Can inflammatory bowel disease be permanently treated with short-term interventions on the microbiome?

Expert Review of Gastroenterology and Hepatology

Volumn 9, Issue 6, 2015, Pages 781-795

  Berg, Dana ^a   Clemente, Jose C ^b   Colombel, Jean Frederic ^a  

^a MOUNT SINAI MEDICAL CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Antibiotics; diet; fecal microbiota transplantation; gut microbiota; gut microbiota modulation; inflammatory bowel disease; prebiotics; probiotics; resilience; stability; Stable microbiome

Indexed keywords

AMOXICILLIN; CIPROFLOXACIN; METRONIDAZOLE; PREBIOTIC AGENT; PROBIOTIC AGENT; RIFAXIMIN; TETRACYCLINE; ANTIINFECTIVE AGENT;

ANTIBIOTIC THERAPY; CLINICAL EFFECTIVENESS; CLOSTRIDIUM DIFFICILE INFECTION; CROHN DISEASE; DIET THERAPY; DISEASE COURSE; ENTERIC FEEDING; ESCHERICHIA COLI; FECES MICROFLORA; FEEDING BEHAVIOR; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; MICROBIOME; NONHUMAN; PATHOGENESIS; RELAPSE; REMISSION; REVIEW; THERAPY EFFECT; TREATMENT DURATION; TREATMENT RESPONSE; ULCERATIVE COLITIS; ADVERSE EFFECTS; COLITIS, ULCERATIVE; FECAL MICROBIOTA TRANSPLANTATION; INTESTINE; MICROBIOLOGY; MICROFLORA; RECURRENT DISEASE; TIME FACTOR; TREATMENT OUTCOME;

ANTI-BACTERIAL AGENTS; COLITIS, ULCERATIVE; CROHN DISEASE; FECAL MICROBIOTA TRANSPLANTATION; HUMANS; INTESTINES; MICROBIOTA; PROBIOTICS; RECURRENCE; REMISSION INDUCTION; TIME FACTORS; TREATMENT OUTCOME;

EID: 84929892612     PISSN: 17474124     EISSN: 17474132     Source Type: Journal    
DOI: 10.1586/17474124.2015.1013031     Document Type: Review

References (94)

1. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006;124(4):837-48
2. Qin J, Li R, Raes J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464(7285):59-65
3. Koenig JE, Spor A, Scalfone N, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci USA 2011;108(Suppl 1): 4578-85
4. Palmer C, Bik EM, DiGiulio DB, et al. Development of the human infant intestinal microbiota. PLoS Biol 2007;5(7):e177
5. Hedin C, Whelan K, Lindsay JO. Evidence for the use of probiotics and prebiotics in inflammatory bowel disease: a review of clinical trials. Proc Nutr Soc 2007;66(3): 307-15
6. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev 2010;90(3):859-904
7. Xu J, Gordon JI. Honor thy symbionts. Proc Natl Acad Sci USA 2003;100(18): 10452-9
8. Sha S, Xu B, Wang X, et al. The biodiversity and composition of the dominant fecal microbiota in patients with inflammatory bowel disease. Diagn Microbiol Infect Dis 2013;75(3):245-51
9. de Wouters T, Dore J, Lepage P. Does our food (environment) change our gut microbiome ('in-vironment'): a potential role for inflammatory bowel disease Dig Dis 2012;30(Suppl 3):33-9
10. Hold GL, Smith M, Grange C, et al. Role of the gut microbiota in inflammatory bowel disease pathogenesis: what have we learnt in the past 10 years World J Gastroenterol 2014;20(5):1192-210
11. 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(34):13780-5
12. Sartor B. Microbial influences in inflammatory bowel diseases. Gastroenterology 2008;134(2):577-94
13. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 2014;15(3):382-92
14. Anderson JL, Edney RJ, Whelan K. Systematic review: faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther 2012;36(6):503-16
15. Scaldaferri F, Gerardi V, Lopetuso LR, et al. Gut Microbial Flora, Prebiotics, and Probiotics in IBD: their Current Usage and Utility. Biomed Res Int 2013;2013:435268
16. Lewis JD, Ruemmele FM, Wu GD. Nutrition, gut microbiota and immunity: therapeutic targets for IBD. Concluding remarks. Nestle Nutr Inst Workshop Ser 2014;79:161-2
17. Kanauchi O, Iwanaga T, Mitsuyama K. Germinated barley foodstuff feeding. A novel neutraceutical therapeutic strategy for ulcerative colitis. Digestion 2001; 63(Suppl 1):60-7
18. Lindsay JO, Whelan K, Stagg AJ, et al. Clinical, microbiological, and immunological effects of fructo-oligosaccharide in patients with Crohn's disease. Gut 2006;55(3):348-55
19. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334(6052):105-8
20. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014; 505(7484):559-63
21. Angelberger S, Reinisch W, Makristathis A, et al. Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am J Gastroenterol 2013; 108(10):1620-30
22. De La Cochetière MF, Durand T, Lepage P, et al. Resilience of the dominant human fecal microbiota upon short-course antibiotic challenge. J Clin Microbiol 2005;43(11): 5588-92
23. Brumfitt W, Franklin I, Grady D, et al. Changes in the pharmacokinetics of ciprofloxacin and fecal flora during administration of a 7-day course to human volunteers. Antimicrob Agents Chemother 1984;26(5):757-61
24. Faith JJ, Guruge JL, Charbonneau M, et al. The long-term stability of the human gut microbiota. Science 2013;341(6141): 1237439
25. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 2008;6(11):e280
26. 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(4):661-73
27. Albenberg LG, Lewis JD, Wu GD. Food and the gut microbiota in inflammatory bowel diseases: a critical connection. Curr Opin Gastroenterol 2012;28(4):314-20
28. Andres PG, Friedman LS. Epidemiology and the natural course of inflammatory bowel disease. Gastroenterol Clin North Am 1999;28(2):255-81, vii
29. Koutroubakis I, Manousos ON, Meuwissen SG, Pena AS. Environmental risk factors in inflammatory bowel disease. Hepatogastroenterology 1996;43(8):381-93
30. Spehlmann ME, Begun AZ, Burghardt J, et al. Epidemiology of inflammatory bowel disease in a German twin cohort: results of a nationwide study. Inflamm Bowel Dis 2008;14(7):968-76
31. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol 2011;106(4): 563-73
32. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012;142(1):46-54; e42; quiz e30
33. Chapman-Kiddell CA, Davies PS, Gillen L, Radford-Smith GL. Role of diet in the development of inflammatory bowel disease. Inflamm Bowel Dis 2010;16(1):137-51
34. Cordain L, Eaton SB, Sebastian A, et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 2005;81(2):341-54
35. Devkota S, Wang Y, Musch MW, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/-mice. Nature 2012;487(7405): 104-8
36. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010;107(33): 14691-6
37. Yatsunenko T, Rey FE, Manary MJ, et al. Human gut microbiome viewed across age and geography. Nature 2012;486(7402): 222-7
38. Muegge BD, Kuczynski J, Knights D, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 2011;332(6032): 970-4
39. Caprilli R, Gassull MA, Escher JC, et al. European evidence based consensus on the diagnosis and management of Crohn's disease: special situations. Gut 2006;55 (Suppl 1):i36-58
40. Day AS, Whitten KE, Lemberg DA, et al. Exclusive enteral feeding as primary therapy for Crohn's disease in Australian children and adolescents: a feasible and effective approach. J Gastroenterol Hepatol 2006; 21(10):1609-14
41. Sandhu BK, Fell JM, Beattie RM, et al. Guidelines for the management of inflammatory bowel disease in children in the United Kingdom. J Pediatr Gastroenterol Nutr 2010;50(Suppl 1):S1-13
42. Lionetti P, Callegari ML, Ferrari S, et al. Enteral nutrition and microflora in pediatric Crohn's disease. JPEN J Parenter Enteral Nutr 2005;29(4 Suppl):S173-5; discussion S175-8, S184-8
43. Shiga H, Kajiura T, Shinozaki J, et al. Changes of faecal microbiota in patients with Crohn's disease treated with an elemental diet and total parenteral nutrition. Dig Liver Dis 2012;44(9):736-42
44. D'Argenio V, Precone V, Casaburi G, et al. An altered gut microbiome profile in a child affected by Crohn's disease normalized after nutritional therapy. Am J Gastroenterol 2013;108(5):851-2
45. Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 1995;125(6):1401-12
46. Damaskos D, Kolios G. Probiotics and prebiotics in inflammatory bowel disease: microflora 'on the scope'. Br J Clin Pharmacol 2008;65(4):453-67
47. Govers MJ, Gannon NJ, Dunshea FR, et al. Wheat bran affects the site of fermentation of resistant starch and luminal indexes related to colon cancer risk: a study in pigs. Gut 1999;45(6):840-7
48. Saëmann MD, Böhmig GA, Osterreicher CH, et al. Anti-inflammatory effects of sodium butyrate on human monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J 2000;14(15):2380-2
49. Kleessen B, Hartmann L, Blaut M. Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora. Br J Nutr 2001;86(2):291-300
50. Videla S, Vilaseca J, Antoĺn M, et al. Dietary inulin improves distal colitis induced by dextran sodium sulfate in the rat. Am J Gastroenterol 2001;96(5):1486-93
51. Hoentjen F, Welling GW, Harmsen H, et al. Reduction of colitis by prebiotics in HLA-B27 transgenic rats is associated with microflora changes and immunomodulation. Inflamm Bowel Dis 2005;11(11):977-85
52. Benjamin JL, Hedin CR, Koutsoumpas A, et al. Randomised, double-blind, placebo-controlled trial of fructo-oligosaccharides in active Crohn's disease. Gut 2011;60(7):923-9
53. Welters CF, Heineman E, Thunnissen FB, et al. Effect of dietary inulin supplementation on inflammation of pouch mucosa in patients with an ileal pouch-anal anastomosis. Dis Colon Rectum 2002; 45(5):621-7
54. Cary VA, Boullata J. What is the evidence for the use of probiotics in the treatment of inflammatory bowel disease J Clin Nurs 2010;19(7-8):904-16
55. Rioux KP, Fedorak RN. Probiotics in the treatment of inflammatory bowel disease. J Clin Gastroenterol 2006;40(3):260-3
56. Gionchetti P, Rizzello F, Venturi A, et al. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology 2000;119(2):305-9
57. Gionchetti P, Rizzello F, Helwig U, et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 2003;124(5):1202-9
58. Rembacken BJ, Snelling AM, Hawkey PM, et al. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 1999; 354(9179):635-9
59. Kruis W, Fric P, Pokrotnieks J, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004;53(11):1617-23
60. Naidoo K, Gordon M, Fagbemi AO, et al. Probiotics for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev 2011(12):CD007443
61. Mallon P, McKay D, Kirk S, et al. Probiotics for induction of remission in ulcerative colitis. Cochrane Database Syst Rev 2007(4):CD005573
62. Meijer BJ, Dieleman LA. Probiotics in the treatment of human inflammatory bowel diseases: update 2011. J Clin Gastroenterol 2011;45(Suppl):S139-44
63. Venturi A, Gionchetti P, Rizzello F, et al. Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther 1999;13(8):1103-8
64. Prantera C, Scribano ML. Antibiotics and probiotics in inflammatory bowel disease: why, when, and how. Curr Opin Gastroenterol 2009;25(4):329-33
65. Colombel JF, Lemann M, Cassagnou M, et al. A controlled trial comparing ciprofloxacin with mesalazine for the treatment of active Crohn's disease. Groupe d'etudes therapeutiques des affections inflammatoires digestives (GETAID). Am J Gastroenterol 1999;94(3):674-8
66. Wang SL, Wang ZR, Yang CQ. Meta-analysis of broad-spectrum antibiotic therapy in patients with active inflammatory bowel disease. Exp Ther Med 2012;4(6): 1051-6
67. Wolfson JS, Hooper DC. Fluoroquinolone antimicrobial agents. Clin Microbiol Rev 1989;2(4):378-424
68. Madden MV, McIntyre AS, Nicholls RJ. Double-blind crossover trial of metronidazole versus placebo in chronic unremitting pouchitis. Dig Dis Sci 1994; 39(6):1193-6
69. Shen B, Remzi FH, Lopez AR, Queener E. Rifaximin for maintenance therapy in antibiotic-dependent pouchitis. BMC Gastroenterol 2008;8:26
70. Swidsinski A, Loening-Baucke V, Bengmark S, et al. Bacterial biofilm suppression with antibiotics for ulcerative and indeterminate colitis: consequences of aggressive treatment. Arch Med Res 2008; 39(2):198-204
71. Koido S, Ohkusa T, Kajiura T, et al. Long-term alteration of intestinal microbiota in patients with ulcerative colitis by antibiotic combination therapy. PLoS One 2014;9(1):e86702
72. Walsh CJ, Guinane CM, O'Toole PW, et al. Beneficial modulation of the gut microbiota. FEBS Lett 2014;588(22): 4120-30
73. Koo HL, DuPont HL. Rifaximin: a unique gastrointestinal-selective antibiotic for enteric diseases. Curr Opin Gastroenterol 2010; 26(1):17-25
74. Scarpignato C, Pelosini I. Rifaximin, a poorly absorbed antibiotic: pharmacology and clinical potential. Chemotherapy 2005; 51(Suppl 1):36-66
75. Prantera C, Lochs H, Grimaldi M, et al. Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn's disease. Gastroenterology 2012; 142(3):473-81; e4
76. Jigaranu AO, Nedelciuc O, Blaj A, et al. Is rifaximin effective in maintaining remission in Crohn's disease Dig Dis 2014;32(4): 378-83
77. Maccaferri S, Vitali B, Klinder A, et al. Rifaximin modulates the colonic microbiota of patients with Crohn's disease: an in vitro approach using a continuous culture colonic model system. J Antimicrob Chemother 2010;65(12):2556-65
78. Surawicz CM, Brandt LJ, Binion DG, et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 2013;108(4): 478-98; quiz 499
79. 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
80. Vindigni SM, Broussard EK, Surawicz CM. Alteration of the intestinal microbiome: fecal microbiota transplant and probiotics for Clostridium difficile and beyond. Expert Rev Gastroenterol Hepatol 2013;7(7): 615-28
81. 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):1079-87
82. Guo B, Harstall C, Louie T, et al. Systematic review: faecal transplantation for the treatment of Clostridium difficile-associated disease. Aliment Pharmacol Ther 2012;35(8):865-75
83. Hamilton MJ, Weingarden AR, Unno T, et al. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes 2013;4(2):125-35
84. Sokol H, Seksik P, Furet JP. Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 2009;15(8): 1183-9
85. Borody TJ, Campbell J. Fecal microbiota transplantation: current status and future directions. Expert Rev Gastroenterol Hepatol 2011;5(6):653-5
86. Kunde S, Pham A, Bonczyk S, et al. Safety, tolerability, and clinical response after fecal transplantation in children and young adults with ulcerative colitis. J Pediatr Gastroenterol Nutr 2013;56(6):597-601
87. Borody TJ, Brandt LJ, Paramsothy S. Therapeutic faecal microbiota transplantation: current status and future developments. Curr Opin Gastroenterol 2014;30(1):97-105
88. Borody TJ, Warren EF, Leis S, et al. Treatment of ulcerative colitis using fecal bacteriotherapy. J Clin Gastroenterol 2003; 37(1):42-7
89. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486(7402):207-14
90. 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(43):16731-6
91. Sokol H. Probiotics and Antibiotics in IBD. Dig Dis 2014;32(Suppl 1):10-17
92. Steidler L, Hans W, Schotte L, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 2000; 289(5483):1352-5
93. 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(6032):974-7
94. Damman CJ, Miller SI, Surawicz CM, et al. The microbiome and inflammatory bowel disease: is there a therapeutic role for fecal microbiota transplantation Am J Gastroenterol 2012;107(10):1452-9