 S45
58. T. Clavel, G. Henderson, C.A. Alpert, C. Philippe, L. Rigottier-Gois, and J. Doré Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans Applied and Environment Microbiology 71 2005 6077 6085
59. A.S. Neish The gut microflora and intestinal epithelial cells: a continuing dialogue Microbes and Infection 4 2002 309 317
60. C.S. Stewart, S.H. Duncan, and D.R. Cave Oxalobacter formigenes and its role in oxalate metabolism in the human gut FEMS Microbiology Letters 230 2004 1 7
61. D.N. Frank, W. Zhu, R.B. Sartor, and E. Li Investigating the biological and clinical significance of human dysbioses Trends in Microbiology 19 2011 427 434
62. D.N. Frank, A.L. St Amand, R.A. Feldman, E.C. Boedeker, N. Harpaz, and N.R. Pace Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Proceedings of the National Academy of Sciences of the United States of America 104 2007 13780 13785
63. B. Willing, J. Halfvarson, J. Dicksved, M. Rosenquist, G. Järnerot, and L. Engstrand Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn's disease Inflammatory Bowel Diseases 15 2009 653 660
64. S.D. McLaughlin, A.W. Walker, C. Churcher, S.K. Clark, P.P. Tekkis, and M.W. Johnson The bacteriology of pouchitis: a molecular phylogenetic analysis using 16S rRNA gene cloning and sequencing Annals of Surgery 252 2010 90 98
65. A.W. Walker, J.D. Sanderson, C. Churcher, G.C. Parkes, B.N. Hudspith, and N. Rayment High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease BMC Microbiology 11 2011 7
66. L. Wen, R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, and A.C. Stonebraker Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
67. R.E. Ley, P.J. Turnbaugh, S. Klein, and J.I. Gordon Microbial ecology: human gut microbes associated with obesity Nature 444 2006 1022 1023
68. M. Vijay-Kumar, J.D. Aitken, F.A. Carvalho, T.C. Cullender, S. Mwangi, and S. Srinivasan Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5 Science 328 2010 228 231
69. J. Henao-Mejia, E. Elinav, C. Jin, L. Hao, W.Z. Mehal, and T. Strowig Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity Nature 482 2012 179 185
70. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, and B. Dugar Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 2011 57 63
71. M. Wang, C. Karlsson, C. Olsson, I. Adlerberth, A.E. Wold, and D.P. Strachan Reduced diversity in the early fecal microbiota of infants with atopic eczema Journal of Allergy and Clinical Immunology 121 2008 129 134
72. C. Manichanh, L. Rigottier-Gois, E. Bonnaud, K. Gloux, E. Pelletier, and L. Frangeul Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach Gut 55 2006 205 211
73. J.Y. Chang, D.A. Antonopoulos, A. Kalra, A. Tonelli, W.T. Khalife, and T.M. Schmidt Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea Journal of Infectious Diseases 197 2008 435 438
74. P. Lepage, R. Häsler, M.E. Spehlmann, A. Rehman, A. Zvirbliene, and A. Begun Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis Gastroenterology 141 2011 227 236
75. H. Sokol, P. Seksik, J.P. Furet, O. Firmesse, I. Nion-Larmurier, and L. Beaugerie Low counts of Faecalibacterium prausnitzii in colitis microbiota Inflammatory Bowel Diseases 15 2009 1183 1189
76. B.P. Willing, J. Dicksved, J. Halfvarson, A.F. Andersson, M. Lucio, and Z. Zheng A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes Gastroenterology 139 2010 1844 1854
77. M. Tvede, and J. Rask-Madsen Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients Lancet 1 1989 1156 1160
78. C. Lupp, M.L. Robertson, M.E. Wickham, I. Sekirov, O.L. Champion, and E.C. Gaynor Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae Cell Host and Microbe 2 2007 119 129
79. B. Stecher, R. Robbiani, A.W. Walker, A.M. Westendorf, M. Barthel, and M. Kremer Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota PLoS Biology 5 2007 2177 2189
80. W.S. Garrett, C.A. Gallini, T. Yatsunenko, M. Michaud, A. DuBois, and M.L. Delaney Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis Cell Host and Microbe 8 2010 292 300
81. V. Mai, C.M. Young, M. Ukhanova, X. Wang, Y. Sun, and G. Casella Fecal microbiota in premature infants prior to necrotizing enterocolitis PLoS ONE 6 2011 e20647
82. M.R. Clausen, H. Bonnén, M. Tvede, and P.B. Mortensen Colonic fermentation to short-chain fatty acids is decreased in antibiotic-associated diarrhea Gastroenterology 101 1991 1497 1504
83. B.S. Ramakrishna, and V.I. Mathan Colonic dysfunction in acute diarrhoea: the role of luminal short chain fatty acids Gut 34 1993 1215 1218
84. L.G. Patwa, T.J. Fan, S. Tchaptchet, Y. Liu, Y.A. Lussier, and R.B. Sartor Chronic intestinal inflammation induces stress-response genes in commensal Escherichia coli Gastroenterology 141 2011 1842 1851
85. F.A. Carvalho, O. Koren, J.K. Goodrich, M.E. Johansson, I. Nalbantoglu, and J.D. Aitken Transient inability to manage Proteobacteria promotes chronic gut inflammation in TLR5-deficient mice Cell Host and Microbe 2012 [Epub ahead of print]
86. M. Raffatellu, M.D. George, Y. Akiyama, M.J. Hornsby, S.P. Nuccio, and T.A. Paixao Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine Cell Host and Microbe 5 2009 476 486
87. S.E. Winter, P. Thiennimitr, M.G. Winter, B.P. Butler, D.L. Huseby, and R.W. Crawford Gut inflammation provides a respiratory electron acceptor for Salmonella Nature 467 2010 426 429
88. C. Stelter, R. Käppeli, C. König, A. Krah, W.D. Hardt, and B. Stecher Salmonella-induced mucosal lectin RegIIIβ kills competing gut microbiota PLoS ONE 6 2011 e20749
89. P. Thiennimitr, S.E. Winter, M.G. Winter, M.N. Xavier, V. Tolstikov, and D.L. Huseby Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota Proceedings of the National Academy of Sciences of the United States of America 108 2011 17480 17485
90. J.Z. Liu, S. Jellbauer, A.J. Poe, V. Ton, M. Pesciaroli, and T.E. Kehl-Fie Zinc sequestration by the neutrophil protein calprotectin enhances salmonella growth in the inflamed gut Cell Host and Microbe 11 2012 227 239
91. D. Artis Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut Nature Reviews Immunology 8 2008 411 420
92. B.P. Willing, S.L. Russell, and B.B. Finlay Shifting the balance: antibiotic effects on host-microbiota mutualism Nature Reviews Microbiology 9 2011 233 243
93. E.A. Smith, and G.T. Macfarlane Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism Journal of Applied Bacteriology 81 1996 288 302
94. M.A. Cooper, and D. Shlaes Fix the antibiotics pipeline Nature 472 2011 32
95. C. Jernberg, S. Löfmark, C. Edlund, and J.K. Jansson Long-term impacts of antibiotic exposure on the human intestinal microbiota Microbiology 156 2010 3216 3223
96. C. Jernberg, S. Löfmark, C. Edlund, and J.K. Jansson Long-term ecological impacts of antibiotic administration on the human intestinal microbiota The ISME Journal 1 2007 56 66
97. L. Dethlefsen, and D.A. Relman Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation Proceedings of the National Academy of Sciences of the United States of America 108 Suppl. 1 2011 4554 4561
98. H.E. Jakobsson, C. Jernberg, A.F. Andersson, M. Sjölund-Karlsson, J.K. Jansson, and L. Engstrand Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome PLoS ONE 5 2010 e9836
99. M.J. Hopkins, and G.T. Macfarlane Nondigestible oligosaccharides enhance bacterial colonization resistance against Clostridium difficile in vitro Applied and Environment Microbiology 69 2003 1920 1927
100. M. Wlodarska, B. Willing, K.M. Keeney, A. Menendez, K.S. Bergstrom, and N. Gill Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis Infection and Immunity 79 2011 1536 1545
101. T.J. Louie, M.A. Miller, K.M. Mullane, K. Weiss, A. Lentnek, and Y. Golan Fidaxomicin versus vancomycin for Clostridium difficile infection New England Journal of Medicine 364 2011 422 431
102. T.J. Louie, J. Emery, W. Krulicki, B. Byrne, and M. Mah OPT-80 eliminates Clostridium difficile and is sparing of Bacteroides species during treatment of C. difficile infection Antimicrobial Agents and Chemotherapy 53 2009 261 263
103. G.W. Tannock, K. Munro, C. Taylor, B. Lawley, W. Young, and B. Byrne A new macrocyclic antibiotic, fidaxomicin (OPT-80), causes less alteration to the bowel microbiota of Clostridium difficile-infected patients than does vancomycin Microbiology 156 2010 3354 3359
104. D.M. Citron, Y.A. Warren, K.L. Tyrrell, V. Merriam, and E.J. Goldstein Comparative in vitro activity of REP3123 against Clostridium difficile and other anaerobic intestinal bacteria Journal of Antimicrobial Chemotherapy 63 2009 972 976
105. M.C. Rea, C.S. Sit, E. Clayton, F. Crispie, F. Fouhy, and P.D. Cotter A posttranslationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile Proceedings of the National Academy of Sciences of the United States of America 107 2010 9352 9357
106. R.B. Sartor Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics Gastroenterology 126 2004 1620 1633
107. P.A. Bron, P. van Baarlen, and M. Kleerebezem Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa Nature Reviews Microbiology 10 2012 66 78
108. S.C. Corr, C. Hill, and C.G. Gahan Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens Advances in Food and Nutrition Research 56 2009 1 15
109. G. Reid, J.A. Younes, H.C. Van der Mei, G.B. Gloor, R. Knight, and H.J. Busscher Microbiota restoration: natural and supplemented recovery of human microbial communities Nature Reviews Microbiology 9 2011 27 38
110. A.C. Ouwehand, and S. Salminen In vitro adhesion assays for probiotics and their in vivo relevance: a review Microbial Ecology in Health and Disease 15 2003 175 184
111. G. Deshpande, S. Rao, S. Patole, and M. Bulsara Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates Pediatrics 125 2010 921 930
112. P.B. Kale-Pradhan, H.K. Jassal, and S.M. Wilhelm Role of Lactobacillus in the prevention of antibiotic-associated diarrhea: a meta-analysis Pharmacotherapy 30 2010 119 126
113. B.C. Johnston, J.Z. Goldenberg, P.O. Vandvik, X. Sun, and G.H. Guyatt Probiotics for the prevention of pediatric antibiotic-associated diarrhea Cochrane database of Systematic Reviews 11 2011 CD004827
114. C. Hedin, K. Whelan, and J.O. Lindsay Evidence for the use of probiotics and prebiotics in inflammatory bowel disease: a review of clinical trials Proceedings of the Nutrition Society 66 2007 307 315
115. G.R. Gibson, and M.B. Roberfroid Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics Journal of Nutrition 125 1995 1401 1412
116. S.J. Langlands, M.J. Hopkins, N. Coleman, and J.H. Cummings Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel Gut 53 2004 1610 1616
117. S.H. Duncan, K.P. Scott, A.G. Ramsay, H.J. Harmsen, G.W. Welling, and C.S. Stewart Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system Applied and Environment Microbiology 69 2003 1136 1142
118. M. de Vrese, and P.R. Marteau Probiotics and prebiotics: effects on diarrhea Journal of Nutrition 137 Suppl. 2 2007 11S 803S
119. S. Fukuda, H. Toh, K. Hase, K. Oshima, Y. Nakanishi, and K. Yoshimura Bifidobacteria can protect from enteropathogenic infection through production of acetate Nature 469 2011 543 547
120. -/- mice Nature 487 2012 104 108
121. T. Hashimoto, T. Perlot, A. Rehman, J. Trichereau, H. Ishiguro, and M. Paolino ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation Nature 487 2012 477 481
122. A.L. Kau, P.P. Ahern, N.W. Griffin, A.L. Goodman, and J.I. Gordon Human nutrition, the gut microbiome and the immune system Nature 474 2011 327 336
123. M.J. Claesson, I.B. Jeffery, S. Conde, S.E. Power, E.M. O'Connor, and S. Cusack Gut microbiota composition correlates with diet and health in the elderly Nature 488 2012 178 184
124. G.H. McIntosh, M. Noakes, P.J. Royle, and P.R. Foster Whole-grain rye and wheat foods and markers of bowel health in overweight middle-aged men American Journal of Clinical Nutrition 77 2003 967 974
125. J. Slavin Why whole grains are protective: biological mechanisms Proceedings of the Nutrition Society 62 2003 129 134
126. C. De Filippo, D. Cavalieri, M. Di Paola, M. Ramazzotti, J.B. Poullet, and S. Massart Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa Proceedings of the National Academy of Sciences of the United States of America 107 2010 14691 14696
127. D.L. Topping, and P.M. Clifton Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides Physiological Reviews 81 2001 1031 1064
128. A. Schwiertz, U. Lehmann, G. Jacobasch, and M. Blaut Influence of resistant starch on the SCFA production and cell counts of butyrate-producing Eubacterium spp. in the human intestine Journal of Applied Microbiology 93 2002 157 162
129. J.G. Muir, E.G. Yeow, J. Keogh, C. Pizzey, A.R. Bird, and K. Sharpe Combining wheat bran with resistant starch has more beneficial effects on fecal indexes than does wheat bran alone American Journal of Clinical Nutrition 79 2004 1020 1028
130. V. Mai, and J.G. Morris Jr. Colonic bacterial flora: changing understandings in the molecular age Journal of Nutrition 134 2004 459 464
131. R. Palmer, and Fecal matters Nature Medicine 17 2011 150 152
132. J.S. Bakken, T. Borody, L.J. Brandt, J.V. Brill, D.C. Demarco, and M.A. Franzos Treating Clostridium difficile infection with fecal microbiota transplantation Clinical Gastroenterology and Hepatology 9 2011 1044 1049
133. J. Landy, H.O. Al-Hassi, S.D. McLaughlin, A.W. Walker, P.J. Ciclitira, and R.J. Nicholls Faecal transplantation therapy for gastrointestinal disease Alimentary Pharmacology and Therapeutics 34 2011 409 415
134. T.J. Borody, and A. Khoruts Fecal microbiota transplantation and emerging applications Nature Reviews Gastroenterology & Hepatology 9 2011 88 96
135. C.R. Kelly, L. de Leon, and N. Jasutkar Fecal microbiota transplantation for relapsing Clostridium difficile infection in 26 patients: methodology and results Journal of Clinical Gastroenterology 46 2012 145 149
136. M.S. Silverman, I. Davis, and D.R. Pillai Success of self-administered home fecal transplantation for chronic Clostridium difficile infection Clinical Gastroenterology and Hepatology 8 2010 471 473
137. M.J. Hamilton, A.R. Weingarden, M.J. Sadowsky, and A. Khoruts Standardized frozen preparation for transplantation of fecal microbiota for recurrent Clostridium difficile infection American Journal of Gastroenterology 107 2012 761 767
138. F.E. Dewhirst, T. Chen, J. Izard, B.J. Paster, A.C. Tanner, and W.H. Yu The human oral microbiome Journal of Bacteriology 192 2010 5002 5017
139. C. Dunne Adaptation of bacteria to the intestinal niche: probiotics and gut disorder Inflammatory Bowel Diseases 7 2001 136 145
140. E.M. Bik, P.B. Eckburg, S.R. Gill, K.E. Nelson, E.A. Purdom, and F. Francois Molecular analysis of the bacterial microbiota in the human stomach Proceedings of the National Academy of Sciences of the United States of America 103 2006 732 737
141. G.A. O'May, N. Reynolds, and G.T. Macfarlane Effect of pH on an in vitro model of gastric microbiota in enteral nutrition patients Applied and Environment Microbiology 71 2005 4777 4783
142. H. Hayashi, R. Takahashi, T. Nishi, M. Sakamoto, and Y. Benno Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism Journal of Medical Microbiology 54 2005 1093 1101
143. S.G. Jeon, H. Kayama, Y. Ueda, T. Takahashi, T. Asahara, and H. Tsuji Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon PLoS Pathogens 8 2012 e1002714
144. V. Liévin, I. Peiffer, S. Hudault, F. Rochat, D. Brassart, and J.R. Neeser Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity Gut 47 2000 646 652
145. M. Joossens, G. Huys, M. Cnockaert, V. De Preter, K. Verbeke, and P. Rutgeerts Dysbiosis of the faecal microbiota in patients with Crohn's disease and their unaffected relatives Gut 60 2011 631 637
146. S.M. Bloom, V.N. Bijanki, G.M. Nava, L. Sun, N.P. Malvin, and D.L. Donermeyer Commensal Bacteroides species induce colitis in host-genotype- specific fashion in a mouse model of inflammatory bowel disease Cell Host and Microbe 9 2011 390 403
147. A. Swidsinski, J. Weber, V. Loening-Baucke, L.P. Hale, and H. Lochs Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease Journal of Clinical Microbiology 43 2005 3380 3389
148. K.J. Rhee, S. Wu, X. Wu, D.L. Huso, B. Karim, and A.A. Franco Induction of persistent colitis by a human commensal, enterotoxigenic Bacteroides fragilis, in wild-type C57BL/6 mice Infection and Immunity 77 2009 1708 1718
149. S.K. Mazmanian, J.L. Round, and D.L. Kasper A microbial symbiosis factor prevents intestinal inflammatory disease Nature 453 2008 620 625
150. A. Khoruts, J. Dicksved, J.K. Jansson, and M.J. Sadowsky Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficile-associated diarrhea Journal of Clinical Gastroenterology 44 2010 354 360
151. V.B. Young, and T.M. Schmidt Antibiotic-associated diarrhea accompanied by large-scale alterations in the composition of the fecal microbiota Journal of Clinical Microbiology 42 2004 1203 1206
152. M. Issa, A.N. Ananthakrishnan, and D.G. Binion Clostridium difficile and inflammatory bowel disease Inflammatory Bowel Diseases 14 2008 1432 1442
153. S. Kang, S.E. Denman, M. Morrison, Z. Yu, J. Dore, and M. Leclerc Dysbiosis of fecal microbiota in Crohn's disease patients as revealed by a custom phylogenetic microarray Inflammatory Bowel Diseases 16 2010 2034 2042
154. X. Wang, and M.M. Huycke Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells Gastroenterology 132 2007 551 561
155. R. Balamurugan, E. Rajendiran, S. George, G.V. Samuel, and B.S. Ramakrishna Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis in the feces of patients with colorectal cancer Journal of Gastroenterology and Hepatology 23 2008 1298 1303
156. P. Lapaquette, M.A. Bringer, and A. Darfeuille-Michaud Defects in autophagy favour adherent-invasive Escherichia coli persistence within macrophages leading to increased pro-inflammatory response Cellular Microbiology 14 2012 791 807
157. M. Hafez, K. Hayes, M. Goldrick, G. Warhurst, R. Grencis, and I.S. Roberts The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction Infection and Immunity 77 2009 2995 3003
158. C. Högenauer, C. Langner, E. Beubler, I.T. Lippe, R. Schicho, and G. Gorkiewicz Klebsiella oxytoca as a causative organism of antibiotic-associated hemorrhagic colitis New England Journal of Medicine 355 2006 2418 2426
159. T.W. Miller, E.A. Wang, S. Gould, E.V. Stein, S. Kaur, and L. Lim Hydrogen sulfide is an endogenous potentiator of T cell activation Journal of Biological Chemistry 287 2012 4211 4221
160. P. Ruggiero Helicobacter pylori infection: what's new Current Opinion in Investigational Drugs 25 2012 337 344
161. J.R. Marchesi, B.E. Dutilh, N. Hall, W.H. Peters, R. Roelofs, and A. Boleij Towards the human colorectal cancer microbiome PLoS ONE 6 2011 e20447
162. A.D. Kostic, D. Gevers, C.S. Pedamallu, M. Michaud, F. Duke, and A.M. Earl Genomic analysis identifies association of Fusobacterium with colorectal carcinoma Genome Research 22 2012 292 298
163. M. Castellarin, R.L. Warren, J.D. Freeman, L. Dreolini, M. Krzywinski, and J. Strauss Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma Genome Research 22 2012 299 306
164. C. Belzer, and W.M. de Vos Microbes inside-from diversity to function: the case of Akkermansia The ISME Journal 6 2012 1449 1458
165. S.L. Gorbach, G. Neale, R. Levitan, and G.W. Hepner Alterations in human intestinal microflora during experimental diarrhoea Gut 11 1970 1 6
166. K. Endt, B. Stecher, S. Chaffron, E. Slack, N. Tchitchek, and A. Benecke The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea PLoS Pathogens 6 2010 e1001097
167. J. Wiström, S.R. Norrby, E.B. Myhre, S. Eriksson, G. Granström, and L. Lagergen Frequency of antibiotic-associated diarrhoea in 2462 antibiotic-treated hospitalized patients: a prospective study Journal of Antimicrobial Chemotherapy 47 2001 43 50
168. K.C. Carroll, and J.G. Bartlett Biology of Clostridium difficile: implications for epidemiology and diagnosis Annual Review of Microbiology 65 2011 501 521
169. P.D. Scanlan, F. Shanahan, C. O'Mahony, and J.R. Marchesi Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn's disease Journal of Clinical Microbiology 44 2006 3980 3988
170. U. Gophna, K. Sommerfeld, S. Gophna, W.F. Doolittle, and S.J. Veldhuyzen van Zanten Differences between tissue-associated intestinal microfloras of patients with Crohn's disease and ulcerative colitis Journal of Clinical Microbiology 44 2006 4136 4141
171. E.C. Claud Neonatal necrotizing enterocolitis-inflammation and intestinal immaturity Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry 8 2009 248 259
172. Y. Wang, J.D. Hoenig, K.J. Malin, S. Qamar, E.O. Petrof, and J. Sun 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis The ISME Journal 3 2009 944 954
173. B. Smith, S. Bodé, B.L. Petersen, T.K. Jensen, C. Pipper, and J. Kloppenborg Community analysis of bacteria colonizing intestinal tissue of neonates with necrotizing enterocolitis BMC Microbiology 11 2011 73
174. P. Munkholm The incidence and prevalence of colorectal cancer in inflammatory bowel disease Alimentary Pharmacology and Therapeutics 18 Suppl. 2 2003 1 5
175. T. Wang, G. Cai, Y. Qiu, N. Fei, M. Zhang, and X. Pang Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers The ISME Journal 6 2012 320 329
176. C.I. Gill, and I.R. Rowland Diet and cancer: assessing the risk British Journal of Nutrition 88 Suppl. 1 2002 S73 S87
177. S.H. Lee, L.L. Hu, J. Gonzalez-Navajas, G.S. Seo, C. Shen, and J. Brick ERK activation drives intestinal tumorigenesis in Apc(min/+) mice Nature Medicine 16 2010 665 670