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Probiotics, Prebiotics, and Antibiotics in IBD

  • Paolo GionchettiEmail author
  • Carlo Calabrese
  • Andrea Calafiore
  • Fernando Rizzello
Chapter

Abstract

The rationale for using probiotics, prebiotics, and antibiotics in IBD is based on convincing evidence that implicates intestinal bacteria in the pathogenesis of the disease.

Probiotics are “living organisms, which upon ingestion in certain numbers, exert health benefits beyond inherent basic nutrition.” Several mechanisms have been proposed to account for the action of probiotics. These include antagonistic activity against pathogenic bacteria, either by inhibition of adherence and translocation, or by production of antibacterial substances such as antimicrobial peptides and hydrogen peroxide. Probiotics also stimulate mucosal defense, both at the level of immune and epithelial function. Encouraging results have been obtained with probiotic therapy in experimental colitis. VSL#3, a highly concentrated cocktail of probiotics has been shown to be effective in the prevention of pouchitis onset and relapses. Results on the use of probiotics in UC are promising, both in terms of the prevention of relapses and the treatment of mild-to-moderate attacks. Results in Crohn’s disease are not yet clear because of conflicting data and the limited number of well-performed studies.

Prebiotics are dietary substances, usually nondigestible carbohydrates, which beneficially affect the host by selectively stimulating the growth and activity of protective commensal enteric bacteria. Evidence supporting the use of these nutraceuticals in IBD is still limited.

The use of antibiotics in UC is not supported by the available studies. Antibiotics have an essential role in treating the septic complications of Crohn’s disease, including intra-abdominal and perianal abscesses and perianal fistulae.

The use of antibiotics in pouchitis is largely justified although proper controlled trials have not been conducted.

Keywords

Probiotics Prebiotics Antibiotics Pouchitis Crohn’s disease Ulcerative colitis 

References

  1. 1.
    Guarner F, Casellas F, Borruel N, Antolín M, Videla S, Vilaseca J, et al. Role of microecology in chronic inflammatory bowel diseases. Eur J Clin Nutr. 2002;56:S34–8.PubMedCrossRefGoogle Scholar
  2. 2.
    Neut C, Bulois P, Desreumaux P, Membré JM, Lederman E, Gambiez L, et al. Changes in the bacterial flora of the neoterminal ileum after ileocolonic resection for Crohn’s disease. Am J Gastroenterol. 2002;97:939–46.PubMedCrossRefGoogle Scholar
  3. 3.
    Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, et al. Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut. 2006;55:205–11.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, et al. Low counts of fecalibacterium pausnitzii in colitis microbiota. Inflamm Bowel Dis. 2009;15:1183–9.PubMedCrossRefGoogle Scholar
  5. 5.
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermúdez-Humarán LG, Gratadoux JJ, et al. Fecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn’ disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–6.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Duchmann R, Kaiser I, Hermann E, Mayet W, Ewe K, Meyer zum Büschenfelde KH. Tolerance exist towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol. 1995;102:445–7.Google Scholar
  7. 7.
    Janowitz HD, Croen EC, Sachar DB. The role of the faecal stream in Crohn’s disease: an historical and analytic perspective. Inflamm Bowel Dis. 1998;4:29–39.PubMedCrossRefGoogle Scholar
  8. 8.
    D’Haens GR, Geboes K, Peeters M, Baert F, Penninckx F, Rutgeerts P. Early lesions of recurrent Crohn’s disease caused by infusion of intestinal contents in excluded ileum. Gastroenterology. 1998;114:771–4.Google Scholar
  9. 9.
    Abdelrazeq AS, Kadiyil N, Botterill ID, Lund JN, Reynolds JR, Holdsworth PJ, et al. Predictors for acute and chronic pouchitis following restorative proctocolectomy for ulcerative colitis. Colorectal Dis. 2007;10:805–13.PubMedCrossRefGoogle Scholar
  10. 10.
    Sartor RB. Insights into the pathogenesis of inflammatory bowel disease provided by new rodent models of spontaneous colitis. Inflamm Bowel Dis. 1995;1:64–75.Google Scholar
  11. 11.
    Campieri M, Gionchetti P. Probiotics in inflammatory bowel disease: new insight to pathogenesis or a possible therapeutic alternative? Gastroenterology. 1999;116:1246–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Metchnikoff E. The prolongation of life: optimistic studies. London: William Heinemann; 1907. p. 161–83.Google Scholar
  13. 13.
    Schaafsma G. State of the art concerning probiotic strains in milk products. IDF Nutr Newsl. 1996;5:23–4.Google Scholar
  14. 14.
    Lee YK, Salminen S. The coming age of probiotics. Trends Food Sci Technol. 1995;6:241–5.CrossRefGoogle Scholar
  15. 15.
    Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC. Mechanism of action of probiotics: recent advances. Inflamm Bowel Dis. 2009;15:300–10.PubMedCrossRefGoogle Scholar
  16. 16.
    Fabia R, Ar’rajab A, Johansson M-L, Willén R, Andersson R, Molin G, et al. The effect of exogenous administration of Lactobacillus reuteri R2LC and oat fiber on acetic acid-induced colitis in the rat. Scand J Gastroenterol. 1993;28:155–62.PubMedCrossRefGoogle Scholar
  17. 17.
    Mao Y, Nobaek S, Kasravi B, Adawi D, Stenram U, Molin G, et al. The effects of Lactobacillus strains and oat fibre on methotrexate-induced enterocolitis in rats. Gastroenterology. 1996;111:334–44.PubMedCrossRefGoogle Scholar
  18. 18.
    Madsen KL, Tavernini MM, Doyle JSG, Tavernini MM, Fedorak RN. Lactobacillus sp. prevents development of enterocolitis in interleukin-10 gene-deficient mice. Gastroenterology. 1999;116:1107–14.PubMedCrossRefGoogle Scholar
  19. 19.
    Schultz M, Veltkamp C, Dieleman LA, Grenther WB, Wyrick PB, Tonkonogy SL, et al. Lactobacillus plantarum 299 V in the treatment and prevention of spontaneous colitis in interleukin-10 deficient mice. Inflamm Bowel Dis. 2002;8:71–80.PubMedCrossRefGoogle Scholar
  20. 20.
    O’Mahony L, Feeney M, O’Halloran S, Murphy L, Kiely B, Fitzgibbon J, et al. Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment Pharmacol Ther. 2001;15:1219–25.PubMedCrossRefGoogle Scholar
  21. 21.
    McCarthy J, O’Mahony L, O’Callaghan L, Murphy L, Kiely B, Fitzgibbon J, et al. Double-blind, placebo-controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut. 2003;52:975–80.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Shibolet O, Karmeli F, Eliakim R, Swennen E, Brigidi P, Gionchetti P, et al. Variable response to probiotics in two models of experimental colitis in rats. Inflamm Bowel Dis. 2002;8:399–408.PubMedCrossRefGoogle Scholar
  23. 23.
    Madsen K, Cornish A, Soper P, McKaigney C, Jijon H, Yachimec C, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001;121:580–91.PubMedCrossRefGoogle Scholar
  24. 24.
    Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F. Probiotics promotes gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci U S A. 2010;107:454–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Kruis W, Schuts E, Fric P, Fixa B, Judmaier G, Stolte M. Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther. 1997;11:853–8.PubMedCrossRefGoogle Scholar
  26. 26.
    Rembacken BJ, Snelling AM, Hawkey P, Chalmers DM, Axon AT. Non pathogenic Escherichia coli vs mesalazine for the treatment of ulcerative colitis: a randomized trial. Lancet. 1999;354:635–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Kruis W, Fric P, Pokrotnieks J, Lukás M, Fixa B, Kascák M, et al. Maintaining remission of ulcerative colitis with Escherichia Coli Nissle 1917 is as effective as with standard mesalazine. Gut. 2004;53:1617–23.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Matthes H, Krummenerl T, Giensch M, Wolff C, Schulze J. Clinical trial: probiotic treatment of acute distal ulcerative colitis with rectally administered Escherichia coli Nissle 1917 (EcN). BMC Complement Altern Med. 2010;10:13–20.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T. Randomized, controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J Am Coll Nutr. 2003;22:56–63.PubMedCrossRefGoogle Scholar
  30. 30.
    Guslandi M, Giollo P, Testoni PA. A pilot trial of Saccharomyces boulardii in ulcerative colitis. Eur J Gastroenterol Hepatol. 2003;15:697–8.PubMedCrossRefGoogle Scholar
  31. 31.
    Venturi A, Gionchetti P, Rizzello F, Johansson R, Zucconi E, Brigidi P, et al. Impact on the faecal flora composition of a new probiotic preparation. Preliminary data on maintenance treatment of patients with ulcerative colitis (UC) intolerant or allergic to 5-aminosalicylic acid (5 ASA). Aliment Pharmacol Ther. 1999;13:1103–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, et al. VSL#3 probiotic mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol. 2005;100:1539–46.PubMedCrossRefGoogle Scholar
  33. 33.
    Sood A, Midha V, Makharia GK, Ahuja V, Singal D, Goswami P, et al. The probiotic preparation, VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis. Clin Gastroenterol Hepatol. 2009;7:1202–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Tursi A, Brandimarte G, Papa A, Giglio A, Elisei W, Giorgetti GM, et al. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol. 2010;105(10):2218–27. doi: 10.1038/ajg.2010.218. Epub 2010 Jun 1.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Miele E, Pascarella F, Riannetti E, Quaglietta L, Baldassano RN, Staiano A. Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol. 2009;104:437–43.PubMedCrossRefGoogle Scholar
  36. 36.
    Huynh HQ, de Bruin J, Guan L, Diaz H, Li M, Girgis S, et al. Probiotic preparation VSL#3 induces remission in children with mild to moderate acute ulcerative colitis: a pilot study. Inflamm Bowel Dis. 2009;15:760–8.PubMedCrossRefGoogle Scholar
  37. 37.
    Pardi DS, D’Haens G, Shen B, Campbell S, Gionchetti P. Clinical guidelines for the management of pouchitis. Inflamm Bowel Dis. 2009;15:1424–31.PubMedCrossRefGoogle Scholar
  38. 38.
    Fazio VW, Ziv Y, Church JM, Oakley JR, Lavery IC, Milsom JW, et al. Ileal pouch-anal anastomoses complications and function in 1005 patients. Ann Surg. 1995;222:120–7.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Sandborn WJ. Pouchitis following ileal pouch-anal anastomosis: definition, pathogenesis, and treatment. Gastroenterology. 1994;107:1856–60.PubMedCrossRefGoogle Scholar
  40. 40.
    Hurst RD, Molinari M, Chung TP, Rubin M, Michelassi F. Prospective study of the incidence, timing and treatment of pouchitis in 104 consecutive patients after restorative proctocolectomy. Arch Surg. 1996;131:497–500. discussion 501–2.PubMedCrossRefGoogle Scholar
  41. 41.
    Meagher AP, Farouk R, Dozois RR, Kelly KA, Pemberton JH. J ileal pouch-anal anastomosis for chronic ulcerative colitis: complications and long-term outcome in 1310 patients. Br J Surg. 1998;85:800–3.PubMedCrossRefGoogle Scholar
  42. 42.
    Penna C, Dozois R, Tremaine W, Sandborn W, LaRusso N, Schleck C, et al. Pouchitis after ileal pouch-anal anastomosis for ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitis. Gut. 1996;38:234–9.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Simchuk EJ, Thirlby RC. Risk factors and true incidence of pouchitis in patients after ileal pouch-anal anastomoses. World J Surg. 2000;24:851–6.PubMedCrossRefGoogle Scholar
  44. 44.
    Stahlberg D, Gullberg K, Liljeqvist L, Hellers G, Lofberg R. Pouchitis following pelvic pouch operation for ulcerative colitis. Incidence, cumulative risk, and risk factors. Dis Colon Rectum. 1996;39:1012–8.PubMedCrossRefGoogle Scholar
  45. 45.
    Shen B. Pouchitis: what every gastroenterologist needs to know. Clin Gastroenterol Hepatol. 2013;11:1538–49.PubMedCrossRefGoogle Scholar
  46. 46.
    Shen B, Achkar JP, Lashner BA, Ormsby AH, Remzi FH, Bevins CL, et al. Endoscopic and histologic evaluation together with symptom assessment are required to diagnose pouchitis. Gastroenterology. 2001;121:261–7.PubMedCrossRefGoogle Scholar
  47. 47.
    Pardi DS, Shen B. Endoscopy in the management of patients after ileal pouch surgery for ulcerative colitis. Endoscopy. 2008;40:529–33.PubMedCrossRefGoogle Scholar
  48. 48.
    Sandborn WJ, Tremaine WJ, Batts KP, Pemberton JH, Phillips SF. Pouchitis after ileal pouch-anal anastomosis: a pouchitis disease activity index. Mayo Clin Proc. 1994;69:409–15.PubMedCrossRefGoogle Scholar
  49. 49.
    Landy J, Al-Hassi HO, McLaughlin SD, Knight SC, Ciclitira PJ, Nicholls RJ, et al. Etiology of pouchitis. Inflamm Bowel Dis. 2012;18:1146–55.PubMedCrossRefGoogle Scholar
  50. 50.
    Batista D, Raffals L. Role of intestinal bacteria in the pathogenesis of pouchitis. Inflamm Bowel Dis. 2014;20:1481–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Nicholls RJ, Belliveau P, Neill M, Wilks M, Tabaqchali S. Restorative proctocolectomy withileal reservoir: a pathophysiological assessment. Gut. 1981;22:462–8.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Santavirta J, Mattila J, Kokki M, Matikainen M. Mucosal morphology and fecal bacteriology after ileoanal anastomosis. Int J Colorectal Dis. 1991;6:38.PubMedCrossRefGoogle Scholar
  53. 53.
    Ruseler-van-Embden JGH, Schouten WR, van Lieshout LMC. Pouchitis: result of microbial imbalance? Gut. 1994;35:658–64.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Meier CB, Hegazi RA, Aisenberg J, Legnani PE, Nilubol N, Cobrin GM, et al. Innate immune receptor genetic polymorphisms in pouchitis: is CARD15 a susceptibility factor? Inflamm Bowel Dis. 2005;11:965–71.PubMedCrossRefGoogle Scholar
  55. 55.
    Tyler AD, Milgrom R, Stempak JM, Xu W, Brumell JH, Muise AM, et al. The NOD2insC polymorphismis associated with worse outcome following ileal pouch-anal anastomosisfor ulcerative colitis. Gut. 2013;62:1433–9.PubMedCrossRefGoogle Scholar
  56. 56.
    Carter MJ, Di Giovine FS, Cox A, Goodfellow P, Jones S, Shorthouse AJ, et al. The interleukin 1 receptor antagonist gene allele 2 as a predictor of pouchitis following colectomyand IPAA in ulcerative colitis. Gastroenterology. 2001;121:805–11.PubMedCrossRefGoogle Scholar
  57. 57.
    Lammers KM, Ouburg S, Morre SA, Crusius JB, Gionchett P, Rizzello F, et al. Combined carriership of TLR9-1237C and CD14-260T alleles enhances the risk of developing chronic relapsing pouchitis. World J Gastroenterol. 2005;11:7323–9.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Gionchetti P, Rizzello F, Venturi A, Brigidi P, Matteuzzi D, Bazzocchi G, et al. Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology. 2000;119:305–9.PubMedCrossRefGoogle Scholar
  59. 59.
    Mimura T, Rizzello F, Helwig U, Poggioli G, Schreiber S, Talbot IC, et al. Once daily high dose probiotic therapy for maintaining remission in recurrent or refractory pouchitis. Gut. 2004;53:108–14.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Ulisse S, Gionchetti P, D’Alò S, Russo FP, Pesce I, Ricci G, et al. Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: effects of probiotic treatment. Gastroenterology. 2001;96:2691–9.Google Scholar
  61. 61.
    Shen B, Brzezinski A, Fazio VW, Remzi FH, Achkar JP, Bennett AE, et al. Maintenance therapy with a probiotic in antibiotic-dependent pouchitis: experience in clinical practice. Aliment Pharmacol Ther. 2005;22:721–8.PubMedCrossRefGoogle Scholar
  62. 62.
    Kuisma J, Mentula S, Kahri A, Kahri A, Saxelin M, Farkkila M. Effect of Lactobacillus rhamnosus GG on ileal pouch inflammation and microbial flora. Aliment Pharmacol Ther. 2003;17:509–15.PubMedCrossRefGoogle Scholar
  63. 63.
    Persborn M, Gerritsen J, Wallon C, Carlsson A, Akkermans LM, Söderholm JD. The effects of probiotics on barrier function and mucosal pouch microbiota during maintenance treatment for severe pouchitis in patients with ulcerative colitis. Aliment Pharmacol Ther. 2013;38:772–83.PubMedCrossRefGoogle Scholar
  64. 64.
    Gionchetti P, Rizzello F, Helwig U, Venturi A, Lammers KM, Brigidi P, et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology. 2003;124(5):1202–9.PubMedCrossRefGoogle Scholar
  65. 65.
    Gionchetti P, Rizzello F, Morselli C, Poggioli G, Tambasco R, Calabrese C, et al. High-dose probiotics for the treatment of active pouchitis. Dis Colon Rectum. 2007;50:2075–82.PubMedCrossRefGoogle Scholar
  66. 66.
    Holubar SD, Cima RR, Sandborn WJ, Pardi DS. Treatment and prevention of pouchitis after ileal-pouch anal anastomosis for ulcerative colitis. Cochrane Database Syst Rev. 2010;6:CD001176.Google Scholar
  67. 67.
    Biancone L, Michetti P, Travis S, Escher JC, Moser G, Forbes A, et al. European evidence-based Consensus in the management of ulcerative colitis: special situations. JCC. 2008;2:63–92.PubMedGoogle Scholar
  68. 68.
    Malchow HA. Crohn’s disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn’s disease? J Clin Gastroenterol. 1997;25:653–8.PubMedCrossRefGoogle Scholar
  69. 69.
    Guslandi M, Mezzi G, Sorghi M, Testoni PA. Saccharomyces boulardii in maintenance treatment of Crohn’s disease. Dig Dis Sci. 2000;45:1462–4.PubMedCrossRefGoogle Scholar
  70. 70.
    Prantera C, Scribano ML, Falasco G, Andreoli A, Luzi C. Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn’s disease: a randomized controlled trial with Lactobacillus GG. Gut. 2002;51:405–9.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Bousvaros A, Guandalini S, Baldassano RN, Botelho C, Evans J, Ferry GD, et al. A randomized, double-blind trial of Lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn’s disease. Inflamm Bowel Dis. 2005;11:833–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Marteau P, Lemann M, Seksik P, Laharie D, Colombel JF, Bouhnik Y, et al. Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of post-operative recurrence in Crohn’s disease: a randomized, double-blind, placebo-controlled GETAID trial. Gut. 2006;55:842–7.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Van Gossum A, Dewit O, Louis E, de Hertogh G, Baert F, Fontaine F, et al. Multicenter, randomized-controlled clinical trial (Lactobacillus Johnsonii LA1) on early endoscopic recurrence of Crohn’s disease after ileo-caecal resection. Inflamm Bowel Dis. 2007;13:135–42.PubMedCrossRefGoogle Scholar
  74. 74.
    Bourreille A, Cadiot G, Le Dreau G, Laharie D, Beaugerie L, Dupas JL, et al. Saccharomyces boulardii does not prevent relapse of Crohn’s disease. Clin Gastroenterol Hepatol. 2013;11:982–7.PubMedCrossRefGoogle Scholar
  75. 75.
    Campieri M, Rizzello F, Venturi A, Poggioli G, Ugolini F. Combination of antibiotic and probiotic treatment is efficacious in prophylaxis of post-operative recurrence of Crohn’s disease: a randomized controlled study VS mesalamine. Gastroenterology. 2000;118:A781.Google Scholar
  76. 76.
    Willert RP, Peddi KK, Ombiga J, Bampton PA, Lawrance IC. Randomised, double-blinded, placebo-controlled study of VSL#3 versus placebo in the maintenance of remission in Crohn’s disease. Gastroenterology. 2010;138 Suppl 1:T1235.Google Scholar
  77. 77.
    Fedorak RN, Feagan BG, Hotte N, Leddin D, Dieleman LA, Petrunia DM, et al. The probiotic VSL#3 has anti-inflammatory effects and could reduce endoscopic recurrence after surgery for Crohn’s Disease. Clin Gastroenterol Hepatol. 2015;13:928–35.PubMedCrossRefGoogle Scholar
  78. 78.
    Gibson GR, Roberfroid MB. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr. 1995;125:1401–12.PubMedGoogle Scholar
  79. 79.
    Jacobasch G, Schmiedl D, Kruschewski M, Schmehl K. Dietary resistant starch and chronic inflammatory bowel diseases. Int J Colorectal Dis. 1999;14:201–11.PubMedCrossRefGoogle Scholar
  80. 80.
    Videla S, Vilaseca J, Antolin M, García-Lafuente A, Guarner F, Crespo E, et al. Dietary inulin improves distal colitis induced by dextran sodium sulphate in the rat. Am J Gastroenterol. 2001;96:1486–93.PubMedCrossRefGoogle Scholar
  81. 81.
    Araki Y, Andoh A, Koyama S, Fujiyama Y, Kanauchi O, Bamba T. Effects of germinated barley foodstuff on microflora and short chain fatty acid production in dextran sulfate sodium-induced colitis in rats. Biosci Biotechnol Biochem. 2000;64:1794–800.PubMedCrossRefGoogle Scholar
  82. 82.
    Cherbut C, Michel C, Lecannu G. The prebiotic characteristics of fructo-oligasaccharides are necessary for necessary for reduction of TNBS-induced colitis in rats. J Nutr. 2003;90:75–85.CrossRefGoogle Scholar
  83. 83.
    Moreau NM, Martin LI, Toquet CS, Laboisse CL, Nguyen PG, Siliart BS, et al. Restoration of the integrity of rat caeco-colonic mucosa by resistant starch, but not by fructo-oligosaccharides, in dextran sulfate sodium-induced experimental colitis. Br J Nutr. 2003;90:75–85.PubMedCrossRefGoogle Scholar
  84. 84.
    Hoentjen F, Welling GW, Harmsen HJ, Zhang X, Snart J, Tannock GW, 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.PubMedCrossRefGoogle Scholar
  85. 85.
    Hallert C, Kaldma M, Petersson BG. Ispaghula husk may relieve gastrointestinal symptoms in ulcerative colitis in remission. Scand J Gastroenterol. 1991;26:747–50.PubMedCrossRefGoogle Scholar
  86. 86.
    Fernandez-Banares F, Hinojosa J, Sanchez-Lombrana JL, Navarro E, Martínez-Salmerón JF, García-Pugés A, et al. Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative colitis. Am J Gastroenterol. 1999;94:427–33.PubMedCrossRefGoogle Scholar
  87. 87.
    Mitsuyama K, Toyonaga A, Sata M. Intestinal microflora as a therapeutic target in inflammatory bowel disease. J Gastroenterol. 2002;37 Suppl 14:73–7.PubMedCrossRefGoogle Scholar
  88. 88.
    Kanauchi O, Mitsuyama K, Homma T, Hibi T, Naganuma M, Homma T, et al. Treatment of ulcerative colitis by feeding with germinated barley foodstuff: first report of a multicenter open control trial. J Gastroenterol. 2002;37:67–72.PubMedCrossRefGoogle Scholar
  89. 89.
    Kanauchi O, Mitsuyama K, Homma T, Takahama K, Fujiyama Y, Andoh A, et al. Treatment of ulcerative colitis patients by long-term administration of germinated barley foodstuff: multicenter open trial. Int J Mol Med. 2003;12:701–4.PubMedGoogle Scholar
  90. 90.
    Lindsay JO, Whelan K, Stagg AJ, Gobin P, Al-Hassi HO, Rayment N, et al. Clinical, microbiological, and immunological effects of fructo-oligosaccharide in patients with Crohn’s disease. Gut. 2006;55:348–55.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Casellas F, Borruel N, Torrejon A, Varela E, Antolin M, Guarner F, et al. Oral oligofructose—enriched inulin supplementation in acute ulcerative colitis is well tolerated and associated with lowered fecal calprotectin. Aliment Pharmacol Ther. 2007;25:1061–7.PubMedCrossRefGoogle Scholar
  92. 92.
    Rath HC, Schultz M, Freitag R, Dieleman LA, Li F, Linde HJ, et al. Different subsets of enteric bacteria induce and perpetuate experimental colitis in rats and mice. Infect Immun. 2001;69:2277–85.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Madsen KL, Doyle JS, Tavernini MM, Jewell LD, Rennie RP, Fedorak RN. Antibiotic therapy attenuates colitis in interleukin 10 gene-deficient mice. Gastroenterology. 2000;118:1094–105.PubMedCrossRefGoogle Scholar
  94. 94.
    Hoentjen F, Harmsen HJ, Braat H, Torrice CD, Mann BA, Sartor RB, et al. Antibiotics with a selective aerobic or anaerobic spectrum have different therapeutic activities in various regions of the colon in interleukin-10 gene deficient mice. Gut. 2003;52:1721–7.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Fiorucci S, Distrutti E, Mencarelli A, Barbanti M, Palazzini E, Morelli A. Inhibition of intestinal bacterial translocation with rifaximin modulates lamina propria monocytic cells reactivity and protects against inflammation in a rodent model of colitis. Digestion. 2002;66:246–56.PubMedCrossRefGoogle Scholar
  96. 96.
    Bamias G, Marini M, Moskaluk CA, Odashima M, Ross WG, Rivera-Nieves J, et al. Down-regulation of intestinal lymphocyte activation and Th1 cytokine production by antibiotic therapy in a murine model of Crohn’s disease. J Immunol. 2002;169:5308–14.PubMedCrossRefGoogle Scholar
  97. 97.
    Yamada T, Deitch E, Specian RD, Perry MA, Sartor RB, Grisham MB. Mechanisms of acute and chronic intestinal inflammation induced by indomethacin. Inflammation. 1993;17:641–62.PubMedCrossRefGoogle Scholar
  98. 98.
    Onderdonk AB, Hermos JA, Dzink JL, Bartlett JG. Protective effect of metronidazole in experimental ulcerative colitis. Gastroenterology. 1978;74:521–6.PubMedGoogle Scholar
  99. 99.
    Videla S, Villaseca J, Guarner F, Salas A, Treserra F, Crespo E, et al. Role of intestinal microflora in chronic inflammation and ulceration of the rat colon. Gut. 1994;35:1090–7.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Dieleman LA, Goerres M, Arends A, Sprengers D, Torrice C, Hoentjen J, et al. Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut. 2003;52:370–6.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Dickinson RJ, O’Connor HJ, Pinder I, Hamilton I, Johnston D, Axon AT. Double-blind controlled trial of oral vancomycin as adjunctive treatment in acute exacerbations of idiopathic colitis. Gut. 1985;26:1380–4.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Chapman RW, Selby WS, Jewell DP. Controlled trial of intravenous metronidazole as adjunct to corticosteroids in severe ulcerative colitis. Gut. 1986;27:1210–2.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Burke DA, Axon ATR, Clayden SA, Dixon MF, Johnston D, Lacey RW. The efficacy of tobramycin in the treatment of ulcerative colitis. Aliment Pharmacol Ther. 1990;4:123–9.PubMedCrossRefGoogle Scholar
  104. 104.
    Mantzaris GJ, Hatzis A, Kontogiannis P, Triadaphyllou G. Intravenous tobramycin and metronidazole as an adjunct to corticosteroids in acute, severe ulcerative colitis. Am J Gastroenterol. 1994;89:43–6.PubMedGoogle Scholar
  105. 105.
    Mantzaris GJ, Archavlis E, Christoforidis P, Kourtessas D, Amberiadis P, Florakis N, et al. A prospective randomized controlled trial of oral ciprofloxacin in acute ulcerative colitis. Am J Gastroenterol. 1997;92:454–6.PubMedGoogle Scholar
  106. 106.
    Mantzaris GJ, Petraki K, Archavlis E, Amberiadis P, Kourtessas D, Christoforidis P, et al. A prospective randomized controlled trial of intravenous ciprofloxacin as an adjunct to corticosteroids in acute, severe ulcerative colitis. Scand J Gastroenterol. 2001;36:971–4.PubMedCrossRefGoogle Scholar
  107. 107.
    Turunen UM, Farkkila MA, Hakala K, Seppala K, Sivonen A, Ogren M, et al. Long-term treatment of ulcerative colitis with ciprofloxacin: a prospective, double-blind, placebo-controlled study. Gastroenterology. 1998;115:1072–8.PubMedCrossRefGoogle Scholar
  108. 108.
    Gionchetti P, Rizzello F, Ferrieri A, Venturi A, Brignola C, Ferretti M, et al. Rifaximin in patients with moderate or severe ulcerative colitis refractory to steroid-treatment: a double-blind, placebo-controlled trial. Dig Dis Sci. 1999;44:1220–1.PubMedCrossRefGoogle Scholar
  109. 109.
    Khan KJ, Ullman TA, Ford AC, Abreu MT, Abadir A, Marshall JK, et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol. 2011;106(4):661–73.PubMedCrossRefGoogle Scholar
  110. 110.
    Blichfeldt P, Blomhoff JP, Myhre E, Gjone E. Metronidazole in Crohn’s disease. A double-blind cross-over clinical trial. Scand J Gastroenterol. 1978;13:123–7.PubMedCrossRefGoogle Scholar
  111. 111.
    Ursing B, Alm T, Barany F, Bergelin I, Ganrot-Norlin K, Hoevels J, et al. A comparative study of metronidazole and sulfasalazine for active Crohn’s disease: the cooperative Crohn’s disease study in Sweden: II. Results. Gastroenterology. 1982;83:550–62.PubMedGoogle Scholar
  112. 112.
    Ambrose NS, Allan RN, Keighley MR, Burdon DW, Youngs D, Lennard-Jones JE. Antibiotic therapy for treatment in relapse of intestinal Crohn’s disease. A prospective randomized study. Dis Colon Rectum. 1985;28:81–5.PubMedCrossRefGoogle Scholar
  113. 113.
    Sutherland LR, Singleton J, Sessions J, Hanauer S, Krawitt E, Rankin G, et al. Double blind, placebo controlled trial of metronidazole in Crohn’s disease. Gut. 1991;32:1071–5.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Prantera C, Zannoni F, Scribano ML, Berto E, Andreoli A, Kohn A, et al. An antibiotic regimen for the treatment of active Crohn’s disease: a randomized controlled clinical trial of metronidazole plus ciprofloxacin. Am J Gastroenterol. 1996;91:328–32.PubMedGoogle Scholar
  115. 115.
    Steinhart AH, Feagan BG, Wong CJ, Vandervoort M, Mikolainins S, Croitoru K, et al. Combined budesonide and antibiotic therapy for active Crohn’s disease: a randomized controlled trial. Gastroenterology. 2002;123:33–40.PubMedCrossRefGoogle Scholar
  116. 116.
    Colombel JF, Lemann M, Cassagnou M, Bouhnik Y, Duclols B, Dupas JL, et al. A controlled trial comparing ciprofloxacin with mesalazine for the treatment of active Crohn’s disease. Am J Gastroenterol. 1999;94:674–8.PubMedCrossRefGoogle Scholar
  117. 117.
    Arnold GL, Beaves MR, Prydun VO, Mook WJ. Preliminary study of ciprofloxacin in active Crohn’s disease. Inflamm Bowel Dis. 2002;8:10–5.PubMedCrossRefGoogle Scholar
  118. 118.
    Shafran I, Dondelinger PJ, Johnson LK, Murdock HR. Efficacy and tolerability of rifaximin, a nonabsorbed, gut-selective, oral antibiotic in the treatment of active Crohn’s disease: results of an open-label study. Am J Gastroenterol. 2003;98:S250.Google Scholar
  119. 119.
    Leiper K, Morris AI, Rhodes JM. Open label trial of oral clarithromycin in active Crohn’s disease. Aliment Pharmacol Ther. 2000;14:801–6.PubMedCrossRefGoogle Scholar
  120. 120.
    Dignass A, Van Assche G, Lindsay JO, Lémann M, Söderholm J, Colombel JF, et al. The second European evidence-based consensus on the diagnosis and management of Crohn’s disease: current management. J Crohns Colitis. 2010;4:28–62.PubMedCrossRefGoogle Scholar
  121. 121.
    Rutgeerts P, Hiele M, Geboes K, Peeters M, Penninckx F, Aerts R, et al. Controlled trial of metronidazole treatment for prevention of Crohn’s recurrence after ileal resection. Gastroenterology. 1995;108:1617–21.PubMedCrossRefGoogle Scholar
  122. 122.
    Rutgeerts P, Van Assche G, D’Haens G, Baert F, Norman M, Aerden I, et al. Ornidazol for prophilaxis of postoperative Crohn’s disease: final results of a double-blind placebo controlled trial. Gastroenterology. 2002;122:A80.Google Scholar
  123. 123.
    Borgaonkar MR, MacIntosh DG, Fardy JM. A meta-analysis of antimycobacterial therapy for Crohn’s disease. Am J Gastroenterol. 2000;95:725–9.PubMedCrossRefGoogle Scholar
  124. 124.
    Schwartz DA, Pemberton JH, Sandborn WJ. Diagnosis and treatment of perianal fistulas in Crohn’s disease. Ann Intern Med. 2001;135:906–18.PubMedCrossRefGoogle Scholar
  125. 125.
    Bernstein LH, Frank MS, Brandt LJ, Boley SJ. Healing of perianal Crohn’s disease with metronidazole. Gastroenterology. 1980;79:357–65.PubMedGoogle Scholar
  126. 126.
    Brandt LJ, Bernstein LH, Boley SJ. Metronidazole therapy for perianal Crohn’s disease: a follow-up study. Gastroenterology. 1982;83:383–7.PubMedGoogle Scholar
  127. 127.
    Solomon MR, McLeod R. Combination ciprofloxacina and metronidazole in severe perianal Crohn’s disease. Can J Gastroenterol. 1993;7:571–3.CrossRefGoogle Scholar
  128. 128.
    Prantera C, Lochs H, Grimaldi M, Danese S, Scribano ML, Gionchetti P, et al. Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn’s disease. Gastroenterology. 2012;142:473–81.PubMedCrossRefGoogle Scholar
  129. 129.
    Sandborn WJ, McLeod R, Jewell DP. Medical therapy for induction and maintenance of remission in pouchitis. A systematic review. Inflamm Bowel Dis. 1999;5:33–9.PubMedCrossRefGoogle Scholar
  130. 130.
    Madden M, McIntyre A, Nicholls RJ. Double- blind cross-over trial of metronidazole versus placebo in chronic unremitting pouchitis. Dig Dis Sci. 1994;39:1193–6.PubMedCrossRefGoogle Scholar
  131. 131.
    Shen B, Achkar JP, Lashner BA, Ormsby AH, Remzi FH, Brzenzinski A, et al. A randomized clinical trial of ciprofloxacin and metronidazole to treat acute pouchitis. Inflamm Bowel Dis. 2001;7:301–5.PubMedCrossRefGoogle Scholar
  132. 132.
    Shen B, Fazio VW, Remzi FH, Bennett AE, Lopez R, Brzezinski A, et al. Combined ciprofloxacin and tinidazole therapy in the treatment of chronic refractory pouchitis. Dis Colon Rectum. 2007;50:498–508.PubMedCrossRefGoogle Scholar
  133. 133.
    Gionchetti P, Rizzello F, Venturi A, Ugolini F, Rossi M, Brigidi P, et al. Antibiotic combination therapy in patients with chronic, treatment-resistant pouchitis. Aliment Pharmacol Ther. 1999;13:713–8.PubMedCrossRefGoogle Scholar
  134. 134.
    Abdelrazeq AS, Kelly SM, Lund JN, Leveson SH. Rifaximin-ciprofloxacin combination therapy is effective in chronic active refractory pouchitis. Colorectal Dis. 2005;7:182–6.PubMedCrossRefGoogle Scholar
  135. 135.
    Mimura T, Rizzello F, Helwig U, Poggioli G, Schreiber S, Talbot IC, et al. Four week open-label trial of metronidazole and ciprofloxacin for the treatment of recurrent or refractory pouchitis. Aliment Pharmacol Ther. 2002;16:909–17.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Paolo Gionchetti
    • 1
    Email author
  • Carlo Calabrese
    • 1
  • Andrea Calafiore
    • 1
  • Fernando Rizzello
    • 1
  1. 1.Department of Medical and Surgical Sciences (DIMEC)University of BolognaBolognaItaly

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