Rifaximin Resistance in Escherichia coli Associated with Inflammatory Bowel Disease Correlates with Prior Rifaximin Use, Mutations in rpoB, and Activity of Phe-Arg-β-Naphthylamide-Inhibitable Efflux Pumps

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 2, 2013, Pages 811-817

  Kothary, Vishesh ^a   Scherl, Ellen J ^b   Bosworth, Brian ^b   Jiang, Zhi Dong ^b   DuPont, Herbert L ^c   Harel, Josee ^d   Simpson, Kenneth W ^e   Dogan, Belgin ^e  

^a Program on Infrastructure Policy   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 NAPHTHYLAMINE; RIFAXIMIN; RNA POLYMERASE BETA SUBUNIT;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIUM ISOLATE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROHN DISEASE; ENTERITIS; ESCHERICHIA COLI; ILEUM MUCOSA; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; MUTATION; NONHUMAN; PATHOGENESIS; PREVALENCE; PRIORITY JOURNAL; ULCERATIVE COLITIS;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; COLITIS, ULCERATIVE; CROHN DISEASE; DIPEPTIDES; DRUG RESISTANCE, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; ILEUM; INTESTINAL MUCOSA; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MUTATION; RIFAMPIN; RIFAMYCINS;

EID: 84872874230     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02163-12     Document Type: Article

References (45)

1. Dogan B, Scherl E, Bosworth B, Yantiss R, Altier C, McDonough PL, Jiang ZD, Dupont HL, Garneau P, Harel J, Rishniw M, Simpson KW. 16 April 2012. Multidrug resistance is common in Escherichia coli associated with ileal Crohn's disease. Inflamm. Bowel Dis. [Epub ahead of print.] doi:10.1002/ibd.22971.
2. Hanauer SB. 2006. Inflammatory bowel disease: Epidemiology, pathogenesis, and therapeutic opportunities. Inflamm. Bowel Dis. 12(Suppl 1): S3-S9.
3. Sartor RB. 2006. Mechanisms of disease: Pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3:390-407.
4. Guslandi M. 2011. Rifaximin in the treatment of inflammatory bowel disease. World J. Gastroenterol. 17:4643-4646.
5. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H. 2002. Mucosal flora in inflammatory bowel disease. Gastroenterology 122: 44-54.
6. Liu Y, van Kruiningen HJ, West AB, Cartun RW, Cortot A, Colombel JF. 1995. Immunocytochemical evidence of Listeria, Escherichia coli, and Streptococcus antigens in Crohn's disease. Gastroenterology 108:1396-1404.
7. Arnott ID, Landers CJ, Nimmo EJ, Drummond HE, Smith BK, Targan SR, Satsangi J. 2004. Sero-reactivity to microbial components in Crohn's disease is associated with disease severity and progression, but not NOD2/ CARD15 genotype. Am. J. Gastroenterol. 99:2376-2384.
8. Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedmann M, McDonough P, Kim SG, Berg D, Schukken Y, Scherl E, Simpson KW. 2007. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J. 1:403-418.
9. Sasaki M, Klapproth JM. 2012. The role of bacteria in the pathogenesis of ulcerative colitis. J. Signal. Transduct. 2012:704953.
10. Feller M, Huwiler K, Schoepfer A, Shang A, Furrer H, Egger M. 2010. Long-term antibiotic treatment for Crohn's disease: Systematic review and meta-analysis of placebo-controlled trials. Clin. Infect. Dis. 50:473-480.
11. Nikfar S, Mirfazaelian H, Abdollahi M. 2010. Efficacy and tolerability of immunoregulators and antibiotics in fistulizing Crohn's disease: A systematic review and meta-analysis of placebo-controlled trials. Curr. Pharm. Des. 16:3684-3698.
12. Rahimi R, Nikfar S, Rezaie A, Abdollahi M. 2007. A meta-analysis of antibiotic therapy for active ulcerative colitis. Dig. Dis. Sci. 52:2920-2925.
13. Guslandi M. 2005. Antibiotics for inflammatory bowel disease: Do they work? Eur. J. Gastroenterol. Hepatol. 17:145-147.
14. Shafran I, Burgunder P. 2010. Adjunctive antibiotic therapy with rifaximin may help reduce Crohn's disease activity. Dig. Dis. Sci. 55:1079-1084.
15. DuPont HL. 2011. Biologic properties and clinical uses of rifaximin. Expert Opin. Pharmacother. 12:293-302.
16. Pons MJ, Mensa L, Gascon J, Ruiz J. 2012. Fitness and molecular mechanisms of resistance to rifaximin in in vitro selected Escherichia coli mutants. Microb. Drug Resist. 18:376-379.
17. Prantera C, Lochs H, Campieri M, Scribano ML, Sturniolo GC, Castiglione F, Cottone M. 2006. Antibiotic treatment of Crohn's disease: Results of a multicentre, double blind, randomized, placebo-controlled trial with rifaximin. Aliment. Pharmacol. Ther. 23:1117-1125.
18. Prantera C, Lochs H, Grimaldi M, Danese S, Scribano ML, Gionchetti P, and Retic Study Group (Rifaximin-EIR Treatment in Crohn'S Disease). 2012. Rifaximin-extended intestinal release induces remission in patients with moderately active Crohn's disease. Gastroenterology 142:473-481.e4.
19. Gionchetti P, Rizzello F, Ferrieri A, Venturi A, Brignola C, Ferretti M, Peruzzo S, Miglioli M, Campieri M. 1999. Rifaximin in patients with moderate or severe ulcerative colitis refractory to steroid-treatment: A double-blind, placebo-controlled trial. Dig. Dis. Sci. 44:1220-1221.
20. Guslandi M, Petrone MC, Testoni PA. 2006. Rifaximin for active ulcerative colitis. Inflamm. Bowel Dis. 12:335.
21. Shen B, Remzi FH, Lopez AR, Queener E. 2008. Rifaximin for maintenance therapy in antibiotic-dependent pouchitis. BMC Gastroenterol. 8:26. doi:10.1186/1471-230X-8-26.
22. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A, Darst SA. 2001. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104:901-912.
23. Ruiz J, Mensa L, Pons MJ, Vila J, Gascon J. 2008. Development of Escherichia coli rifaximin-resistant mutants: Frequency of selection and stability. J. Antimicrob. Chemother. 61:1016-1019.
24. Tupin A, Gualtieri M, Roquet-Baneres F, Morichaud Z, Brodolin K, Leonetti JP. 2010. Resistance to rifampicin: At the crossroads between ecological, genomic and medical concerns. Int. J. Antimicrob. Agents 35: 519-523.
25. Vitali B, Turroni S, Dal Piaz F, Candela M, Wasinger V, Brigidi P. 2007. Genetic and proteomic characterization of rifaximin resistance in Bifidobacterium infantis BI07. Res. Microbiol. 158:355-362.
26. Sulavik MC, Houseweart C, Cramer C, Jiwani N, Murgolo N, Greene J, DiDomenico B, Shaw KJ, Miller GH, Hare R, Shimer G. 2001. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob. Agents Chemother. 45:1126-1136.
27. Kern WV, Steinke P, Schumacher A, Schuster S, von Baum H, Bohnert JA. 2006. Effect of 1-(1-naphthylmethyl)-piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Escherichia coli. J. Antimicrob. Chemother. 57:339-343.
28. Saenz Y, Ruiz J, Zarazaga M, Teixido M, Torres C, Vila J. 2004. Effect of the efflux pump inhibitor Phe-Arg-beta-naphthylamide on the MIC values of the quinolones, tetracycline and chloramphenicol, in Escherichia coli isolates of different origin. J. Antimicrob. Chemother. 53:544-545.
29. Silverberg MS, Satsangi J, Ahmad T, Arnott ID, Bernstein CN, Brant SR, Caprilli R, Colombel JF, Gasche C, Geboes K, Jewell DP, Karban A, Loftus EV, Jr, Pena AS, Riddell RH, Sachar DB, Schreiber S, Steinhart AH, Targan SR, Vermeire S, Warren BF. 2005. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: Report of a Working Party of the 2005 Montreal World Congress of Gastroenterology Can. J. Gastroenterol. 19(Suppl A):5-36.
30. Wang G, Whittam TS, Berg CM, Berg DE. 1993. RAPD (arbitrary primer) PCR is more sensitive than multilocus enzyme electrophoresis for distinguishing related bacterial strains. Nucleic Acids Res. 21: 5930-5933.
31. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:4555-4558.
32. Clinical and Laboratory Standards Institute. 2007. Methods for antimicrobial susceptibility testing of anaerobic bacteria. Approved standard M11-A7, 7th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
33. Villain-Guillot P, Bastide L, Gualtieri M, Leonetti JP. 2007. Progress in targeting bacterial transcription. Drug Discov. Today. 12:200-208.
34. Reynolds MG. 2000. Compensatory evolution in rifampin-resistant Escherichia coli. Genetics 156:1471-1481.
35. Bohnert JA, Kern WV. 2005. Selected arylpiperazines are capable of reversing multidrug resistance in Escherichia coli overexpressing RND efflux pumps. Antimicrob. Agents Chemother. 49:849-852.
36. Pages JM, Masi M, Barbe J. 2005. Inhibitors of efflux pumps in Gramnegative bacteria. Trends Mol. Med. 11:382-389.
37. De Leo C, Eftimiadi C, Schito GC. 1986. Rapid disappearance from the intestinal tract of bacteria resistant to rifaximin. Drugs Exp. Clin. Res. 12:979-981.
38. Vitali B, Turroni S, Serina S, Sosio M, Vannini L, Candela M, Guerzoni ME, Brigidi P. 2008. Molecular and phenotypic traits of in-vitro-selected mutants of Bifidobacterium resistant to rifaximin. Int. J. Antimicrob. Agents. 31:555-560.
39. Liao CH, Ko WC, Lu JJ, Hsueh PR. 2012. Characterizations of clinical isolates of Clostridium difficile by toxin genotypes and by susceptibility to 12 antimicrobial agents, including fidaxomicin (OPT-80) and rifaximin: A multicenter study in Taiwan. Antimicrob. Agents Chemother. 56:3943-3949.
40. DuPont HL, Jiang ZD, Ericsson CD, Adachi JA, Mathewson JJ, DuPont MW, Palazzini E, Riopel LM, Ashley D, Martinez-Sandoval F. 2001. Rifaximin versus ciprofloxacin for the treatment of traveler's diarrhea: A randomized, double-blind clinical trial. Clin. Infect. Dis. 33:1807-1815.
41. DuPont HL, Ericsson CD, Mathewson JJ, Palazzini E, DuPont MW, Jiang ZD, Mosavi A, de la Cabada FJ. 1998. Rifaximin: A nonabsorbed antimicrobial in the therapy of travelers' diarrhea. Digestion 59:708-714.
42. DuPont HL, Jiang ZD. 2004. Influence of rifaximin treatment on the susceptibility of intestinal Gram-negative flora and enterococci. Clin. Microbiol. Infect. 10:1009-1011.
43. Jiang ZD, Ke S, Palazzini E, Riopel L, Dupont H. 2000. In vitro activity and fecal concentration of rifaximin after oral administration. Antimicrob. Agents Chemother. 44:2205-2206.
44. Darkoh C, Lichtenberger LM, Ajami N, Dial EJ, Jiang ZD, DuPont HL. 2010. Bile acids improve the antimicrobial effect of rifaximin. Antimicrob. Agents Chemother. 54:3618-3624.
45. Maccaferri S, Vitali B, Klinder A, Kolida S, Ndagijimana M, Laghi L, Calanni F, Brigidi P, Gibson GR, Costabile A. 2010. 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. 65:2556-2565.