The Korean Journal of Gastroenterology (대한소화기학회지)

The Korean Society of Gastroenterology (대한소화기학회)
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Future Trends of Helicobacter pylori Eradication Therapy in Korea

헬리코박터 제균 치료의 미래

  • Lee, Ju Yup (Department of Internal Medicine, Seoul National University Bundang Hospital) ;
  • Kim, Nayoung (Department of Internal Medicine, Seoul National University Bundang Hospital)
  • 이주엽 (분당서울대학교병원 내과) ;
  • 김나영 (분당서울대학교병원 내과)
  • Published : 2014.03.25
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Abstract

The prevalence of Helicobacter pylori infection in Korea shows a decreasing trend and has changed to that of developed country, especially for those below 30 years old. However, the primary antibiotic resistance rates are higher than those of developed countries. The reason for the decrease in the efficacy of standard triple therapy is mainly due to the increase in the resistance against clarithromycin. Sequential therapy seems to be more effective than the standard triple therapy, but the intention-to-treat eradication rate of sequential therapy in Korea, which is mostly under 80.0%, is still not satisfactory. Therefore, a promising regimen is needed. Recently, the Japanese health insurance system admitted 'H. pylori-infected gastritis' as an indication of eradication. Furthermore, the Kyoto Consensus Meeting on H. pylori Gastritis held from January 30th to February 1st, 2014, proposed that 'all H. pylori positive patients should be offered to receive H. pylori eradication'. This suggests that the concept of eradication has been changed from 'treatment' to 'prevention'. Various individualized tailored therapy based on the polymorphism, age and other demographic factors and antibiotic resistance has been attempted to maximize H. pylori eradication therapy. The aim of this article is to review the current epidemiology, H. pylori resistance state, treatment guideline, and to assess the possible future strategy and treatment for H. pylori infection in Korea.

Keywords

References

  1. McColl KE. Clinical practice. Helicobacter pylori infection. N Engl J Med 2010;362:1597-1604. https://doi.org/10.1056/NEJMcp1001110
  2. NIH Consensus Conference. H. pylori in peptic ulcer disease. NIH Consensus development panel on Helicobacter pylori in peptic ulcer disease. JAMA 1994;272:65-69. https://doi.org/10.1001/jama.1994.03520010077036
  3. Graham DY, Lew GM, Klein PD, et al. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer. A randomized, controlled study. Ann Intern Med 1992;116:705-708. https://doi.org/10.7326/0003-4819-116-9-705
  4. Bayerdorffer E, Neubauer A, Rudolph B, et al. Regression of primary gastric lymphoma of mucosa-associated lymphoid tissue type after cure of Helicobacter pylori infection. MALT Lymphoma Study Group. Lancet 1995;345:1591-1594. https://doi.org/10.1016/S0140-6736(95)90113-2
  5. Kim N, Kim JJ, Choe YH, Kim HS, Kim JI, Chung IS; Korean College of Helicobacter and Upper Gastrointestinal Research; Korean Association of Gastroenterology. Diagnosis and treatment guidelines for Helicobacter pylori infection in Korea. Korean J Gastroenterol 2009;54:269-278. https://doi.org/10.4166/kjg.2009.54.5.269
  6. Lee JY, Kim N, Kim MS, et al. Factors affecting first-line triple therapy of Helicobacter pylori including CYP2C19 genotype and antibiotic resistance. Dig Dis Sci 2014. doi: 10.1007/ s10620-014-3093-7. 1-9.
  7. World Gastroenterology Organisation global guideline: Helicobacter pylori in developing countries. J Dig Dis 2011;12:319-326. https://doi.org/10.1111/j.1751-2980.2011.00529.x
  8. Klein PD, Graham DY, Gaillour A, Opekun AR, Smith EO. Water source as risk factor for Helicobacter pylori infection in Peruvian children. Gastrointestinal Physiology Working Group. Lancet 1991;337:1503-1506. https://doi.org/10.1016/0140-6736(91)93196-G
  9. al-Moagel MA, Evans DG, Abdulghani ME, et al. Prevalence of Helicobacter (formerly Campylobacter) pylori infection in Saudia Arabia, and comparison of those with and without upper gastrointestinal symptoms. Am J Gastroenterol 1990;85: 944-948.
  10. Malaty HM, Evans DG, Evans DJ Jr, Graham DY. Helicobacter pylori in Hispanics: comparison with blacks and whites of similar age and socioeconomic class. Gastroenterology 1992;103: 813-816. https://doi.org/10.1016/0016-5085(92)90011-M
  11. Graham DY, Malaty HM, Evans DG, Evans DJ Jr, Klein PD, Adam E. Epidemiology of Helicobacter pylori in an asymptomatic population in the United States. Effect of age, race, and socioeconomic status. Gastroenterology 1991;100:1495-1501. https://doi.org/10.1016/0016-5085(91)90644-Z
  12. Malaty HM, Graham DY. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut 1994;35:742-745. https://doi.org/10.1136/gut.35.6.742
  13. Bures J, Kopacova M, Koupil I, et al; European Society for Primary Care Gastroenterology. Epidemiology of Helicobacter pylori infection in the Czech Republic. Helicobacter 2006;11: 56-65. https://doi.org/10.1111/j.0083-8703.2006.00369.x
  14. Shi R, Xu S, Zhang H, et al. Prevalence and risk factors for Helicobacter pylori infection in Chinese populations. Helicobacter 2008;13:157-165. https://doi.org/10.1111/j.1523-5378.2008.00586.x
  15. Cheng H, Hu F, Zhang L, et al. Prevalence of Helicobacter pylori infection and identification of risk factors in rural and urban Beijing, China. Helicobacter 2009;14:128-133. https://doi.org/10.1111/j.1523-5378.2009.00668.x
  16. Kim JH, Kim HY, Kim NY, et al; Korea H. pylori Study Group, South Korea. Seroepidemiological study of Helicobacter pylori infection in asymptomatic people in South Korea. J Gastroenterol Hepatol 2001;16:969-975. https://doi.org/10.1046/j.1440-1746.2001.02568.x
  17. Yim JY, Kim N, Choi SH, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter 2007;12:333-340. https://doi.org/10.1111/j.1523-5378.2007.00504.x
  18. Lim SH, Kwon JW, Kim N, et al. Prevalence and risk factors of Helicobacter pylori infection in Korea: nationwide multicenter study over 13 years. BMC Gastroenterol 2013;13:104. https://doi.org/10.1186/1471-230X-13-104
  19. Asaka M, Kimura T, Kudo M, et al. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology 1992;102:760-766. https://doi.org/10.1016/0016-5085(92)90156-S
  20. Shiota S, Murakami K, Fujioka T, Yamaoka Y. Population-based strategies for Helicobacter pylori-associated disease management: a Japanese perspective. Expert Rev Gastroenterol Hepatol 2010;4:149-156. https://doi.org/10.1586/egh.10.7
  21. Shiota S, Murakawi K, Suzuki R, Fujioka T, Yamaoka Y. Helicobacter pylori infection in Japan. Expert Rev Gastroenterol Hepatol 2013;7:35-40. https://doi.org/10.1586/egh.12.67
  22. Nishizawa T, Suzuki H, Suzuki M, Takahashi M, Hibi T. Proton pump inhibitor-amoxicillin-clarithromycin versus proton pump inhibitor-amoxicillin-metronidazole as first-line Helicobacter pylori eradication therapy. J Clin Biochem Nutr 2012;51:114-116. https://doi.org/10.3164/jcbn.D-11-00029R1
  23. Oh HS, Lee DH, Seo JY, et al. Ten-day sequential therapy is more effective than proton pump inhibitor-based therapy in Korea: a prospective, randomized study. J Gastroenterol Hepatol 2012;27:504-509. https://doi.org/10.1111/j.1440-1746.2011.06922.x
  24. Basu PP, Rayapudi K, Pacana T, Shah NJ, Krishnaswamy N, Flynn M. A randomized study comparing levofloxacin, omeprazole, nitazoxanide, and doxycycline versus triple therapy for the eradication of Helicobacter pylori. Am J Gastroenterol 2011; 106:1970-1975. https://doi.org/10.1038/ajg.2011.306
  25. Perri F, Villani MR, Festa V, Quitadamo M, Andriulli A. Predictors of failure of Helicobacter pylori eradication with the standard 'Maastricht triple therapy'. Aliment Pharmacol Ther 2001;15: 1023-1029. https://doi.org/10.1046/j.1365-2036.2001.01006.x
  26. Bigard MA, Delchier JC, Riachi G, Thibault P, Barthelemy P. One-week triple therapy using omeprazole, amoxycillin and clarithromycin for the eradication of Helicobacter pylori in patients with non-ulcer dyspepsia: influence of dosage of omeprazole and clarithromycin. Aliment Pharmacol Ther 1998;12: 383-388. https://doi.org/10.1046/j.1365-2036.1998.00315.x
  27. De Francesco V, Giorgio F, Hassan C, et al. Worldwide H. pylori antibiotic resistance: a systematic review. J Gastrointestin Liver Dis 2010;19:409-414.
  28. Kobayashi I, Murakami K, Kato M, et al. Changing antimicrobial susceptibility epidemiology of Helicobacter pylori strains in Japan between 2002 and 2005. J Clin Microbiol 2007;45: 4006-4010. https://doi.org/10.1128/JCM.00740-07
  29. Duck WM, Sobel J, Pruckler JM, et al. Antimicrobial resistance incidence and risk factors among Helicobacter pylori-infected persons, United States. Emerg Infect Dis 2004;10:1088-1094. https://doi.org/10.3201/eid1006.030744
  30. Megraud F, Coenen S, Versporten A, et al; Study Group participants. Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut 2013;62:34-42. https://doi.org/10.1136/gutjnl-2012-302254
  31. Rafeey M, Ghotaslou R, Nikvash S, Hafez AA. Primary resistance in Helicobacter pylori isolated in children from Iran. J Infect Chemother 2007;13:291-295. https://doi.org/10.1007/s10156-007-0543-6
  32. Datta S, Chattopadhyay S, Patra R, et al. Most Helicobacter pylori strains of Kolkata in India are resistant to metronidazole but susceptible to other drugs commonly used for eradication and ulcer therapy. Aliment Pharmacol Ther 2005;22:51-57. https://doi.org/10.1111/j.1365-2036.2005.02533.x
  33. Sherif M, Mohran Z, Fathy H, Rockabrand DM, Rozmajzl PJ, Frenck RW. Universal high-level primary metronidazole resistance in Helicobacter pylori isolated from children in Egypt. J Clin Microbiol 2004;42:4832-4834. https://doi.org/10.1128/JCM.42.10.4832-4834.2004
  34. Miyachi H, Miki I, Aoyama N, et al. Primary levofloxacin resistance and gyrA/B mutations among Helicobacter pylori in Japan. Helicobacter 2006;11:243-249. https://doi.org/10.1111/j.1523-5378.2006.00415.x
  35. Toracchio S, Marzio L. Primary and secondary antibiotic resistance of Helicobacter pylori strains isolated in central Italy during the years 1998-2002. Dig Liver Dis 2003;35:541-545. https://doi.org/10.1016/S1590-8658(03)00265-2
  36. Boyanova L. Prevalence of multidrug-resistant Helicobacter pylori in Bulgaria. J Med Microbiol 2009;58:930-935. https://doi.org/10.1099/jmm.0.009993-0
  37. Asrat D, Kassa E, Mengistu Y, Nilsson I, Wadstrom T. Antimicrobial susceptibility pattern of Helicobacter pylori strains isolated from adult dyspeptic patients in Tikur Anbassa University Hospital, Addis Ababa, Ethiopia. Ethiop Med J 2004;42:79-85.
  38. Nahar S, Mukhopadhyay AK, Khan R, et al. Antimicrobial susceptibility of Helicobacter pylori strains isolated in Bangladesh. J Clin Microbiol 2004;42:4856-4858. https://doi.org/10.1128/JCM.42.10.4856-4858.2004
  39. Boyanova L, Mitov I. Geographic map and evolution of primary Helicobacter pylori resistance to antibacterial agents. Expert Rev Anti Infect Ther 2010;8:59-70. https://doi.org/10.1586/eri.09.113
  40. Vakil N, Vaira D. Treatment for H. pylori infection: new challenges with antimicrobial resistance. J Clin Gastroenterol 2013;47:383-388. https://doi.org/10.1097/MCG.0b013e318277577b
  41. Su P, Li Y, Li H, et al. Antibiotic resistance of Helicobacter pylori isolated in the Southeast Coastal Region of China. Helicobacter 2013;18:274-279. https://doi.org/10.1111/hel.12046
  42. Kim JM, Kim JS, Jung HC, Kim N, Kim YJ, Song IS. Distribution of antibiotic MICs for Helicobacter pylori strains over a 16-year period in patients from Seoul, South Korea. Antimicrob Agents Chemother 2004;48:4843-4847. https://doi.org/10.1128/AAC.48.12.4843-4847.2004
  43. Lee JW, Kim N, Kim JM, et al. Prevalence of primary and secondary antimicrobial resistance of Helicobacter pylori in Korea from 2003 through 2012. Helicobacter 2013;18:206-214. https://doi.org/10.1111/hel.12031
  44. Kim JJ, Reddy R, Lee M, et al. Analysis of metronidazole, clarithromycin and tetracycline resistance of Helicobacter pylori isolates from Korea. J Antimicrob Chemother 2001;47:459-461. https://doi.org/10.1093/jac/47.4.459
  45. Kim JY, Kim NY, Kim SJ, et al. Regional difference of antibiotic resistance of Helicobacter pylori strains in Korea. Korean J Gastroenterol 2011;57:221-229. https://doi.org/10.4166/kjg.2011.57.4.221
  46. Kim JM. Antibiotic resistance of Helicobacter pylori isolated from Korean patients. Korean J Gastroenterol 2006;47:337-349.
  47. Asaka M, Kato M, Takahashi S, et al; Japanese Society for Helicobacter Research. Guidelines for the management of Helicobacter pylori infection in Japan: 2009 revised edition. Helicobacter 2010;15:1-20.
  48. Kim SG, Jung HK, Lee HL, et al; Korean College of Helicobacter and Upper Gastrointestinal Research. Guidelines for the diagnosis and treatment of Helicobacter pylori infection in Korea, 2013 revised edition. Korean J Gastroenterol 2013;62:3-26. https://doi.org/10.4166/kjg.2013.62.1.3
  49. Malfertheiner P, Megraud F, O'Morain CA, et al; European Helicobacter Study Group. Management of Helicobacter pylori infection--the Maastricht IV/ Florence Consensus Report. Gut 2012;61:646-664. https://doi.org/10.1136/gutjnl-2012-302084
  50. Chey WD, Wong BC; Practice Parameters Committee of the American College of Gastroenterology. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol 2007;102:1808-1825. https://doi.org/10.1111/j.1572-0241.2007.01393.x
  51. Fock KM, Katelaris P, Sugano K, et al; Second Asia-Pacific Conference. Second Asia-Pacific Consensus Guidelines for Helicobacter pylori infection. J Gastroenterol Hepatol 2009; 24:1587-1600. https://doi.org/10.1111/j.1440-1746.2009.05982.x
  52. Chinese Society of Gastroenterology, Chinese Study Group on Helicobacter pylori, Liu WZ, et al. Fourth Chinese National Consensus Report on the management of Helicobacter pylori infection. J Dig Dis 2013;14:211-221. https://doi.org/10.1111/1751-2980.12034
  53. Fukase K, Kato M, Kikuchi S, et al; Japan Gast Study Group. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008;372:392-397. https://doi.org/10.1016/S0140-6736(08)61159-9
  54. Gisbert JP, Khorrami S, Carballo F, Calvet X, Gené E, Dominguez-Munoz JE. H. pylori eradication therapy vs. antisecretory non-eradication therapy (with or without long-term maintenance antisecretory therapy) for the prevention of recurrent bleeding from peptic ulcer. Cochrane Database Syst Rev 2004;(2):CD004062.
  55. Wong BC, Lam SK, Wong WM, et al; China Gastric Cancer Study Group. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 2004;291:187-194. https://doi.org/10.1001/jama.291.2.187
  56. Ito M, Takata S, Tatsugami M, et al. Clinical prevention of gastric cancer by Helicobacter pylori eradication therapy: a systematic review. J Gastroenterol 2009;44:365-371. https://doi.org/10.1007/s00535-009-0036-8
  57. Kodama M, Murakami K, Okimoto T, et al. Helicobacter pylori eradication improves gastric atrophy and intestinal metaplasia in long-term observation. Digestion 2012;85:126-130. https://doi.org/10.1159/000334684
  58. Kodama M, Murakami K, Okimoto T, et al. Ten-year prospective follow-up of histological changes at five points on the gastric mucosa as recommended by the updated Sydney system after Helicobacter pylori eradication. J Gastroenterol 2012;47:394-403. https://doi.org/10.1007/s00535-011-0504-9
  59. de Martel C, Ferlay J, Franceschi S, et al. Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 2012;13:607-615. https://doi.org/10.1016/S1470-2045(12)70137-7
  60. Choi IJ. Current evidence of effects of Helicobacter pylori eradication on prevention of gastric cancer. Korean J Intern Med 2013;28:525-537. https://doi.org/10.3904/kjim.2013.28.5.525
  61. Lee YC, Chen TH, Chiu HM, et al. The benefit of mass eradication of Helicobacter pylori infection: a community-based study of gastric cancer prevention. Gut 2013;62:676-682. https://doi.org/10.1136/gutjnl-2012-302240
  62. Ma JL, Zhang L, Brown LM, et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst 2012; 104:488-492. https://doi.org/10.1093/jnci/djs003
  63. Asaka M, Kato M, Graham DY. Strategy for eliminating gastric cancer in Japan. Helicobacter 2010;15:486-490. https://doi.org/10.1111/j.1523-5378.2010.00799.x
  64. Asaka M. A new approach for elimination of gastric cancer deaths in Japan. Int J Cancer 2013;132:1272-1276. https://doi.org/10.1002/ijc.27965
  65. Wu CY, Kuo KN, Wu MS, Chen YJ, Wang CB, Lin JT. Early Helicobacter pylori eradication decreases risk of gastric cancer in patients with peptic ulcer disease. Gastroenterology 2009;137:1641-1648.e1-2. https://doi.org/10.1053/j.gastro.2009.07.060
  66. Asaka M, Kato M, Graham DY. Prevention of gastric cancer by Helicobacter pylori eradication. Intern Med 2010;49:633-636. https://doi.org/10.2169/internalmedicine.49.3470
  67. Lam SK, Talley NJ. Report of the 1997 Asia Pacific Consensus Conference on the management of Helicobacter pylori infection. J Gastroenterol Hepatol 1998;13:1-12. https://doi.org/10.1111/j.1440-1746.1998.tb00537.x
  68. European Helicobacter pylori Study Group. Current European concepts in the management of Helicobacter pylori infection. The Maastricht Consensus Report. Gut 1997;41:8-13. https://doi.org/10.1136/gut.41.1.8
  69. Graham DY, Fischbach L. Helicobacter pylori treatment in the era of increasing antibiotic resistance. Gut 2010;59:1143-1153. https://doi.org/10.1136/gut.2009.192757
  70. Zullo A, Rinaldi V, Winn S, et al. A new highly effective short-term therapy schedule for Helicobacter pylori eradication. Aliment Pharmacol Ther 2000;14:715-718. https://doi.org/10.1046/j.1365-2036.2000.00766.x
  71. Jafri NS, Hornung CA, Howden CW. Meta-analysis: sequential therapy appears superior to standard therapy for Helicobacter pylori infection in patients naive to treatment. Ann Intern Med 2008;148:923-931. https://doi.org/10.7326/0003-4819-148-12-200806170-00226
  72. 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. https://doi.org/10.1038/ajg.2009.555
  73. Tong JL, Ran ZH, Shen J, Xiao SD. Sequential therapy vs. standard triple therapies for Helicobacter pylori infection: a meta-analysis. J Clin Pharm Ther 2009;34:41-53. https://doi.org/10.1111/j.1365-2710.2008.00969.x
  74. Urgesi R, Pelecca G, Cianci R, et al. Helicobacter pylori infection: is sequential therapy superior to standard triple therapy? A single-centre Italian study in treatment-naive and non-treatment-naive patients. Can J Gastroenterol 2011;25: 315-318. https://doi.org/10.1155/2011/967671
  75. Paoluzi OA, Visconti E, Andrei F, et al. Ten and eight-day sequential therapy in comparison to standard triple therapy for eradicating Helicobacter pylori infection: a randomized controlled study on efficacy and tolerability. J Clin Gastroenterol 2010;44: 261-266. https://doi.org/10.1097/MCG.0b013e3181acebef
  76. Romano M, Cuomo A, Gravina AG, et al. Empirical levofloxacin- containing versus clarithromycin-containing sequential therapy for Helicobacter pylori eradication: a randomised trial. Gut 2010;59:1465-1470. https://doi.org/10.1136/gut.2010.215350
  77. Zullo A, Scaccianoce G, De Francesco V, et al. Concomitant, sequential, and hybrid therapy for H. pylori eradication: a pilot study. Clin Res Hepatol Gastroenterol 2013;37:647-650. https://doi.org/10.1016/j.clinre.2013.04.003
  78. Molina-Infante J, Perez-Gallardo B, Fernandez-Bermejo M, et al. Clinical trial: clarithromycin vs. levofloxacin in first-line triple and sequential regimens for Helicobacter pylori eradication. Aliment Pharmacol Ther 2010;31:1077-1084.
  79. McNicholl AG, Marin AC, Molina-Infante J, et al; Participant Centres. Randomised clinical trial comparing sequential and concomitant therapies for Helicobacter pylori eradication in routine clinical practice. Gut 2014;63:244-249. https://doi.org/10.1136/gutjnl-2013-304820
  80. Gatta L, Vakil N, Vaira D, Scarpignato C. Global eradication rates for Helicobacter pylori infection: systematic review and meta-analysis of sequential therapy. BMJ 2013;347:f4587. https://doi.org/10.1136/bmj.f4587
  81. Kim JS, Kim BW, Ham JH, et al. Sequential therapy for Helicobacter pylori infection in Korea: systematic review and meta-analysis. Gut Liver 2013;7:546-551. https://doi.org/10.5009/gnl.2013.7.5.546
  82. Yoon H, Lee DH, Kim N, et al. Meta-analysis: is sequential therapy superior to standard triple therapy for Helicobacter pylori infection in Asian adults? J Gastroenterol Hepatol 2013;28: 1801-1809. https://doi.org/10.1111/jgh.12397
  83. Vaira D, Zullo A, Vakil N, et al. Sequential therapy versus standard triple-drug therapy for Helicobacter pylori eradication: a randomized trial. Ann Intern Med 2007;146:556-563. https://doi.org/10.7326/0003-4819-146-8-200704170-00006
  84. Zullo A, Perna F, Hassan C, et al. Primary antibiotic resistance in Helicobacter pylori strains isolated in northern and central Italy. Aliment Pharmacol Ther 2007;25:1429-1434. https://doi.org/10.1111/j.1365-2036.2007.03331.x
  85. Chung JW, Jung YK, Kim YJ, et al. Ten-day sequential versus triple therapy for Helicobacter pylori eradication: a prospective, open-label, randomized trial. J Gastroenterol Hepatol 2012; 27:1675-1680. https://doi.org/10.1111/j.1440-1746.2012.07249.x
  86. Abadi AT, Taghvaei T, Mobarez AM, Carpenter BM, Merrell DS. Frequency of antibiotic resistance in Helicobacter pylori strains isolated from the northern population of Iran. J Microbiol 2011;49:987-993. https://doi.org/10.1007/s12275-011-1170-6
  87. Thyagarajan SP, Ray P, Das BK, et al. Geographical difference in antimicrobial resistance pattern of Helicobacter pylori clinical isolates from Indian patients: multicentric study. J Gastroenterol Hepatol 2003;18:1373-1378. https://doi.org/10.1046/j.1440-1746.2003.03174.x
  88. Graham DY, Lee YC, Wu MS. Rational Helicobacter pylori therapy: evidence-based medicine rather than medicine-based evidence. Clin Gastroenterol Hepatol 2014;12:177-186.e3. https://doi.org/10.1016/j.cgh.2013.05.028
  89. Essa AS, Kramer JR, Graham DY, Treiber G. Meta-analysis: four-drug, three-antibiotic, non-bismuth-containing "concomitant therapy" versus triple therapy for Helicobacter pylori eradication. Helicobacter 2009;14:109-118. https://doi.org/10.1111/j.1523-5378.2009.00671.x
  90. Fischbach LA, van Zanten S, Dickason J. Meta-analysis: the efficacy, adverse events, and adherence related to first-line anti- Helicobacter pylori quadruple therapies. Aliment Pharmacol Ther 2004;20:1071-1082. https://doi.org/10.1111/j.1365-2036.2004.02248.x
  91. Gisbert JP, Calvet X. Review article: non-bismuth quadruple (concomitant) therapy for eradication of Helicobater pylori. Aliment Pharmacol Ther 2011;34:604-617. https://doi.org/10.1111/j.1365-2036.2011.04770.x
  92. Kim SY, Lee SW, Hyun JJ, et al. Comparative study of Helicobacter pylori eradication rates with 5-day quadruple "concomitant" therapy and 7-day standard triple therapy. J Clin Gastroenterol 2013;47:21-24. https://doi.org/10.1097/MCG.0b013e3182548ad4
  93. Hsu PI, Wu DC, Wu JY, Graham DY. Modified sequential Helicobacter pylori therapy: proton pump inhibitor and amoxicillin for 14 days with clarithromycin and metronidazole added as a quadruple (hybrid) therapy for the final 7 days. Helicobacter 2011;16:139-145. https://doi.org/10.1111/j.1523-5378.2011.00828.x
  94. Sardarian H, Fakheri H, Hosseini V, et al. Comparison of hybrid and sequential therapies for Helicobacter pylori eradication in Iran: a prospective randomized trial. Helicobacter 2013;18: 129-134. https://doi.org/10.1111/hel.12017
  95. Molina-Infante J, Romano M, Fernandez-Bermejo M, et al. Optimized nonbismuth quadruple therapies cure most patients with Helicobacter pylori infection in populations with high rates of antibiotic resistance. Gastroenterology 2013; 145:121-128.e1. https://doi.org/10.1053/j.gastro.2013.03.050
  96. Suzuki T, Matsuo K, Ito H, et al. Smoking increases the treatment failure for Helicobacter pylori eradication. Am J Med 2006;119:217-224. https://doi.org/10.1016/j.amjmed.2005.10.003
  97. Sargyn M, Uygur-Bayramicli O, Sargyn H, Orbay E, Yavuzer D, Yayla A. Type 2 diabetes mellitus affects eradication rate of Helicobacter pylori. World J Gastroenterol 2003;9:1126-1128. https://doi.org/10.3748/wjg.v9.i5.1126
  98. Osawa H, Kawakami M, Fujii M, et al. Helicobacter pylori infection and coronary heart disease in Japanese patients. Cardiology 2001;95:14-19. https://doi.org/10.1159/000047337
  99. Aydemir S, Boyacioglu S, Gur G, et al. Helicobacter pylori infection in hemodialysis patients: susceptibility to amoxicillin and clarithromycin. World J Gastroenterol 2005;11:842-845. https://doi.org/10.3748/wjg.v11.i6.842
  100. Dickson EJ, Stuart RC. Genetics of response to proton pump inhibitor therapy: clinical implications. Am J Pharmacogenomics 2003;3:303-315.
  101. Chong E, Ensom MH. Pharmacogenetics of the proton pump inhibitors: a systematic review. Pharmacotherapy 2003;23:460-471. https://doi.org/10.1592/phco.23.4.460.32128
  102. Padol S, Yuan Y, Thabane M, Padol IT, Hunt RH. The effect of CYP2C19 polymorphisms on H. pylori eradication rate in dual and triple first-line PPI therapies: a meta-analysis. Am J Gastroenterol 2006;101:1467-1475. https://doi.org/10.1111/j.1572-0241.2006.00717.x
  103. McNicholl AG, Linares PM, Nyssen OP, Calvet X, Gisbert JP. Meta-analysis: esomeprazole or rabeprazole vs. first-generation pump inhibitors in the treatment of Helicobacter pylori infection. Aliment Pharmacol Ther 2012;36:414-425. https://doi.org/10.1111/j.1365-2036.2012.05211.x
  104. Zhao F, Wang J, Yang Y, et al. Effect of CYP2C19 genetic polymorphisms on the efficacy of proton pump inhibitor-based triple therapy for Helicobacter pylori eradication: a meta-analysis. Helicobacter 2008;13:532-541. https://doi.org/10.1111/j.1523-5378.2008.00643.x
  105. Tang HL, Li Y, Hu YF, Xie HG, Zhai SD. Effects of CYP2C19 loss-of-function variants on the eradication of H. pylori infection in patients treated with proton pump inhibitor-based triple therapy regimens: a meta-analysis of randomized clinical trials. PLoS One 2013;8:e62162. https://doi.org/10.1371/journal.pone.0062162
  106. Lee JH, Jung HY, Choi KD, Song HJ, Lee GH, Kim JH. The influence of CYP2C19 polymorphism on eradication of Helicobacter pylori: a prospective randomized study of lansoprazole and rabeprazole. Gut Liver 2010;4:201-206. https://doi.org/10.5009/gnl.2010.4.2.201
  107. Kang JM, Kim N, Lee DH, et al. Effect of the CYP2C19 polymorphism on the eradication rate of Helicobacter pylori infection by 7-day triple therapy with regular proton pump inhibitor dosage. J Gastroenterol Hepatol 2008;23:1287-1291. https://doi.org/10.1111/j.1440-1746.2008.05392.x
  108. Houben MH, van de Beek D, Hensen EF, de Craen AJ, Rauws EA, Tytgat GN. A systematic review of Helicobacter pylori eradication therapy--the impact of antimicrobial resistance on eradication rates. Aliment Pharmacol Ther 1999;13:1047-1055. https://doi.org/10.1046/j.1365-2036.1999.00555.x
  109. Kim N, Kim JM, Kim CH, et al. Institutional difference of antibiotic resistance of Helicobacter pylori strains in Korea. J Clin Gastroenterol 2006;40:683-687. https://doi.org/10.1097/00004836-200609000-00004
  110. Hwang TJ, Kim N, Kim HB, et al. Change in antibiotic resistance of Helicobacter pylori strains and the effect of A2143G point mutation of 23S rRNA on the eradication of H. pylori in a single center of Korea. J Clin Gastroenterol 2010;44:536-543.
  111. Woo HY, Park DI, Park H, et al. Dual-priming oligonucleotide- based multiplex PCR for the detection of Helicobacter pylori and determination of clarithromycin resistance with gastric biopsy specimens. Helicobacter 2009;14:22-28. https://doi.org/10.1111/j.1523-5378.2009.00654.x
  112. Gerrits MM, van Vliet AH, Kuipers EJ, Kusters JG. Helicobacter pylori and antimicrobial resistance: molecular mechanisms and clinical implications. Lancet Infect Dis 2006;6:699-709. https://doi.org/10.1016/S1473-3099(06)70627-2
  113. Shin WG. New trend of Helicobacter pylori treatment. Korean J Med 2013;85:586-588. https://doi.org/10.3904/kjm.2013.85.6.586
  114. Lee HJ, Kim JI, Cheung DY, et al. Eradication of Helicobacter pylori according to 23S ribosomal RNA point mutations associated with clarithromycin resistance. J Infect Dis 2013;208: 1123-1130. https://doi.org/10.1093/infdis/jit287
  115. Furuta T, Shirai N, Kodaira M, et al. Pharmacogenomics-based tailored versus standard therapeutic regimen for eradication of H. pylori. Clin Pharmacol Ther 2007;81:521-528. https://doi.org/10.1038/sj.clpt.6100043

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