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Clarithromycin Resistance Prevalence and Icea Gene Status in Helicobacter Pylori Clinical Isolates in Turkish Patients with Duodenal Ulcer and Functional Dyspepsia  

Baglan Peren H. (Institute of Hepatology, Ankara University)
Bozdayi Gulendam (Department of Clinical Microbiology, Gazi University)
Ozkan Muhip (Biometry Genetics Department, Agriculture Faculty, Ankara University)
Ahmed Kamruddin (Department of Molecular Biology and Genetics, Bilkent University, Division of Molecular Epidemiology, Nagasaki University School of Medicine)
Bozdayi A. Mithat (Institute of Hepatology, Ankara University, Department of Gastroenterology, School of Medicine, Ankara University)
Ozden Ali (Department of Gastroenterology, School of Medicine, Ankara University)
Publication Information
Journal of Microbiology / v.44, no.4, 2006 , pp. 409-416 More about this Journal
Abstract
Clarithromycin resistance in Helicobacter pylori is a principal cause of failure of eradication therapies, and its prevalence varies geographically. The IceA gene is a virulence factor associated with clinical outcomes. The objective of this study was to determine the current state of clarithromycin resistance prevalence, and to investigate the role of iceA genotypes in 87 Turkish adult patients (65 with functional dyspepsia and 22 with duodenal ulcer). A2143G and A2144G point mutations were tested by PCR-RFLP for clarithromycin resistance. Among the patients in the study, 28 patients were tested by agar dilution as well. Allelic variants of the iceA gene were identified by PCR. A total of 24 (27.6%) strains evidenced one of the mutations, either A2143G or A2144G. IceA1 was found to be positive in 28 of the strains (32.2 %), iceA2 was positive in 12 (13.8 %) and, both iceA1 and iceA2 were positive in 22 (25.3 %) strains. In conclusion, we discovered no relationships between iceA genotypes and functional dyspepsia or duodenal ulcer, nor between clarithromycin resistance and iceA genotypes. clarithromycin resistance appears to be more prevalent in Turkish patients.
Keywords
Helicobacter pylori; clarithromycin resistance; 23S rRNA; iceA;
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1 Bayerdorffer, E., A. Neubauer, B. Rudolph, C. Thiede, N. Lehn, S. Eidt, and M. Stolte. 1995. Regression of primary gastric lymphoma of mucosa-associated lymphoid tissue type after cure of Helicobacter pylori infection. MALT Lymphoma Study Group. Lancet 345, 1591-1594   DOI   ScienceOn
2 Broutet, N., S. Tchamgoue, E. Pereira, H. Lamouliatte, R. Salamon, and F. Megraud. 2003. Risk factors for failure of Helicobacter pylori therapy-results of an individual data analysis of 2751 patients. Aliment. Pharmacol. Ther. 17, 99-109   DOI   ScienceOn
3 Ende, A, L.J. Doorn, S. Rooijakkers, M. Feller, G.N.J. Tytgat, and J. Dankert. 2001. Clarithromycin- susceptible and -resistant Helicobacter pylori isolates with identical randomly amplified polymorphic DNA-PCR genotypes cultured from single gastic biopsy specimens prior to antibiotic therapy. J. Clin. Microbiol. 39, 2648-2651   DOI   ScienceOn
4 Goldman, R.C., D. Zakula, R. Flamm, I. Beyer, and I. Capobianco. 1994. Tight binding of clarithromycin, its 14- (R)-hydroxy metabolite, and erythromycin to Helicobacter pylori ribosomes. Antimicrob. Agents Chemother. 38, 1496- 1500   DOI   ScienceOn
5 Lui, S.Y., K.G. Yeoh, and B. Ho. 2003. Metronidazole-resistant Helicobacter pylori is more prevalent in patients with nonulcer dyspepsia than in peptic ulcer patients in a multiethnic Asian population. J. Clin. Microbiol. 41, 5011- 5014   DOI
6 Megraud, F., C. Camou-Juncas, A. Occhialini, and C. Birac. 1996. Helicobacter pylori resistance levels to clarithromycin remain stable. Gastroenterology 100, A192
7 Megraud, F. 2004. Helicobacter pylori resistance: prevalence importance and advances in testing. Gut 53, 1374-1384   DOI   ScienceOn
8 Palabiyikoglu, M., F. Sahin, A. Ozden, and O. Uzunalimoglu. 1997. Determination of primary resistance in Helicobacter pylori isolates to clarithromycin and amoxycilline by disc diffusion method and the comparison with resistance in recurrent cases. Turk. J. Gastroenterol. 8, 309-312
9 Ribeiro, M.L., L. Vitiello, M.C.B. Miranda, Y.H.B. Benvengo, A.P.O. Godoy, S. Mendonca, and J. Pedrazolli, Jr. 2003. Mutations in the 23S rRNA gene are associated with clarithromycin resistance in Helicobacter pylori isolates in Brazil. Annal. Clinic. Microbiol. Antimicrob. 2, 1-15   DOI
10 Simsek, H., Y.H. Balaban, D.D. Gunes, G. Hascelik, E. Ozarslan, and G. Tatar. 2005. Alarming Clarithromycin Resistance of Helicobacter pylori in Turkish Population Helicobacter 10, 360-361   DOI   ScienceOn
11 Teo, E.K., Fock K.M., T.M. Ng, C.J. Khor, and A.L. Tan. 2000. Metronidazole-resistant Helicobacter pylori in an urban Asian population. J. Gastroenterol. Hepatol. 15, 494-497   DOI   ScienceOn
12 Uemura, N., S. Okamoto, S. Yamamamoto, N. Matsumura, S. Yamaguchi, M. Yamakido, K. Taniyama, N. Sasaki, and R.J. Schlemper. 2001. Helicobacter pylori infection and the development of gastric cancers. N. England. J. Med. 345, 784-789   DOI   ScienceOn
13 Van Doorn, L.J., J. Yvette, Y.J. Debets-Ossenkopp, A. Marais, R. Sana, F. Megraud, J.G. Kusters, and W.G.V. Quint. 1999. Rapid detection, by PCR and Reverse Hybridization of Mutations in the Helicobacter pylori 23S rRNA gene, associated with macrolide resistance. Antimicrob. Agent. Chemother. 43, 1779-1782
14 Van Doorn, L.J., Y. Glupczynski, J.G. Kusters, R. Megraud, P. Midolo, N. Maggi-Soloca, D.M.M. Quiroz, N. Nouhan, E. Stet, and W.G.V. Quint. 2001. Accurate prediction of macrolide resistance in Helicobacter pylori by a PCR line prob assay for detection of mutations in the 23S rRNA Gene: Multicenter validation study. Antimicrob. Agent. Chemother. 45, 1500-1504   DOI   ScienceOn
15 Sipponen, P. 1991. Helicobacter pylori and chronic gastritis: an increased risk of peptic ulcer? Scand. J. Gastroenterol. 26, 6-10
16 NIH. 1994. Consensus Development Panel on Helicobacter pylori in Peptic Ulcer Disease. J. Am. Med. Assn. 272, 65-69   DOI
17 Khan, R., S. Nahar, J. Sultana, M.M. Ahmad, and R. Motiur. 2004. T2182C Mutation in 23S rRNA is associated with clarithromycin resistance in Helicobacter pylori isolates obtained in Bangladesh. Antimicrob. Agents Chemother. 48, 3567-3569   DOI   ScienceOn
18 Taylor, D.E., Z. Ge, D. Purych, T. Lo, and K. Hiratsuka. 1997. 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. 41, 2621-2628
19 Dzierzanowska-Fangrat, K., E. Rozynek, P. Jozwiak, D. Celinska-Cedro, K. Madalinski, and D. Dzierzanowska. 2001. Primary resistance to clarithromycin in clinical strains of Helicobacter pylori isolated from children in Poland. In.t J. Antimicrob. Agents 18, 387-390   DOI   ScienceOn
20 Toracchio, S., G.M. Aceto, R. Mariani-Costantini, P. Battista, and L. Marzio. 2004. Identification of a Novel Mutation Affecting Domain V of the 23S rRNA Gene in Helicobacter pylori. Helicobacter 9, 396-399   DOI   ScienceOn
21 Marshall, B.J. 1994. Helicobacter pylori. Am. J. Gastroenterol. 89, 116-118
22 Perng, C.L., H.J. Lin, W.C. Lo, G.Y. Tseng, I.C. Sun, and Y.H. Ou. 2004. Genotypes of Helicobacter pylori in patients with peptic ulcer bleeding. World J. Gastroenterol. 10, 602-605   DOI
23 Yamaoka, Y., T. Kodama, O. Gutierrez, J.G. Kim, K. Kashima, and D.Y. Graham. 1999. Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J. Clin. Microbiol. 37, 2274-2279
24 Eun, C.S., D.S. Han, J.Y. Park, Y.C. Jeon, J.S. Hahm, K.S. Kim, and J.O. Kang. 2003. Changing pattern of antimicrobial resistance of Helicobacter pylori in Korean patients with peptic ulcer diseases. Gastroenterol. 38, 436-441   DOI
25 Fallone, C.A. 2000. Epidemiology of the antibiotic resistance of Helicobacter pylori in Canada. Can. J. Gastroenterol. 14, 879-882
26 Figueiredo, C., L.J. van Doorn, C. Nogueira, J.M. Soares, C. Pinho, P. Figueira, W.G. Quint, and F. Carneiro. 2001. Helicobacter pylori genotypes are associated with clinical outcome in Portuguese patients and show a high prevalence of infections with multiple strains. Scand. J. Gastroenterol. 36, 128-135   DOI
27 Ashour, A.A., G.B. Collares, E.N. Mendes, V.R. Gusmao, D.M. Queiroz, P.P. Magalhaes, A.S. de Carvalho, C.A. de Oliveira, A.M. Nogueira, G.A. Rocha, and A.M. Rocha. 2001. IceA genotypes of Helicobacter pylori strains isolated from Brazilian children and adults. J. Clin. Microbiol. 39, 1746-1750   DOI   ScienceOn
28 Peek, R.M. Jr, S.A. Thompson, J.P. Donahue, K.T. Tham, J.C. Atherton, M.J. Blaser, and G.G. Miller. 1998. Adherance to gastric epithelial cells induces expression of a Helicobacter pylori gene, iceA, that is associated with clinical outcome. Proc. Assoc. Am. Physicians. 110, 531- 544
29 Van Doorn, L.J., C. Figueiredo, R. Rossau, G. Jannes, M. van Asbroek, J.C. Sousa, F. Carneiro, W.G. Quint. 1998. Typing of Helicobacter pylori vacA gene, and detection of cagA gene by PCR, and reverse hybridization. J. Clin. Microbiol. 36, 1271-1276
30 Kato, M., Y. Yamaoka, J.J. Kim, R. Reddy, M. Asaka, K. Kashima, M.S. Osato, F.A. El-Zaatari, D.Y. Graham, and D.H. Kwon. 2000. Regional differences in metronidazole resistance and increasing clarithromycin resistance among Helicobacter pylori isolates from Japan. Antimicrob. Agents Chemother. 44, 2214-2216   DOI
31 Sevin, E., D. Lamarque, J.C. Delchier, C.J. Soussy, and J. Tankovic. 1998. Co-detection of Helicobacter pylori and of its resistance to clarithromycin by PCR. FEMS Microbiol. Letters 165, 369-372   DOI
32 Wu, C.C., P.Y. Chou, C.T. Hu, Z.C. Liu, C.Y. Lin, Y.H. Tseng, and N.T. Lin. 2005. Clinical Relevance of the vacA, iceA, cagA, and flaA genes of Helicobacter pylori strains isolated in Eastern Taiwan. J. Clin. Microbiol. 43, 2913- 2915   DOI   ScienceOn
33 Ling, T.K.W., W.K. Leung, C.C. Lee, E.K. Ng, M.Y. Yung, M.Y. Chung, S.S. Chung, J.J. Sung, and A.F. Cheng. 2002. The antimicrobial susceptibility of Helicobacter pylori in Hong Kong (1997-2001). Helicobacter 7, 327-329   DOI   ScienceOn
34 Nomura, A., G.N. Stemmarman, and P.H. Chyou. 1994. Helicobacter pylori infection and the risk for duodenal and gastric ulceration. Ann. Intern. Med. 120, 977-981   DOI   ScienceOn
35 Van Doorn, L.J., C. Figueiredo, R. Sanna, A. Plaisier, P. Schneeberger, W. de Boer, and W. Quint. 1998. Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology 115, 58-66   DOI   ScienceOn
36 Han, Y.H, W.Z. Liu, H.Y. Zhu, and S.D. Xiao. 2004. Clinical relevance of iceA and babA2 genotypes of Helicobacter pylori in a Shanghai population. Chin. J. Dig. Dis. 5, 181-185   DOI   ScienceOn
37 National Committee for Laboratory Standards. Performance standards for antimicrobial testing. 1999. VI th International supplement. M100S9. National Committee for Clinical Laboratory Standards, Villanova, PA, USA
38 Osato, M.S., R. Reddy, S.G. Reddy, R.L. Penland, H.M. Malaty, and D.Y. Graham. 2001. Pattern of primary resistance of Helicobacter pylori to metronidazole or clarithromycin in the United States. Arch. Intern. Med. 161, 1217-1220   DOI   ScienceOn
39 Sarma, Z., H. Shmuely, Y. Niv, G. Dinari, D.J. Passaro, A. Geler, E. Gal, M. Fishman, J. Bachor, and J. Yahav. 2002. Resistance of Helicobacter pylori isolated in Israel to metronidazole, clarithromycin, tetracycline, amoxicillin and cefixime. J. Antimicrob. Chemother. 49, 1023-1026   DOI   ScienceOn
40 Fraser, A.G., L. Moore, M. Hackett, and B. Hollis. 1999. Helicobacter pylori treatment and antibiotic susceptibility: results of a five-year audit. Aust. N. Z. J. Med. 29, 512-516   DOI   ScienceOn
41 Dubois, A., D.E. Berg, E.T. Incecik, N. Fiala, A.L. Heman, P.G. Perez, and M.J. Blaser. 1996. Transient and persistent experimental infection of non-human primates with Helicobacter pylori: implications for human disease. Infect. Immun. 64, 2885-2891
42 Hirschl, A.M., M. Richter, A. Makristathis, P.M. Pruckl, B. Willinger, K. Schutze, and M.L. Rotter. 1994. Single and multiple strain colonization in patients with Helicobacter pylori-associated gastritis: Detection by macrorestriction DNA analysis. J. Inf. Dis. 170, 829-33
43 Inan, A., S. Gulsun, H. Guveli, J. Tascioglu, and P. Goktas. 2005. An investigation of Helicobacter pylori using culture, histopathological and serological examination methods and its antimicrobial sensitivities. Saudi. Med. J. 26, 597-600
44 Solerman, A., A. Perren, S. Schmid, F. Eigenmann, R. Guller, K.B. Weher, F. Meier, P. Eichenberger, and P. Komminoth. 2005. Assesment of Helicobacter pylori clarihromycin resistance mutations in archival gastric biopsy samples. Swiss. Med. Wkly. 135, 327-332
45 Kidd, M., R.M. Peek, A.J. Lastovica, D.A. Israel, A.F. Kummer, and J.A. Louw. 2001. Analysis of iceA genotypes in South African Helicobacter pylori strains and relationship to clinically significant disease. Gut 49, 629-635   DOI
46 Loivukene, K., H. Kolk, H.I. Maaroos, P. Kasenomm, M. Ustav, and M. Mikelsaar. 2000. Metronidazole and clarithromycin susceptibility and the subtypes of vacA of Helicobacter pylori isolates in Estonia. Scand. J. Infect. Dis. 32, 59-62   DOI
47 Mohammadi, M., D. Doroud, S. Massarrat, and M.J. Farahvash. 2003. Clarithromycin resistance in Iranian H. pylori strains before introduction of clarithromycin. Helicobacter 8, 79-80
48 Alarcon, T., D. Domingo, and M. Lopez-Brea. 1999. Antibiotic resistance problems with Helicobacter pylori. Inter. J. Antimicro. Agents 1, 19-26
49 Kim, J.J., R. Reddy, M. Lee, J.G. Kim, F.A. El-Zaatari, M.S. Osato, D.Y. Graham, and D.H. Kwon. 2001. Analysis of metronidazole, clarithromycin and tetracycline resistance of Helicobacter pylori isolates from Korea. J. Antimicrob. Chemother. 47, 459-461   DOI   ScienceOn
50 Megraud, F. 2003. Surveillance de la resistance de Helicobacter pylori aux antibiotiques, p. 327-329. In Surveillance nationale des maladies infectieuses, 1998-2000. Institut de Veille Sanitaire, St. Maurice, France
51 Lee, A. and F. Megraud. 1996. Helicobacter pylori: Techniques for clinical diagnosis and basic research, p. 122-123. In J. Hua, C. Birac, and F. Megraud. PCR-based RAPD 'fingerprinting' of clinical isolates of Helicobacter pylori, 2nd ed. Saunders Company Ltd, London, UK
52 Sahin, F., A. Ozden, E. Unver, H. Ozenci, O. Uzunalimoglu, G. Atalay, and O. Koc. 1994. Detecting the resistance by agar dilution method for metronidazole and disc diffusion method for amoxycilline and clarithromycin in Helicobacter pylori isolates. Gastroenterology 5, 203-206
53 Fontana, C., M. Favaro, S. Minelli, A.A. Criscuolo, A. Peitro Yusti, A. Galante, and C. Favalli. 2002. New site of 23S rRNA associated with clarithromycin resistance of Helicobacter pylori clinical isolates. Antimicro. Agents Chemother. 46, 3765-3769   DOI
54 Godoy, A.P.O., M.L. Ribeiro, Y.H.B. Benvengo, L. Vitiello, M.C.B. Miranda, S. Mendonca, and J. Pedrazolli, Jr. 2003. Analysis of antimicrobial susceptibility and virulence factors in Helicobacter pylori clinical isolates. BMC Gastroenter. 3, 20-26   DOI   ScienceOn
55 Perez Aldana, L., M. Kato, S. Nakagawa, M. Kawarasaki, T. Nagasako, T. Mizushima, H. Oda, J. Kodaira, Y. Shimizu, Y. Komatsu, R. Zheng, H. Takeda, T. Sugiyama, and M. Asaka. 2002. The relationship between consumption of antimicrobial agents and the prevalence of primary Helicobacter pylori resistance. Helicobacter 7, 306-309   DOI   ScienceOn
56 Soltesz, V., B. Zeeberg, and T. Wadstrom. 1992. Optimal survival of Helicobacter pylori under various transport conditions. J. Clin. Microbiol. 30, 1453-1456
57 Damaso, D., T. Alarcon, N. Prieto, and M. Lopez-Brea. 1999. Relationship between antimicrobial susceptibility and virulence factors in Helicobacter pylori clinical isolates. Rev. Esp. Quimioter. 12, 340-345
58 Laine, L., M.B. Fennerty, M. Osato, J. Sugg, L. Suchower, P. Probst, and J.G. Levine. 2000. Esomeprazole-based Helicobacter pylori eradication therapy and the effect of antibiotic resistance: results of three US multicentre, double-blind trials. Am. J. Gastroenterol. 95, 3393-3398   DOI
59 Guliter, S., H. Keles, Z.N. Ozkurt, D.U. Cengiz, and E. Kolukisa. 2005. Can lansoprazole, amoxicillin, and clarithromycin combination still be used as a first-line therapy for eradication of Helicobacter pylori? Turk. J. Gastroenterol. 16, 29-33
60 Nishiya, D., T. Shimoyama, S. Fukuda, T. Yoshimura, M. Tanaka, and A. Munakata. 2000. Evaluation of the clinical relevance of the iceA1 gene in patients with Helicobacter pylori infection in Japan. Scand. J. Gastroenterol. 35, 36-39   DOI
61 Pounder, R.E. 1997. New developments in Helicobacter pylori eradication therapy. Scand. J. Gastroenterol. Suppl. 223, 43-45
62 Versalovic, J., D. Shortridge, K. Kibler, M.V. Griffy, J. Beyer, R.K. Flamm, S.K. Tanaka, D.Y. Graham, and M.F. Go. 1996. Mutations in 23S rRNA are associated with clarithromycin resistance in Helicobacter pylori. Antimicrob. Agents. Chemother. 40, 477-480
63 Glupczynski, Y., F. Megraud, M. Lopez-Brea, and L.P. Andersen. 2001. European multicenter survey of in vitro antimicrobial resistance in Helicobacter pylori. Eur. J. Clin. Microbiol. Infect. Dis. 11, 820-823
64 Graham, D.Y., G.M. Lew, P.D. Klein, D.G. Evans, D.J. Evans, Jr., 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   DOI   ScienceOn
65 Jorgensen, M., G. Daskalopoulus, 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   DOI   ScienceOn
66 Laine, L., R. Hunt, H. El-Zimaity, B. Nguyen, M. Osato, and J. Spenard. 2003. Bismuth-based quadruple therapy using a single capsule of bismuth biskalcitrate, metronidazole, and tetracycline given with omeprazole versus omeprazole, amoxicillin, and clarithromycin for eradication of Helicobacter pylori in duodenal ulcer patients: a prospective, randomized, multicentre, North American trial. Am. J. Gastroenterol. 98, 562-567   DOI
67 World Health Organization. 1994. IARC monographs on the evaluation of carcinogenic risks to human, Geneva. World Health Organization 61, 177-240