Multidrug resistance is common in Escherichia coli associated with ileal Crohn's disease

Inflammatory Bowel Diseases

Volumn 19, Issue 1, 2013, Pages 141-150

  Dogan, Belgin ^a   Scherl, Ellen ^b   Bosworth, Brian ^b   Yantiss, Rhonda ^b   Altier, Craig ^a   McDonough, Patrick L ^a   Jiang, Zhi Dong ^c   DuPont, Herbert L ^c   Garneau, Philippe ^d   Harel, Josee ^d   Rishniw, Mark ^a   Simpson, Kenneth W ^a  

^a Department of Molecular Biology and Genetics   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

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

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

AIEC; Antimicrobial resistance; Crohn's disease; Escherichia coli; Rifaximin

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; CEFOXITIN; CHLORAMPHENICOL; CIPROFLOXACIN; CLARITHROMYCIN; COTRIMOXAZOLE; GENTAMICIN; KANAMYCIN; NALIDIXIC ACID; RIFAMPICIN; RIFAXIMIN; STREPTOMYCIN; TETRACYCLINE;

ADULT; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ARTICLE; CELL INVASION; CLINICAL ARTICLE; CONTROLLED STUDY; CROHN DISEASE; DISEASE DURATION; DISEASE SEVERITY; ESCHERICHIA COLI; FAMILY HISTORY; FEMALE; HISTOLOGY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; ILEUM; ILEUM MUCOSA; INTESTINE EPITHELIUM CELL; MACROPHAGE; MALE; MULTIDRUG RESISTANCE; NONHUMAN; PATHOTYPE; POLYPECTOMY; PRIORITY JOURNAL;

ADULT; ANTI-BACTERIAL AGENTS; CELLS, CULTURED; CROHN DISEASE; DRUG RESISTANCE, BACTERIAL; DRUG RESISTANCE, MULTIPLE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; FEMALE; FOLLOW-UP STUDIES; HUMANS; ILEUM; MACROPHAGES; MALE; MICROBIAL SENSITIVITY TESTS; MIDDLE AGED; MUTATION; PROGNOSIS; PROSPECTIVE STUDIES; RISK FACTORS;

EID: 84873716806     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.22971     Document Type: Article

References (59)

1. Hanauer SB. Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities. Inflamm Bowel Dis. 2006;12(Suppl 1): S3-S9.
2. Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol. 2006;3:390-407.
3. Rutgeerts P, Goboes K, Peeters M, et al. Effect of faecal stream diversion on recurrence of Crohn's disease in the neoterminal ileum. Lancet. 1991; 338:771-774.
4. Dianda L, Hanby AM, Wright NA, et al. T cell receptor-alpha beta-deficient mice fail to develop colitis in the absence of a microbial environment. Am J Pathol. 1997;150:91-97.
5. Sellon RK, Tonkonogy S, Schultz M, et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun. 1998;66:5224-5231.
6. Pineton de CG, Colombel JF, Poulain D, et al. Pathogenic agents in inflammatory bowel diseases. Curr Opin Gastroenterol. 2008;24:440-447.
7. Prantera C. Mycobacteria and Crohn's disease: the endless story. Dig Liver Dis. 2007;39:452-454.
8. Liu Y, van Kruiningen HJ, West AB, et al. Immunocytochemical evidence of Listeria, Escherichia coli, and Streptococcus antigens in Crohn's disease. Gastroenterology. 1995;108:1396-1404.
9. Arnott ID, Landers CJ, Nimmo EJ, et al. Sero-reactivity to microbial components in Crohn's disease is associated with disease severity and progression, but not NOD2/CARD15 genotype. Am J Gastroenterol. 2004;99:2376-2384.
10. Baumgart M, Dogan B, Rishniw M, et al. 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. 2007;1:403-418.
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: 13780-13785.
12. Willing B, Halfvarson J, Dicksved J, et al. Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal Crohn's disease. Inflamm Bowel Dis. 2009;15:653-660.
13. Darfeuille-Michaud A. Adherent-invasive Escherichia coli: a putative new E. coli pathotype associated with Crohn's disease. Int J Med Microbiol. 2002;292:185-193.
14. Sasaki M, Sitaraman SV, Babbin BA, et al. Invasive Escherichia coli are a feature of Crohn's disease. Lab Invest. 2007;87:1042-1054.
15. Martinez-Medina M, Aldeguer X, Lopez-Siles M, et al. Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn's disease. Inflamm Bowel Dis. 2009;15:872-882.
16. Barnich N, Carvalho FA, Glasser AL, et al. CEACAM6 acts as a receptor for adherent-invasive E. coli, supporting ileal mucosa colonization in Crohn disease.J Clin Invest. 2007;117:1566-1574.
17. Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology. 2004;127:412-421.
18. Rolhion N, Barnich N, Bringer MA, et al. Abnormally expressed ER stress response chaperone Gp96 in CD favours adherent-invasive Escherichia coli invasion. Gut. 2010;59:1355-1362.
19. Lapaquette P, Glasser AL, Huett A, et al. Crohn's disease-associated adherent-invasive E. coli are selectively favoured by impaired autophagy to replicate intracellularly. Cell Microbiol. 2010;12:99-113.
20. Simpson KW, Dogan B, Rishniw M, et al. Adherent and invasive Escherichia coli is associated with granulomatous colitis in Boxer dogs. Infect Immun. 2006;74:4778-4792.
21. Mansfield CS, James FE, Craven M, et al. Remission of histiocytic ul-cerative colitis in Boxer dogs correlates with eradication of invasive intramucosal Escherichia coli. J Vet Intern Med. 2009;23:964-969.
22. Craven M, Dogan B, Schukken A, et al. Antimicrobial resistance impacts clinical outcome of granulomatous colitis in Boxer dogs.J Vet Intern Med. 2010;24:819-824.
23. Mary JY, Modigliani R. Development and validation of an endoscopic index of the severity for Crohn's disease: a prospective multicentre study. Groupe d'Etudes Therapeutiques des Affections Inflammatoires du Tube Digestif (GETAID). Gut. 1989;30:983-989.
24. Daperno M, D'Haens G, Van Assche G, et al. Development and validation of a new, simplified endoscopic activity score for Crohn's disease: the SES-CD. Gastrointest Endosc. 2004;60:505-512.
25. Odze R, Antonioli D, Peppercorn M, et al. Effect of topical 5-ami-nosalicylic acid (5-ASA) therapy on rectal mucosal biopsy morphology in chronic ulcerative colitis. Am J Surg Pathol. 1993;17:869-875.
26. Silverberg MS, Satsangi J, Ahmad T, et al. 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. 2005;19(Suppl A):5-36.
27. Malinen E, Kassinen A, Rinttila T, et al. Comparison of real-time PCR with SYBR Green I or 5'-nuclease assays and dot-blot hybridization with rDNA-targeted oligonucleotide probes in quantification of selected faecal bacteria. Microbiology. 2003; 149:269-277.
28. Wang G, Whittam TS, Berg CM, et al. RAPD (arbitrary primer) PCR is more sensitive than multilocus enzyme electrophoresis for distinguishing related bacterial strains. Nucleic Acids Res. 1993;21:5930-5933.
29. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol. 2000; 66:4555-4558.
30. DebRoy C, Maddox CW. Identification of virulence attributes of gastrointestinal Escherichia coli isolates of veterinary significance. Anim Health Res Rev. 2001;2:129-140.
31. NCCLS. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals, Approved Standard-Second Edition. NCCLS document M31-A 2. NCCLS: Wayne, PA;2002.
32. CDC. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS). 2004 Human Isolates Final Report. Atlanta, GA: U.S. Department of Health and Human Services, CDC; 2007.
33. Adachi JA, Dupont HL. Rifaximin: a novel nonabsorbed rifamycin for gastrointestinal disorders. Clin Infect Dis. 2006;42:541-547.
34. Magiorakos AP, Srinivasan A, Carey RB, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268-281.
35. Bruant G, Maynard C, Bekal S, et al. Development and validation of an oligonucleotide microarray for detection of multiple virulence and antimicrobial resistance genes in Escherichia coli. Appl Environ Microbiol. 2006;72:3780-3784.
36. Subramanian S, Roberts CL, Hart CA, et al. Replication of colonic Crohn's disease mucosal Escherichia coli isolates within macrophages and their susceptibility to antibiotics. Antimicrob Agents Chemother. 2008;52:427-434.
37. Sartor RB. Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology. 2004;126:1620-1633.
38. Guslandi M. Antibiotics for inflammatory bowel disease: do they work? Eur J Gastroenterol Hepatol. 2005;17:145-147.
39. Thukral C, Travassos WJ, Peppercorn MA. The role of antibiotics in inflammatory bowel disease. Curr Treat Options Gastroenterol. 2005;8: 223-228.
40. Khan KJ, Ullman TA, Ford AC, et al. Antibiotic therapy in inflammatory bowel disease: a systematic review and meta-analysis. Am J Gastroenterol. 2011;106:661-673.
41. Feller M, Huwiler K, Schoepfer A, et al. Long-term antibiotic treatment for Crohn's disease: systematic review and meta-analysis of placebo-controlled trials. Clin Infect Dis. 2010;50:473-480.
42. Magro F, Portela F, Lago P, et al. Crohn's disease in a southern European country: Montreal classification and clinical activity. Inflamm Bowel Dis. 2009;15:1343-1350.
43. Freeman HJ. Application of the Montreal classification for Crohn's disease to a single clinician database of 1015 patients. Can J Gastroenterol. 2007;21:363-366.
44. Martin HM, Campbell BJ, Hart CA, et al. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology. 2004;127:80-93.
45. Prescott NJ, Fisher SA, Franke A, et al. A nonsynonymous SNP in ATG16L1 predisposes to ileal Crohn's disease and is independent of CARD15 and IBD5. Gastroenterology. 2007;132:1665-1671.
46. Marquez A, Nunez C, Martinez A, et al. Role of ATG16L1 Thr300Ala polymorphism in inflammatory bowel disease: a study in the Spanish population and a meta-analysis. Inflamm Bowel Dis. 2009;15: 1697-1704.
47. Darfeuille-Michaud A, Neut C, Barnich N, et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology. 1998;115:1405-1413.
48. Glasser AL, Boudeau J, Barnich N, et al. Adherent invasive Escherichia coli strains from patients with Crohn's disease survive and replicate within macrophages without inducing host cell death. Infect Immun. 2001;69: 5529-5537.
49. Arnold GL, Beaves MR, Pryjdun VO, et al. Preliminary study of ciprofloxacin in active Crohn's disease. Inflamm Bowel Dis. 2002;8:10-15.
50. 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: 674-678.
51. Prantera C, Zannoni F, Scribano ML, 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: 328-332.
52. Leiper K, Martin K, Ellis A, et al. Clinical trial: randomized study of clarithromycin versus placebo in active Crohn's disease. Aliment Pharmacol Ther. 2008;27:1233-1239.
53. Shafran I, Burgunder P. Rifaximin for the treatment of newly diagnosed Crohn's disease: a case series. Am J Gastroenterol. 2008; 103: 2158-2160.
54. Shafran I, Johnson LK. An open-label evaluation of rifaximin in the treatment of active Crohn's disease. Curr Med Res Opin. 2005;21:1165-1169.
55. Prantera C, Lochs H, Campieri M, et alAntibiotic treatment of Crohn's disease: results of a multicentre, double blind, randomized, placebo-controlled trial with rifaximin. Aliment Pharmacol Ther. 2006;23:1117-1125.
56. Ruiz J, Mensa L, Pons MJ, et al. Development of Escherichia coli rifaximin-resistant mutants: frequency of selection and stability. J Antimicrob Chemother. 2008;61:1016-1019.
57. Angelberger S, Reinisch W, Dejaco C, et al. NOD2/CARD15 gene variants are linked to failure of antibiotic treatment in perianal fistulating Crohn's disease. Am J Gastroenterol. 2008;103:1197-1202.
58. Landers CJ, Cohavy O, Misra R, et al. Selected loss of tolerance evidenced by Crohn's disease-associated immune responses to auto-and microbial antigens. Gastroenterology. 2002;123:689-699.
59. Mow WS, Landers CJ, Steinhart AH, et al. High-level serum antibodies to bacterial antigens are associated with antibiotic-induced clinical remission in Crohn's disease: a pilot study. Dig Dis Sci. 2004;49: 1280-1286.