Exposure to metronidazole in vivo readily induces resistance in Helicobacter pylori and reduces the efficacy of eradication therapy in mice

Antimicrobial Agents and Chemotherapy

Volumn 43, Issue 4, 1999, Pages 777-781

  Jenks, Peter J ^a   Labigne, Agnes ^a   Ferrero, Richard L ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CLARITHROMYCIN; METRONIDAZOLE; OMEPRAZOLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM CULTURE; BACTERIUM ISOLATION; DRUG EFFICACY; ERADICATION THERAPY; GRAM NEGATIVE INFECTION; HELICOBACTER PYLORI; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 0032891973     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/aac.43.4.777     Document Type: Article

References (48)

1. Adamek, R. J., S. Suerbaum, B. Pfaffenbach, and W. Opferkuch. 1998. Primary and acquired Helicobacter pylori resistance to clarithromycin, metronidazole and amoxycillin - influence on treatment outcome. Am. J. Gastroenterol. 93:385-389.
2. Banatvala, N., G. R. Davies, Y. Abdi, L. Clements, D. S. Rampton, J. M. Hardie, and R. A. Feldman. 1994. High prevalence of Helicobacter pylori metronidazole resistance in migrants to east London: relationship with previous nitroimidazole exposure and gastrointestinal disease. Gut 35:1562-1566.
3. Bazzoli, F., M. Zagari, P. Pozzato, O. Varoli, S. Fossi, L. Ricciardiello, G. Alampi, G. Nicolini, S. Sottili, P. Simoni, A. Roda, and E. Roda. 1998. Evaluation of short-term low-dose triple therapy for the eradication of Helicobacter pylori by factorial design in a randomized, double-blind, controlled study. Aliment. Pharmacol. Ther. 12:439-445.
4. Becx, M. C., A. J. H. M. Janssen, H. A. L. Clasener, and R. W. de Koning. 1990. Metronidazole-resistant Helicobacter pylori. Lancet 335:539-540.
5. Bell, G. D., K. Powell, S. M. Burridge, A. Pallecaros, P. H. Jones, P. W. Gant, G. Harrison, and J. E. Trowell. 1992. Experience with "triple" anti-Helicobacter pylori eradication therapy: side effects and the importance of testing the pre-treatment bacterial isolate for metronidazole resistance. Aliment. Pharmacol. Ther. 6:427-435.
6. Bell, G. D., K. Powell, S. M. Burridge, A. F. Bowden, W. Atoyebi, G. H. Bolton, P. H. Jones, and C. Browns. 1995. Rapid eradication of Helicobacter pylori infection. Aliment. Pharmacol. Ther. 9:41-46.
7. Buckley, M. J. M., H. X. Xia, D. M. Hyde, C. T. Keane, and C. A. O'Morain. 1997. Metronidazole resistance reduces efficacy of triple therapy and leads to secondary clarithromycin resistance. Dig. Dis. Sci. 42:2111-2115.
8. Dore, M. P., M. S. Osato, D. H. Kwon, D. Y. Graham, and F. A. K. El-Zaatari. 1998. Demonstration of unexpected antibiotic resistance of genotypically identical Helicobacter pylori isolates. Clin. Infect. Dis. 27:84-89.
9. Dunn, B. E., H. Cohen, and M. J. Blaser. 1997. Helicobacter pylori. Clin. Microbiol. Rev. 10:720-741.
10. European Helicobacter pylori Study Group. 1997. Current European concepts in the management of Helicobacter pylori infection. The Maastricht Consensus Report. Gut 41:8-13.
11. European Study Group on Antibiotic Susceptibility of Helicobacter pylori. 1942. Results of a multicentre European survey in 1991 of metronidazole resistance in Helicobacter pylori. Eur. J. Clin. Microbiol. Infect. Dis. 11:777-781.
12. Ferrero, R. L., J. M. Thiberge, M. Huerre, and A. Labigne. 1998. Immune responses of specific-pathogen-free mice to chronic Helicobacter pylori (strain SSI) infection. Infect. Immun. 66:1349-1355.
13. Glupczynski, Y., A. Burette, E. De Koster, J. F. Nyst, M. Deltenre, S. Cadranel, L. Bourdeaux, and D. De Vos. 1990. Metronidazole resistance in Helicobacter pylori. Lancet 335:976-977.
14. Goodwin, A., D. Kersulyte, G. Sisson, S. J. O. Veldhuyzen van Zanten, D. E. Berg, and P. S. Hoffman. 1998. Metronidazole resistance in Helicobacter pylori is due to null mutations in a gene (rdxA) that encodes an oxygen-insensitive NADPH nitroreductase. Mol. Microbiol. 28:383-393.
15. Goodwin, C. S., B. J. Marshall, E. D. Blincow, D. H. Wilson, S. Blackbourn, and M. Phillips. 1988. Prevention of nitroimidazole resistance in Campylobacter pylori by coadministration of colloidal bismuth subcitrate: clinical and in vitro studies. J. Clin. Pathol. 41:207-210.
16. Graham, D. Y., G. M. Lew, P. D. Klein, D. G. Evans, D. J. Evans, Z. A. Saeed, and H. M. Malaty. 1992. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer. A randomized, controlled study. Ann. Intern. Med. 116:705-708.
17. Graham, D. Y., W. A. de Boer, and G. N. Tytgat. 1996. Choosing the best anti-Helicobacter pylori therapy: effect of antimicrobial resistance. Am. J. Gastroenterol. 91:1072-1076.
18. Haas, C. E., D. E. Nix, and J. J. Schentag. 1990. In vitro selection of resistant Helicobacter pylori. Antimicrob. Agents Chemother. 34:1637-1641.
19. Harris, A. W., D. I. Pryce, S. M. Gabe, Q. N. Karim, M. M. Walker, H. Langworthy, J. H. Baron, and J. J. Misiewicz. 1996. Lansoprazole, clarithromycin and metronidazole for seven days in Helicobacter pylori infection. Aliment. Pharmacol. Ther. 10:1005-1008.
20. Hirschl, A. M., E. Hentschel, K. Schutze, H. Nemec, R. Potzi, A. Gangl, W. Weiss, M. Pletschette, G. Stanek, and M. L. Rotter. 1988. The efficacy of antimicrobial treatment in Campylobacter pylori-associated gastritis and duodenal ulcer. Scand. J. Gastroenterol. 23(Suppl.):S76-S81.
21. Jorgensen, M., G. Daskalopoulos, V. Warburton, H. M. Mitchell, and S. L. Hazell. 1996. Multiple strain colonization and metronidazole resistance in Helicobacter pylori-infected patients: identification from sequential and multiple biopsy specimens. J. Infect. Dis. 174:631-635.
22. Kist, M., S. Strobel, U. R. Folsch, T. Kirchner, E. G. Hahn, D. H. Kleist, H. U. Klor, and H. G. Dammann. 1997. Prospective assessment of the impact of primary antimicrobial resistances on cure rates of Helicobacter pylori infections, ahstr. 09/328. In Abstracts of the Xth International Workshop on Gastroduodenal Pathology and Helicobacter pylori. Gut 41(Suppl. 1):A90.
23. Krakowka, S., K. A. Eaton, and R. D. Leunk. 1998. Antimicrobial therapies for Helicobacter pylori infection in gnotobiotic piglets. Antimicrob. Agents Chemother. 42:1549-1554.
24. Lee, A., J. O'Rourke, M. Corazon de Ungria, B. Robertson, G. Daskalopoulos, and M. F. Dixon. 1997. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386-1397.
25. Lerang, F., B. Mourn, J. B. Haug, P. Tolas, O. Breder, E. Aubert, O. Hoie, T. Soberg, B. Flaaten, P. Farup, and T. Berge. 1997. Highly effective twice-daily triple therapies for Helicobacter pylori infection and peptic ulcer disease: does in vitro metronidazole resistance have any clinical relevance? Am. J. Gastroenterol. 92:248-253.
26. Leung, V., J. O'Rourke, and A. Lee. 1998. Transmission of Helicobacter pylori between C57/BL6 mice, abstr. 05/146. In Abstracts of the XIth International Workshop on Gastroduodenal Pathology and Helicobacter pylori. Gut 43 (Suppl. 2):A44.
27. Lind, T., F. Mégraud, K. D. Bardhan, E. Bayerdorffer, M. Hellblom, C. O'Morain, R. C. Spiller, P. Unge, S. J. O. Veldhuyzen van Zanten, M. Wrangstadh, L. Zeijlon, and C. Cederberg. 1997. The MACH2 study: antimicrobial resistance in Helicobacter pylori therapy - the impact of omeprazole, abstr. 09/324. In Abstracts of the Xth International Workshop on Gastroduodenal Pathology and Helicobacter pylori. Gut 41(Suppl. 1):A89.
28. Marshall, B. J., C. S. Goodwill, J. R. Warren, R. Murray, E. D. Blincow, S. J. Blackbourn, M. Philips, T. E. Waters, and C. R. Sanderson. 1988. Prospective double-blind trial of duodenal ulcer relapse after eradication of Campylobacter pylori. Lancet ii:1437-1442.
29. Matsumoto, S., Y. Washizuka, Y. Matsumoto, S. Tawara, F. Ikeda, Y. Yokota, and M. Karita. 1997. Appearance of a metronidazole-resistant Helicobacter pylori strain in an infected-ICR-mouse model and difference in eradication of metronidazole-resistant and -sensitive strains. Antimicrob. Agents Chemother. 41:2602-2605.
30. Mégraud, F., and H. P. Doermann. 1998. Clinical relevance of resistant strains of Helicobacter pylori: a review of current data. Gut 43(Suppl. 1):S61-S65.
31. Misiewicz, J. J., A. W. Harris, K. D. Bardhan, S. Levi, C. A. O'Morain, B. T. Cooper, G. D. Kerr, M. F. Dixon, H. Langworthy, D. Piper, and the Lansoprazole Helicobacter Study Group. 1997. One week triple therapy for Helicobacter pylori: a multicentre comparative study. Gut 41:735-739.
32. Moayyedi, P., P. Sahay, D. S. Tompkins, and A. T. Axon. 1995. Efficacy and optimum dose of omeprazole in a new 1-week triple therapy regimen to eradicate Helicobacter pylori. Eur. J. Gastroenterol. Hepatol. 7:835-840.
33. Moayyedi, P., P. L. Ragunathan, N. Mapstone, A. T. Axon, and D. S. Tompkins. 1998. Relevance of antibiotic sensitivities in predicting failure of omeprazole, clarithromycin, and tinidazole to eradicate Helicobacter pylori. J. Gastroenterol. 33:160-163.
34. Noach, L. A., W. L. Langenberg, M. A. Bertola, J. Dankert, and G. N. J. Tytgat. 1994. Impact of metronidazole resistance on the eradication of Helicobacter pylori. Scand. J. Infect. Dis. 26:321-327.
35. Peitz, U., A. Nusch, B. Tillenburg, M. Stolte, G. Borsch, and J. Labenz. 1996. High cure rate of H. pylori (HP) infection by one-week therapy with omeprazole (OME), metronidazole (MET) and clarithromycin (CLA) despite a negative impact by MET resistance, abstr. 1A:03. In Abstracts of the IXth International Workshop on Gastroduodenal Pathology and Helicobacter pylori. Gut 39(Suppl. 2):A5.
36. Peitz, U., M. Menegatti, D. Vaira, and P. Malfertheiner. 1998. The European meeting on Helicobacter pylori: therapeutic news from Lisbon. Gut 43(Suppl. 1):S66-S69.
37. Rautelin, H., K. Seppala, O. V. Renkonen, U. Vainio, and T. U. Kosunen. 1992. Role of metronidazole in therapy of Helicobacter pylori infections. Antimicrob. Agents Chemother. 36:163-166.
38. Rautelin, H., W. Tee, K. Seppala, and T. U. Kosunen. 1994. Ribotyping patterns and emergence of metronidazole resistance in paired clinical samples of Helicobacter pylori. J. Clin. Microbiol. 32:1079-1082.
39. Taylor, N. S., J. G. Fox, N. S. Akopyants, D. E. Berg, N. Thompson, B. Shames, L. Yan, E. Fontham, F. Janney, F. M. Hunter, and P. Correa. 1995. Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J. Clin. Microbiol. 33:918-923.
40. Thijs, J. C., A. A. Van Zwet, W. J. Thijs, E. J. Van der Wouden, and A. Kooy. 1997. One-week triple therapy with omeprazole, amoxycillin and tinidazole for Helicobacter pylori infection: the significance of imidazole resistance. Aliment. Pharmacol. Ther. 11:305-309.
41. van de Hulst, R. W. M., A. van der Ende, A. Homan, P. Roorda, J. Dankert, and G. N. J. Tytgat. 1998. Influence of metronidazole resistance on efficacy of quadruple therapy for Helicobacter pylori eradication. Gut 42:166-169.
42. Vanzanten, S. V., R. H. Hunt, A. Cockeram, G. Schep, U. Malatjalian, J. Sidorov, A. Matisko, and D. Jewell. 1998. Adding once-daily omeprazole 20 mg to metronidazole/amoxicillin treatment for Helicobacter pylori gastritis -a randomized, double-blind trial showing the importance of metronidazole resistance. Am. J. Gastroenterol. 93:5-10.
43. van Zwet, A. A., J. C. Thijs, W. S. Vries, J. Schiphuis, and J. A. M. Snijder. 1994. In vitro studies on stability and development of metronidazole resistance in Helicobacter pylori. Antimicrob. Agents Chemother. 38:360-362.
44. Warren, J. R., and B. Marshall. 1983. Unidentified curved bacilli on gastric epithelium in chronic active gastritis. Lancet i:1273-1275.
45. Weel, J. F. L., R. W. M. van der Hulst, Y. Gerrits, G. N. J. Tytgat, A. van der Ende, and J. Dankert. 1996. Heterogeneity in susceptibility to metronidazole among Helicobacter pylori isolates from patients with gastritis or peptic ulcer disease. J. Clin. Microbiol. 34:2158-2162.
46. Working Party of the European Helicobacter pylori Study Group. 1997. Guidelines for clinical trials in Helicobacter pylori infection. Gut 41(Suppl. 2): S1-S23.
47. Xia, H. X., C. T. Keane, S. Beattie, and C. A. O'Morain. 1994. Standardization of disk diffusion test and its clinical significance for susceptibility testing of metronidazole against Helicobacter pylori. Antimicrob. Agents Chemother. 38:2357-2361.
48. Yousfi, M. M., H. M. el-Zimaity, M. T. al-Assi, R. A. Cole, R. M. Genta, and D. Y. Graham. 1995. Metronidazole, omeprazole and clarithromycin: an effective combination therapy for Helicobacter pylori infection. Aliment. Pharmacol. Ther. 9:209-212.