Heteroresistance of Helicobacter pylori from the same patient prior to antibiotic treatment

Infection, Genetics and Evolution

Volumn 23, Issue , 2014, Pages 196-202

  Kao, Cheng Yen ^a   Lee, Ai Yun ^a   Huang, Ay Huey ^a   Song, Pin Yi ^a   Yang, Yao Jong ^b   Sheu, Shew Meei ^a   Chang, Wei Lun ^a   Sheu, Bor Shyang ^a   Wu, Jiunn Jong ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Antibiotic; Helicobacter pylori; Heteroresistance; Treatment failure

Indexed keywords

AMOXICILLIN; CLARITHROMYCIN; DNA TOPOISOMERASE (ATP HYDROLYSING) A; DNA TOPOISOMERASE (ATP HYDROLYSING) B; LEVOFLOXACIN; METRONIDAZOLE; RNA 23S; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; NITROREDUCTASE; RDXA PROTEIN, HELICOBACTER PYLORI;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; EPSILOMETER TEST; FRXA GENE; GENE MUTATION; GYRA GENE; GYRB GENE; HELICOBACTER PYLORI; MINIMUM INHIBITORY CONCENTRATION; MISSENSE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RANDOM AMPLIFIED POLYMORPHIC DNA; RDXA GENE; CLASSIFICATION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; HELICOBACTER INFECTIONS; HUMAN; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MUTATION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENETIC VARIATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MICROBIAL SENSITIVITY TESTS; MUTATION; NITROREDUCTASES; SEQUENCE ANALYSIS, DNA;

EID: 84897885108     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.02.009     Document Type: Article

References (42)

1. Ahmad A., Govil Y., Frank B.B. Gastric mucosa-associated lymphoid tissue lymphoma. Am. J. Gastroenterol. 2003, 98:975-986.
2. Akopyanz N., Bukanov N.O., Westblom T.U., Kresovich S., Berg D.E. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res. 1992, 20:5137-5142.
3. Aldana L.P., Kato M., Kondo T., Nakagawa S., Zheng R., Sugiyama T., Asaka M., Kwon D.H. In vitro induction of resistance to metronidazole, and analysis of mutations in rdxA and frxA genes from Helicobacter pylori isolates. J. Infect. Chemother. 2005, 11:59-63.
4. Arents N.L., Smeets L.C., van Zwet A.A., Thijs J.C., van der Wouden E.J., de Jong A., Degener J.E., Kusters J.G. Implications of the simultaneous presence of metronidazole-susceptible and -resistant Helicobacter pylori colonies within a single biopsy specimen. Eur. J. Clin. Microbiol. Infect. Dis. 2001, 20:418-420.
5. Chang W.L., Sheu B.S., Cheng H.C., Yang Y.J., Yang H.B., Wu J.J. Resistance to metronidazole, clarithromycin and levofloxacin of Helicobacter pylori before and after clarithromycin-based therapy in Taiwan. J. Gastroenterol. Hepatol. 2009, 24:1230-1235.
6. Chang W.L., Kao C.Y., Wu C.T., Huang A.H., Wu J.J., Yang H.B., Cheng H.C., Sheu B.S. Gemifloxacin can partially overcome quinolone resistance of H. pylori with gyrA mutation in Taiwan. Helicobacter 2012, 17:210-215.
7. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing, 20th Informational Supplement, M100-S20 2010, Clinical and Laboratory Standards Institute, Wayne, PA.
8. Gatta L., Vakil N., Leandro G., Di Mario F., Vaira D. Sequential therapy or triple therapy for Helicobacter pylori infection: systematic review and meta-analysis of randomized controlled trials in adults and children. Am. J. Gastroenterol. 2009, 104:3069-3079.
9. Gerrits M.M., van Vliet A.H., Kuipers E.J., Kusters J.G. Helicobacter pylori and antimicrobial resistance: molecular mechanisms and clinical implications. Lancet Infect. Dis. 2006, 6:699-709.
10. Giorgio F., Principi M., Francesco V.De, Zullo A., Losurdo G., Leo A.Di, Ierardi E. Primary clarithromycin resistance to Helicobacter pylori: is this the main reason for triple therapy failure?. World J. Gastrointest. Pathophysiol. 2013, 4:43-46.
11. Graham D.Y. Therapy of Helicobacter pylori: current status and issues. Gastroenterology 2000, 118(2 Suppl 1):S2-S8.
12. Graham D.Y., Fischbach L. Helicobacter pylori treatment in the era of increasing antibiotic resistance. Gut 2010, 59:1143-1153.
13. Graham D.Y., Hepps K.S., Ramirez F.C., Lew G.M., Saeed Z.A. Treatment of Helicobacter pylori reduces the rate of rebleeding in peptic ulcer disease. Scand. J. Gastroenterol. 1993, 28:939-942.
14. Hung K.H., Sheu B.S., Chang W.L., Wu H.M., Liu C.C., Wu J.J. Prevalence of primary fluoroquinolone resistance among clinical isolates of Helicobacter pylori at a university hospital in southern Taiwan. Helicobacter 2009, 14:61-65.
15. Israel D.A., Salama N., Krishna U., Rieger U.M., Atherton J.C., Falkow S., Peek R.M. Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc. Natl. Acad. Sci. USA 2001, 98:14625-14630.
16. Jenks P.J., Ferrero R.L., Labigne A. The role of the rdxA gene in the evolution of metronidazole resistance in Helicobacter pylori. J. Antimicrob. Chemother. 1999, 43:753-758.
17. Jeong J.Y., Berg D.E. Mouse-colonizing Helicobacter pylori SS1 is unusually susceptible to metronidazole due to two complementary reductase activities. Antimicrob. Agents Chemother. 2000, 44:3127-3132.
18. Jeong J.Y., Mukhopadhyay A.K., Dailidiene D., Wang Y., Velapatino B., Gilman R.H., Parkinson A.J., Nair G.B., Wong B.C., Lam S.K., Mistry R., Segal I., Yuan Y., Gao H., Alarcon T., Brea M.L., Ito Y., Kersulyte D., Lee H.K., Gong Y., Goodwin A., Hoffman P.S., Berg D.E. Sequential inactivation of rdxA (HP0954) and frxA (HP0642) nitroreductase genes causes moderate and high-level metronidazole resistance in Helicobacter pylori. J. Bacteriol. 2000, 182:5082-5090.
19. Kennemann L., Didelot X., Aebischer T., Kuhn S., Drescher B., Droege M., Reinhardt R., Correa P., Meyer T.F., Josenhans C., Falush D., Suerbaum S. Helicobacter pylori genome evolution during human infection. Proc. Natl. Acad. Sci. USA 2011, 108:5033-5038.
20. Kwon D.H., Hulten K., Kato M., Kim J.J., Lee M., El-Zaatari F.A., Osato M.S., Graham D.Y. DNA sequence analysis of rdxA and frxA from 12 pairs of metronidazole-sensitive and -resistant clinical Helicobacter pylori isolates. Antimicrob. Agents Chemother. 2001, 45:2609-2615.
21. Lee Y.C., Lee S.Y., Pyo J.H., Kwon D.H., Rhee J.C., Kim J.J. Isogenic variation of Helicobacter pylori strain resulting in heteroresistant antibacterial phenotypes in a single host in vivo. Helicobacter 2005, 10:240-248.
22. Lin C.K., Hsu P.I., Lai K.H., Lo G.H., Tseng H.H., Lo C.C., Peng N.J., Chen H.C., Jou H.S., Huang W.K., Chen J.L., Hsu P.N. One-week quadruple therapy is an effective salvage regimen for Helicobacter pylori infection in patients after failure of standard triple therapy. J. Clin. Gastroenterol. 2002, 34:547-551.
23. Lundin A., Bjorkholm B., Kupershmidt I., Unemo M., Nilsson P., Andersson D.I., Engstrand L. Slow genetic divergence of Helicobacter pylori strains during long-term colonization. Infect. Immunol. 2005, 73:4818-4822.
24. Malfertheiner P., Megraud F., O'Morain C., Bazzoli F., El-Omar E., Graham D., Hunt R., Rokkas T., Vakil N., Kuipers E.J. Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut 2007, 56:772-781.
25. Marais A., Bilardi C., Cantet F., Mendz G.L., Megraud F. Characterization of the genes rdxA and frxA involved in metronidazole resistance in Helicobacter pylori. Res. Microbiol. 2003, 154:137-144.
26. Marshall B.J., Warren J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984, 1:1311-1315.
27. Matteo M.J., Perez C.V., Domingo M.R., Olmos M., Sanchez C., Catalano M. DNA sequence analysis of rdxA and frxA from paired metronidazole-sensitive and -resistant Helicobacter pylori isolates obtained from patients with heteroresistance. Int. J. Antimicrob. Agents 2006, 27:152-158.
28. Megraud F. H pylori antibiotic resistance: prevalence, importance, and advances in testing. Gut 2004, 53:1374-1384.
29. Megraud F. Helicobacter pylori and antibiotic resistance. Gut 2007, 56:1502.
30. Miyachi H., Miki I., Aoyama N., Shirasaka D., Matsumoto Y., Toyoda M., Mitani T., Morita Y., Tamura T., Kinoshita S., Okano Y., Kumagai S., Kasuga M. Primary levofloxacin resistance and gyrA/B mutations among Helicobacter pylori in Japan. Helicobacter 2006, 11:243-249.
31. Okada M., Nishimura H., Kawashima K., Okabe N., Maeda K., Seo M., Ohkuma K., Takata T. A new quadruple therapy for Helicobacter pylori: influence of resistant strains on treatment outcome. Aliment. Pharmacol. Ther. 1999, 13:769-774.
32. Park H.G., Jung M.K., Jung J.T., Kwon J.G., Kim E.Y., Seo H.E., Lee J.H., Yang C.H., Kim E.S., Cho K.B., Park K.S., Lee S.H., Kim K.O., Jeon S.W. Randomised clinical trial: a comparative study of 10-day sequential therapy with 7-day standard triple therapy for Helicobacter pylori infection in naive patients. Aliment. Pharmacol. Ther. 2012, 35:56-65.
33. Parsonnet J., Friedman G.D., Vandersteen D.P., Chang Y., Vogelman J.H., Orentreich N., Sibley R.K. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl. J. Med. 1991, 325:1127-1131.
34. Pounder R.E., Ng D. The prevalence of Helicobacter pylori infection in different countries. Aliment. Pharmacol. Ther. 1995, 9(Suppl):33-39.
35. Rauws E.A., Tytgat G.N. Cure of duodenal ulcer associated with eradication of Helicobacter pylori. Lancet 1990, 335:1233-1235.
36. Sheu S.M., Sheu B.S., Lu C.C., Yang H.B., Wu J.J. Mixed infections of Helicobacter pylori: tissue tropism and histological significance. Clin. Microbiol. Infect. 2009, 15:253-259.
37. Tankovic J., Lascols C., Sculo Q., Petit J.C., Soussy C.J. Single and double mutations in gyrA but not in gyrB are associated with low- and high-level fluoroquinolone resistance in Helicobacter pylori. Antimicrob. Agents Chemother. 2003, 47:3942-3944.
38. Taylor D.E., Ge Z., Purych D., Lo T., Hiratsuka K. Cloning and sequence analysis of two copies of a 23S rRNA gene from Helicobacter pylori and association of clarithromycin resistance with 23S rRNA mutations. Antimicrob. Agents Chemother. 1997, 41:2621-2628.
39. Tomb J.F., White O., Kerlavage A.R., Clayton R.A., Sutton G.G., Fleischmann R.D., Ketchum K.A., Klenk H.P., Gill S., Dougherty B.A., Nelson K., Quackenbush J., Zhou L., Kirkness E.F., Peterson S., Loftus B., Richardson D., Dodson R., Khalak H.G., Glodek A., McKenney K., Fitzegerald L.M., Lee N., Adams M.D., Hickey E.K., Berg D.E., Gocayne L.D., Utterback T.R., Peterson J.D., Kelley J.M., Cotton M.D., Weidman J.M., Fujii C., Bowman C., Watthey L., Wallin E., Hayes W.S., Borodovsky M., Karp P.D., Smith H.O., Fraser C.M., Venter J.C. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388:539-547.
40. Vaira D., Zullo A., Vakil N., Gatta L., Ricci C., Perna F., Hassan C., Bernabucci V., Tampieri A., Morini S. Sequential therapy versus standard triple-drug therapy for Helicobacter pylori eradication: a randomized trial. Ann. Int. Med. 2007, 146:556-563.
41. van der Ende A., van Doorn L.J., Rooijakkers S., Feller M., Tytgat G.N., Dankert J. Clarithromycin-susceptible and -resistant Helicobacter pylori isolates with identical randomly amplified polymorphic DNA-PCR genotypes cultured from single gastric biopsy specimens prior to antibiotic therapy. J. Clin. Microbiol. 2001, 39:2648-2651.
42. Yang Y.J., Wu J.J., Sheu B.S., Kao A.W., Huang A.H. The rdxA gene plays a more major role than frxA gene mutation in high-level metronidazole resistance of Helicobacter pylori in Taiwan. Helicobacter 2004, 9:400-407.