Rifaximin modulates the colonic microbiota of patients with Crohn's disease: An in vitro approach using a continuous culture colonic model system

Journal of Antimicrobial Chemotherapy

Volumn 65, Issue 12, 2010, Pages 2556-2565

  Maccaferri, Simone ^a   Vitali, Beatrice ^a   Klinder, Annett ^b   Kolida, Sofia ^b   Ndagijimana, Maurice ^a   Laghi, Luca ^a   Calanni, Fiorella ^c   Brigidi, Patrizia ^a   Gibson, Glenn R ^b   Costabile, Adele ^b  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF READING   (United Kingdom)

^c Alfa Wassermann SpA   (Italy)

Author keywords

Human gut model; Inflammatory bowel disease; Inflammatory bowel disorder

Indexed keywords

AROMATIC COMPOUND; DECANOL; HYDROGEN PEROXIDE; PROPANOL; RIFAXIMIN; SHORT CHAIN FATTY ACID;

ARTICLE; BACTERIAL METABOLISM; BACTERIUM CULTURE; BIFIDOBACTERIUM; CELL ASSAY; CHEMOPROPHYLAXIS; COLON FLORA; COMET ASSAY; CONTROLLED STUDY; CROHN DISEASE; DENATURING GRADIENT GEL ELECTROPHORESIS; DISEASE ACTIVITY; DNA DAMAGE; DRUG CYTOTOXICITY; FECES MICROFLORA; FLUORESCENCE IN SITU HYBRIDIZATION; GENOTOXICITY; GROWTH CURVE; HUMAN; HUMAN CELL; IN VITRO STUDY; MASS FRAGMENTOGRAPHY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SOLID PHASE MICROEXTRACTION;

ANTI-INFECTIVE AGENTS; BACTERIOLOGICAL TECHNIQUES; BIFIDOBACTERIUM; COLON; CROHN DISEASE; CULTURE MEDIA; DENATURING GRADIENT GEL ELECTROPHORESIS; ECOSYSTEM; FECES; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; METAGENOME; POLYMERASE CHAIN REACTION; RIFAMYCINS;

EID: 78149477874     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkq345     Document Type: Article

References (58)

1. Packey CD, Sartor RB. Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr Opin Infect Dis 2009; 22: 292-301.
2. Sartor RB, Muehlbauer M. Microbial host interactions in IBD: implications for pathogenesis and therapy. Curr Gastroenterol Rep 2007; 9: 497-507.
3. Manichanh C, Rigottier-Gois L, Bonnaud E et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006; 55: 205-11.
4. Frank DN, St. Amand AL, Feldman RA et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007; 104: 13780-5.
5. Bäckhed F, Ley RE, Sonnenburg JL et al. Host-bacterial mutualism in the human intestine. Science 2005; 307: 1915-20.
6. Swidsinski A, Loenin-Baucke V, Vaneechoutte M et al. Active Crohn's disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora. Inflamm Bowel Dis 2008; 14: 147-61.
7. Ewaschuk J, Tejpar QZ, Soo I et al. The role of antibiotic and probiotic therapies in current and future management of inflammatory bowel disease. Curr Gastroenterol Rep 2006; 8: 486-98.
8. Dejaco C, Harrer M, Waldhoer T et al. Antibiotics and azathioprine for the treatment of perianal fistulas in Crohn's disease. Aliment Pharmacol Ther 2003; 18: 1113-20.
9. Wild GE. The role of antibiotics in the management of Crohn's disease. Inflamm Bowel Dis 2004; 10: 321-3.
10. Prantera C, Lochs H, Campieri M et al. Antibiotic treatment of Crohn's disease: results of a multicentre, double blind, randomized, placebo-controlled trial with rifaximin. Aliment Pharmacol Ther 2006; 23: 1117-25.
11. Gillis J, Brogden RN. Rifaximin. A review of its antibacterial activity, pharmacokinetic properties and therapeutic potential in conditions mediated by gastrointestinal bacteria. Drugs 1995; 49: 467-84.
12. Scarpignato C, Pelosini I. Rifaximin, a poorly absorbed antibiotic: pharmacology and clinical potential. Chemotherapy 2005; 51: 36-66.
13. Robins G, Wellington K. Rifaximin: a review of its use in the management of traveller's diarrhoea. Drugs 2005; 65: 1697-713.
14. Papi C, Koch M, Capurso L. Management of diverticular disease: is there room for rifaximin. Chemotherapy 2005; 51: 110-4.
15. Di Stefano M, Malservisi S, Veneto G et al. Rifaximin versus chlortetracycline in the short-term treatment of small intestinal bacterial overgrowth. Aliment Pharmacol Ther 2000; 14: 551-6.
16. Shafran I, Johnson LK. An open-label evaluation of rifaximin in the treatment of active Crohn's disease. Curr Med Res Opin 2005; 21: 1165-9.
17. Campieri M, Rizzello F, Venturi A et al. Combination of antibiotic and probiotic treatment is efficacious in prophylaxis of post-operative recurrence of Crohn's disease: a randomized controlled study versus mesalazine. Gastroenterology 2000; 118: 713-8.
18. Wilson I, Nicholson JK. The role of gut microbiota in drug response. Curr Pharm Des 2009; 15: 1519-23.
19. Macfarlane G, Macfarlane S, Gibson GR. Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb Ecol 1998; 35: 180-7.
20. Freeman J, O'Neill FJ, Wilcox MH. Effects of cefotaxime and desacetylcefotaxime upon Clostridium difficile proliferation and toxin production in a triple-stage chemostat model of the human gut. J Antimicrob Chemother 2003; 52: 96-102.
21. Martin-Pelaez S, Gibson GR, Martin-Orue SM et al. In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella Typhimurium growth in batch culture systems. FEMS Microbiol Ecol 2008; 66: 608-19.
22. Walter J, Tannock GW, Tilsala-Timisjarvi A et al. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gradient gel electrophoresis and species-specific PCR primers. Appl Environ Microbiol 2000; 66: 297-303.
23. Konstantinov S, Zhu WY, Williams BA et al. Effect of fermentable carbohydrates on piglet faecal bacterial communities as revealed by denaturing gradient gel electrophoresis analysis of 16S ribosomal DNA. FEMS Microbiol Ecol 2003; 43: 225-35.
24. Magurran A. Measuring Biological Diversity. Oxford: Blackwell Publishing; 2004.
25. Kok R, de Waal A, Schut F et al. Specific detection and analysis of a probiotic Bifidobacterium strain in infant feces. Appl Environ Microbiol 1996; 62: 3668-72.
26. Schell M, Karmirantzou M, Snel B et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci USA 2002; 99: 14422-7.
27. Klinder A, Gietl L, Hughes R et al. Gut fermentation products of inulin-derived prebiotics beneficially modulate markers of tumour progression in human colon tumor cells. Int J Canc Prevent 2004; 1: 19-32.
28. Singh NP, McCoy MT, Tice RR et al. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 1988; 175: 184-91.
29. Costabile A, Klinder A, Fava F et al. Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr 2008; 99: 110-20.
30. Di Cagno R, Rizzello CG, Gagliardi F et al. Different fecal microbiota and volatile organic compounds in treated and untreated children with celiac disease. Appl Environ Microbiol 2009; 75: 3963-71.
31. Garner C, Smith S, de Lacy Costello B et al. Volatile organic compounds from feces and their potential for diagnosis of gastrointestinal disease. FASEB J 2007; 21: 1675-88.
32. Ndagijimana M, Laghi L, Vitali B et al. Effect of a synbiotic food consumption on human gut metabolic profiles evaluated by 1H nuclear magnetic resonance spectroscopy. Int J Food Microbiol 2009; 134: 147-53.
33. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007; 448: 427-34.
34. Marchesi J, Holmes E, Khan F et al. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease. J Proteome Res 2007; 6: 546-51.
35. Saxton K, Baines SD, Freeman J et al. Effects of exposure of Clostridium difficile PCR ribotypes 027 and 001 to fluoroquinolones in a human gut model. Antimicrob Agents Chemother 2009; 53: 412-20.
36. Baines SD, O'Connor R, Saxton K et al. Activity of vancomycin against epidemic Clostridium difficile strains in a human gut model. J Antimicrob Chemother 2009; 63: 520-5.
37. Freeman J, Baines SD, Jabes D et al. Comparison of the efficacy of ramoplanin and vancomycin in both in vitro and in vivo models of clindamycin-induced Clostridium difficile infection. J Antimicrob Chemother 2005; 56: 717-25.
38. Baines SD, O'Connor R, Saxton K et al. Comparison of oritavancin versus vancomycin as treatments for clindamycin-induced Clostridium difficile PCR ribotype 027 infection in a human gut model. J Antimicrob Chemother 2008; 62: 1078-85.
39. Baines SD, Freeman J, Wilcox MH. Effects of piperacillin/tazobactam on Clostridium difficile growth and toxin production in a human gut model. J Antimicrob Chemother 2005; 55: 974-82.
40. Fedorak RN. Understanding why probiotic therapies can be effective in treating IBD. J Clin Gastroenterol 2008; 42 Suppl 3 Pt 1: S111-5.
41. Ventura M, O'Flaherty S, Claesson MJ et al. Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 2009; 7: 61-71.
42. Barcenilla A, Pryde SE, Martin JC et al. Phylogenetic relationship of butyrate producing bacteria from the human gut. Appl Environ Microbiol 2000; 66: 1654-61.
43. Sokol H, Pigneur B, Watterlot L et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008; 105: 16731-36.
44. Harmsen HJ, Wildeboer-Veloo AC, Grijpstra J et al. Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol 2000; 66: 4523-7.
45. Jiang Z, Ke S, Palazzini E et al. In vitro activity and fecal concentration of rifaximin after oral administration. Antimicrob Agents Chemother 2000; 44: 2205-6.
46. Finegold SM, Molitoris D, Vaisanen ML. Study of the in vitro activities of rifaximin and comparator agents against 536 anaerobic intestinal bacteria from the perspective of potential utility in pathology involving bowel flora. Antimicrob Agents Chemother 2009; 53: 281-6.
47. Brigidi P, Swennen E, Rizzello F et al. Effects of rifaximin administration on the intestinal microbiota in patients with ulcerative colitis. J Chemother 2002; 14: 290-5.
48. Jiang Z, Ke S, Dupont H. Rifaximin-induced alteration of virulence of diarrhoea-producing Escherichia coli and Shigella sonnei. Int J Antimicrob Agents 2009; 35: 278-81.
49. Brown EL, Xue Q, Jiang Z et al. Pretreatment of epithelial cells with rifaximin alters bacterial attachment and internalization profiles. Antimicrob Agents Chemother 2010; 54: 388-96.
50. Cianci R, Iacopini F, Petruzziello L et al. Involvement of central immunity in uncomplicated diverticular disease. Scand J Gastroenterol 2009; 44: 108-5.
51. Vitali B, Perna F, Lammers K et al. Immunoregolatory activity of rifaximin associated with a resistant mutant of Bifidobacterium infantis. Int J Antimicrob Agents 2009; 33: 387-9.
52. Scheppach W, Weiler F. The butyrate story: old wine in new bottles? Curr Opin Clin Nutr Metab Care 2004; 7: 563-7.
53. Macfarlane S, Macfarlane GT, Cummings JH. Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 2006; 24: 701-14.
54. Jacobs D, Gaudier E, van Duynhoven J et al. Non-digestible food ingredients, colonic microbiota and the impact on gut health and immunity: a role for metabolomics. Curr Drug Metab 2009; 10: 41-54.
55. Blachier F, Mariotti F, Huneau JF et al. Effects of amino acid-derived luminal metabolites on the colonic epithelium and physiopathological consequences. Amino Acids 2007; 33: 547-62.
56. Martin F, Sprenger N, Yap IKS et al. Panorganismal gut microbiota-host metabolic crosstalk. J Proteome Res 2009; 8: 2090-105.
57. Wollowski I, Ji ST, Bakalinsky AT et al. Bacteria used for the production of yogurt inactivate carcinogens and prevent DNA damage in the colon of rats. J Nutr 1999; 129: 77-82.
58. Burns AJ, Rowland IR. Antigenotoxicity of probiotics and prebiotics on faecal water-induced DNA damage in human colon adenocarcinoma cells. Mutat Res 2004; 51: 233-43.