Helicobacter pylori Eradication Therapies in the Era of Increasing Antibiotic Resistance: A Paradigm Shift to Improved Efficacy

Sotirios D Georgopoulos, Vasilios Papastergiou, Stylianos Karatapanis, Sotirios D Georgopoulos, Vasilios Papastergiou, Stylianos Karatapanis

Abstract

With the rising prevalence of antimicrobial resistance, the eradication rates of Helicobacter pylori (H. pylori) with standard treatments are decreasing to unacceptable levels (i.e., ≤80%) in most countries. After these disappointing results, several authorities have proposed that infection with H. pylori should be approached and treated as any other bacterial infectious disease. This implicates that clinicians should prescribe empirical treatments yielding a per protocol eradication of at least 90%. In recent years several treatments producing ≥90% cure rates have been proposed including sequential therapy, concomitant quadruple therapy, hybrid (dual-concomitant) therapy, and bismuth-containing quadruple therapy. These treatments are likely to represent the recommended first-line treatments in the near future. In the present paper, we are considering a series of critical issues regarding currently available means and approaches for the management of H. pylori infection. Clinical needs and realistic endpoints are taken into account. Furthermore, emerging strategies for the eradication of H. pylori and the existing evidence of their clinical validation and widespread applicability are discussed.

References

    1. Moayyedi P, Hunt RH. Helicobacter pylori public health implications. Helicobacter. 2004;9(supplement 1):67–72.
    1. Suerbaum S, Michetti P. Helicobacter pylori infection. The New England Journal of Medicine. 2002;347(15):1175–1186.
    1. Fuccio L, Zagari RM, Eusebi LH, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Annals of Internal Medicine. 2009;151(2):121–128.
    1. Fukase K, Kato M, Kikuchi S, et al. 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. The Lancet. 2008;372(9636):392–397.
    1. Malfertheiner P, Chan FK, McColl KE. Peptic ulcer disease. The Lancet. 2009;374(9699):1449–1461.
    1. Stathis A, Bertoni F, Zucca E. Treatment of gastric marginal zone lymphoma of MALT type. Expert Opinion on Pharmacotherapy. 2010;11(13):2141–2152.
    1. Graham DY. Antibiotic resistance in Helicobacter pylori: implications for therapy. Gastroenterology. 1998;115(5):1272–1277.
    1. Mégraud F. H pylori antibiotic resistance: prevalence, importance, and advances in testing. Gut. 2004;53(9):1374–1384.
    1. Megraud F. Helicobacter pylori and antibiotic resistance. Gut. 2007;56(11):p. 1502.
    1. Broutet N, Tchamgoué S, Pereira E, Lamouliatte H, Salamon R, Mégraud F. Risk factors for failure of Helicobacter pylori therapy—results of an individual data analysis of 2751 patients. Alimentary Pharmacology & Therapeutics. 2003;17(1):99–109.
    1. Georgopoulos SD, Ladas SD, Karatapanis S, et al. Factors that may affect treatment outcome of triple Helicobacter pylori eradication therapy with omeprazole, amoxicillin, and clarithromycin. Digestive Diseases and Sciences. 2000;45(1):63–67.
    1. Current European concepts in the management of Helicobacter pylori infection. The Maastricht Consensus Report. European Helicobacter Pylori Study Group. Gut. 1997;41(1):8–13.
    1. Lind T, van Zanten SV, Unge P, et al. Eradication of Helicobacter pylori using one-week triple therapies combining omeprazole with two antimicrobials: the MACH I study. Helicobacter. 1996;1(3):138–144.
    1. De Francesco V, Margiotta M, Zullo A, et al. Prevalence of primary clarithromycin resistance in Helicobacter pylori strains over a 15 year period in Italy. Journal of Antimicrobial Chemotherapy. 2007;59(4):783–785.
    1. Gisbert JP, Pajares R, Pajares JM. Evolution of Helicobacter pylori therapy from a meta-analytical perspective. Helicobacter. 2007;12(supplement 2):50–58.
    1. De Francesco V, Giorgio F, Hassan C, et al. Worldwide H. pylori antibiotic resistance: a systematic review. Journal of Gastrointestinal and Liver Diseases. 2010;19(4):409–414.
    1. Fischbach LA, Goodman KJ, Feldman M, Aragaki C. Sources of variation of Helicobacter pylori treatment success in adults worldwide: a meta-analysis. International Journal of Epidemiology. 2002;31(1):128–139.
    1. Janssen MJ, Van Oijen AH, Verbeek AL, Jansen JB, De Boer WA. A systematic comparison of triple therapies for treatment of Helicobacter pylori infection with proton pump inhibitor/ranitidine bismuth citrate plus clarithromycin and either amoxicillin or a nitroimidazole. Alimentary Pharmacology & Therapeutics. 2001;15(5):613–624.
    1. Laheij RJ, Rossum LG, Jansen JB, Straatman H, Verbeek AL. Evaluation of treatment regimens to cure Helicobacter pylori infection—a meta-analysis. Alimentary Pharmacology & Therapeutics. 1999;13(7):857–864.
    1. Malfertheiner P, Mégraud F, O’Morain C, et al. Current concepts in the management of Helicobacter pylori infection—the Maastricht 2-2000 Consensus Report. Alimentary Pharmacology & Therapeutics. 2002;16(2):167–180.
    1. Katelaris PH, Forbes GM, Talley NJ, Crotty B. A randomized comparison of quadruple and triple therapies for Helicobacter pylori eradication: the QUADRATE study. Gastroenterology. 2002;123(6):1763–1769.
    1. Calvet X, Ducons J, Guardiola J, et al. One-week triple vs. quadruple therapy for Helicobacter pylori infection—a randomized trial. Alimentary Pharmacology & Therapeutics. 2002;16(7):1261–1267.
    1. Luther J, Higgins PD, Schoenfeld PS, Moayyedi P, Vakil N, Chey WD. Empiric quadruple vs. triple therapy for primary treatment of Helicobacter pylori infection: systematic review and meta-analysis of efficacy and tolerability. American Journal of Gastroenterology. 2010;105(1):65–73.
    1. Graham DY, Dore MP. Helicobacter pylori therapy demystified. Helicobacter. 2011;16(5):343–345.
    1. Chey WD, Wong BC. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. American Journal of Gastroenterology. 2007;102(8):1808–1825.
    1. Caselli M, Zullo A, Maconi G, et al. ‘Cervia II Working Group Report 2006’: guidelines on diagnosis and treatment of Helicobacter pylori infection in Italy. Digestive and Liver Disease. 2007;39(8):782–789.
    1. Maconi G, Tosetti C, Miroglio G, et al. Management of Helicobacter pylori-related gastrointestinal diseases by general practitioners in Italy. Alimentary Pharmacology & Therapeutics. 1999;13(11):1499–1504.
    1. Georgopoulos SD, Ladas SD, Karatapanis S, et al. Effectiveness of two quadruple, tetracycline- or clarithromycin-containing, second-line, Helicobacter pylori eradication therapies. Alimentary Pharmacology & Therapeutics. 2002;16(3):569–575.
    1. Mantzaris GJ, Petraki K, Archavlis E, et al. Omeprazole triple therapy versus omeprazole quadruple therapy for healing duodenal ulcer and eradication of Helicobacter pylori infection: 24-month follow-up study. European Journal of Gastroenterology and Hepatology. 2002;14(11):1237–1243.
    1. Karatapanis S, Georgopoulos SD, Papastergiou V, et al. 7, 10 and 14-days rabeprazole-based standard triple therapies for H. pylori eradication: are they still effective? A randomized trial. Acta Gastroenterol Belg. 2011;74(3):407–412.
    1. Rokkas T, Sechopoulos P, Robotis I, Margantinis G, Pistiolas D. Cumulative H. pylori eradication rates in clinical practice by adopting first and second-line regimens proposed by the Maastricht III consensus and a third-line empirical regimen. American Journal of Gastroenterology. 2009;104(1):21–25.
    1. Boyanova L, Mentis A, Gubina M, et al. The status of antimicrobial resistance of Helicobacter pylori in Eastern Europe. Clinical Microbiology and Infection. 2002;8(7):388–396.
    1. Glupczynski Y, Mégraud F, Lopez-Brea M, Andersen LP. European multicentre survey of in vitro antimicrobial resistance in Helicobacter pylori. European Journal of Clinical Microbiology and Infectious Diseases. 2001;20(11):820–823.
    1. Mentis AF, Roma E, Pangalis A, Katsiyiannakis E. Susceptibilities of Helicobacter pylori strains isolated from children with gastritis to selected antibiotics. Journal of Antimicrobial Chemotherapy. 1999;44(5):720–722.
    1. Gisbert JP, Gisbert JL, Marcos S, Jimenez-Alonso I, Moreno-Otero R, Pajares JM. Empirical rescue therapy after Helicobacter pylori treatment failure: a 10-year single-centre study of 500 patients. Alimentary Pharmacology & Therapeutics. 2008;27(4):346–354.
    1. Seppälä K, Kosunen TU, Veijola L, et al. Cure of Helicobacter pylori infection in all compliant patients: report on 644 subjects. Scandinavian Journal of Gastroenterology. 2008;43(9):1149–1150.
    1. Fuccio L, Zagari RM, Bazzoli F. What is the best salvage therapy for patients with Helicobacter pylori infection? Nature Clinical Practice Gastroenterology and Hepatology. 2008;5(11):608–609.
    1. Huang JQ, Hunt RH. Treatment after failure: the problem of ‘non-responders’. Gut. 1999;45(supplement 1):I40–I44.
    1. Chuah SK, Tsay FW, Hsu PI, Wu DC. A new look at anti-Helicobacter pylori therapy. World Journal of Gastroenterology. 2011;17(35):3971–3975.
    1. Graham DY, Lu H, Yamaoka Y. A report card to grade Helicobacter pylori therapy. Helicobacter. 2007;12(4):275–278.
    1. Graham DY. Efficient identification and evaluation of effective Helicobacter pylori therapies. Clinical Gastroenterology and Hepatology. 2009;7(2):145–148.
    1. Graham DY, Fischbach L. Helicobacter pylori treatment in the era of increasing antibiotic resistance. Gut. 2010;59(8):1143–1153.
    1. Gisbert JP, Calvet X, O’Connor A, Mégraud F, O’Morain CA. Sequential therapy for Helicobacter pylori eradication: a critical review. Journal of Clinical Gastroenterology. 2010;44(5):313–325.
    1. Moayyedi P. Sequential regimens for Helicobacter pylori eradication. The Lancet. 2007;370(9592):1010–1012.
    1. Jafri NS, Hornung CA, Howden CW. Meta-analysis: sequential therapy appears superior to standard therapy for Helicobacter pylori infection in patients naive to treatment. Annals of Internal Medicine. 2008;148(12):923–931.
    1. Tong JL, Ran ZH, Shen J, Xiao SD. Sequential therapy vs. standard triple therapies for Helicobacter pylori infection: a meta-analysis. Journal of Clinical Pharmacy and Therapeutics. 2009;34(1):41–53.
    1. 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. American Journal of Gastroenterology. 2009;104(12):3069–3079.
    1. Zullo A, De Francesco V, Hassan C, Morini S, Vaira D. The sequential therapy regimen for Helicobacter pylori eradication: a pooled-data analysis. Gut. 2007;56(10):1353–1357.
    1. Vaira D, Zullo A, Vakil N, et al. Sequential therapy versus standard triple-drug therapy for Helicobacter pylori eradication: a randomized trial. Annals of Internal Medicine. 2007;146(8):556–563.
    1. Wu DC, Hsu PI, Wu JY, et al. Sequential and concomitant therapy with four drugs is equally effective for eradication of H pylori infection. Clinical Gastroenterology and Hepatology. 2010;8(1):36.e1–41.e1.
    1. Paulsen IT, Brown MH, Skurray RA. Proton-dependent multidrug efflux systems. Microbiological Reviews. 1996;60(4):575–608.
    1. Webber MA, Piddock LJ. The importance of efflux pumps in bacterial antibiotic resistance. Journal of Antimicrobial Chemotherapy. 2003;51(1):9–11.
    1. Roberts MC. Resistance to macrolide, lincosamide, streptogramin, ketolide, and oxazolidinone antibiotics. Molecular Biotechnology. 2004;28(1):47–62.
    1. Molina-Infante J, Pazos-Pacheco C, Perez-Gallardo B. Efficacy of nonbismuth quadruple “concomitant” therapy for H. pylori infection in a setting with high clarithromycin resistance. Helicobacter. 2011;138, article 880(supplement 1)
    1. 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. Alimentary Pharmacology & Therapeutics. 2010;31(10):1077–1084.
    1. de Boer WA, Kuipers EJ, Kusters JG. Sequential therapy; a new treatment for Helicobacter pylori infection: but is it ready for general use? Digestive and Liver Disease. 2004;36(5):311–314.
    1. Sánchez-Delgado J, Calvet X, Bujanda L, Gisbert JP, Titó L, Castro M. Ten-day sequential treatment for Helicobacter pylori eradication in clinical practice. American Journal of Gastroenterology. 2008;103(9):2220–2223.
    1. O’Morain CA, O’Connor JP. Is sequential therapy superior to standard triple therapy for the treatment of Helicobacter pylori infection? Nature Clinical Practice Gastroenterology and Hepatology. 2009;6(1):8–9.
    1. Moayyedi P, Malfertheiner P. Editorial: sequential therapy for eradication of Helicobacter pylori: a new guiding light or a false dawn? American Journal of Gastroenterology. 2009;104(12):3081–3083.
    1. Luther J, Chey WD. Sequential therapy for Helicobacter pylori: a two for one deal that’s worth the extra effort? Gastroenterology. 2009;136(2):720–722.
    1. Choi WH, Park DI, Oh SJ, et al. Effectiveness of 10 day-sequential therapy for Helicobacter pylori eradication in Korea. The Korean Journal of Gastroenterology. 2008;51(5):280–284.
    1. Gao XZ, Qiao XL, Song WC, Wang XF, Liu F. Standard triple, bismuth pectin quadruple and sequential therapies for Helicobacter pylori eradication. World Journal of Gastroenterology. 2010;16(34):4357–4362.
    1. Greenberg ER, Anderson GL, Morgan DR, et al. 14-day triple, 5-day concomitant, and 10-day sequential therapies for Helicobacter pylori infection in seven Latin American sites: a randomised trial. The Lancet. 2011;378(9790):507–514.
    1. Graham DY, Rimbara E. Understanding and appreciating sequential therapy for Helicobacter pylori eradication. Journal of Clinical Gastroenterology. 2011;45(4):309–313.
    1. Park HG, Jung MK, Jung JT, et al. Randomised clinical trial: a comparative study of 10-day sequential therapy with 7-day standard triple therapy for Helicobacter pylori infection in naive patients. Alimentary Pharmacology & Therapeutics. 2012;35(1):56–65.
    1. Merali A, Leontiadis GI. Sequential therapy—more studies are still required. Alimentary Pharmacology & Therapeutics. 2012;35(1):194–195.
    1. Gisbert JP, Calvet X. Review article: non-bismuth quadruple (concomitant) therapy for eradication of Helicobater pylori. Alimentary Pharmacology & Therapeutics. 2011;34(6):604–617.
    1. Fakheri H, Taghvaei T, Hosseini V, Bari Z. A comparison between sequential therapy and a modified bismuth-based quadruple therapy for Helicobacter pylori eradication in Iran: a randomized clinical trial. Helicobacter. 2012;17(1):43–48.
    1. Graham DY, Shiotani A. New concepts of resistance in the treatment of Helicobacter pylori infections. Nature Clinical Practice Gastroenterology and Hepatology. 2008;5(6):321–331.
    1. Treiber G, Wittig J, Ammon S, Walker S, van Doorn LJ, Klotz U. Clinical outcome and influencing factors of a new short-term quadruple therapy for Helicobacter pylori eradication: a randomized controlled trial (MACLOR study) Archives of Internal Medicine. 2002;162(2):153–160.
    1. 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(2):109–118.
    1. Fischbach LA, Bravo LE, Zarama GR, et al. A randomized clinical trial to determine the efficacy of regimens containing clarithromycin, metronidazole, and amoxicillin among histologic subgroups for Helicobacter pylori eradication in a developing country. Helicobacter. 2009;14(2):100–108.
    1. Hsu PI, Wu DC, Wu JY, Graham DY. Modified sequential Helicobacter pylori therapy: proton pump inhibitor and amoxicilin for 14 days with clarithromycin and metronidazole added as a quadruple (hybrid) therapy for the final 7 days. Helicobacter. 2011;16(2):146–152.
    1. Georgopoulos S, Papastergiou V, Xirouchakis E, et al. Evaluation of a four-drug, three-antibiotic, nonbismuth-containing “concomitant” therapy as first-line Helicobacter pylori eradication regimen in Greece. Helicobacter. 2011;16(2):139–145.
    1. Georgopoulos SD, Xirouchakis E, Laoudi F. Clinical evaluation of a 10-day regimenwith esomeprazole, metronidazole, amoxycilline and clarithromycin for the eradication of Helicobacter pylori (E-MACH study) Helicobacter. 2011;16, article A136(supplement 1)
    1. Liou JM, Lin JT, Chang CY, et al. Levofloxacin-based and clarithromycin-based triple therapies as first-line and second-line treatments for Helicobacter pylori infection: a randomised comparative trial with crossover design. Gut. 2010;59(5):572–578.
    1. Malfertheiner P, Megraud F, O’Morain C, et al. Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut. 2007;56(6):772–781.
    1. Fischbach LA, van Zanten S, Dickason J. Meta-analysis: the efficacy, adverse events, and adherence related to first-line anti-Helicobacter pylori quadruple therapies. Alimentary Pharmacology & Therapeutics. 2004;20(10):1071–1082.
    1. Fischbach L, Evans EL. Meta-analysis: the effect of antibiotic resistance status on the efficacy of triple and quadruple first-line therapies for Helicobacter pylori. Alimentary Pharmacology & Therapeutics. 2007;26(3):343–357.
    1. Michopoulos S, Tsibouris P, Bouzakis H, et al. Randomized study comparing omeprazole with ranitidine as anti-secretory agents combined in quadruple second-Iine Helicobacter pylori eradication regimens. Alimentary Pharmacology & Therapeutics. 2000;14(6):737–744.
    1. Perri F, Festa V, Merla A, Quitadamo M, Clemente R, Andriulli A. Amoxicillin/tetracycline combinations are inadequate as alternative therapies for Helicobacter pylori infection. Helicobacter. 2002;7(2):99–104.
    1. Garcia N, Calvet X, Gene E, Campo R, Brullet E. Limited usefulness of a seven-day twice-a-day quadruple therapy. European Journal of Gastroenterology and Hepatology. 2000;12(12):1315–1318.
    1. de Boer WA, van Etten RJ, Schneeberger PM, Tytgat GN. A single drug for Helicobacter pylori infection: first results with a new bismuth triple monocapsule. American Journal of Gastroenterology. 2000;95(3):641–645.
    1. de Boer WA. A novel therapeutic approach for Helicobacter pylori infection: the bismuth-based triple therapy monocapsule. Expert Opinion on Investigational Drugs. 2001;10(8):1559–1566.
    1. Laine L, Hunt R, EI-Zimaity H, Nguyen B, Osato M, Spénard J. 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, multicenter, North American trial. American Journal of Gastroenterology. 2003;98(3):562–567.
    1. O’Morain C, Borody T, Farley A, et al. Efficacy and safety of single-triple capsules of bismuth biskalcitrate, metronidazole and tetracycline, given with omeprazole, for the eradication of Helicobacter pylori: an international multicentre study. Alimentary Pharmacology & Therapeutics. 2003;17(3):415–420.
    1. Saleem A, Qasim A, O’Connor HJ, O’Morain CA. Pylera for the eradication of Helicobacter pylori infection. Expert Review of Anti-Infective Therapy. 2009;7(7):793–799.
    1. Malfertheiner P, Bazzoli F, Delchier JC, et al. Helicobacter pylori eradication with a capsule containing bismuth subcitrate potassium, metronidazole, and tetracycline given with omeprazole versus clarithromycin-based triple therapy: a randomised, open-label, non-inferiority, phase 3 trial. The Lancet. 2011;377(9769):905–913.
    1. 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(11):1465–1470.
    1. Berning M, Krasz S, Miehlke S. Should quinolones come first in Helicobacter pylori therapy? Therapeutic Advances in Gastroenterology. 2011;4(2):103–114.
    1. Perna F, Zullo A, Ricci C, Hassan C, Morini S, Vaira D. Levofloxacin-based triple therapy for Helicobacter pylori re-treatment: role of bacterial resistance. Digestive and Liver Disease. 2007;39(11):1001–1005.
    1. Bogaerts P, Berhin C, Nizet H, Glupczynski Y. Prevalence and mechanisms of resistance to fluoroquinolones in Helicobacter pylori strains from patients living in Belgium. Helicobacter. 2006;11(5):441–445.
    1. Carothers JJ, Bruce MG, Hennessy TW, et al. The relationship between previous fluoroquinolone use and levofloxacin resistance in Helicobacter pylori infection. Clinical Infectious Diseases. 2007;44(2):e5–e8.
    1. van der Linden PD, Sturkenboom MC, Herings RM, Leufkens HG, Stricker BH. Fluoroquinolones and risk of achilles tendon disorders: case-control study. British Medical Journal. 2002;324(7349):1306–1307.
    1. Croom KF, Goa KL. Levofloxacin: a review of its use in the treatment of bacterial infections in the United States. Drugs. 2003;63(24):2769–2802.
    1. Bilardi C, Dulbecco P, Zentilin P, et al. A 10-day levofloxacin-based therapy in patients with resistant Helicobacter pylori infection: a controlled trial. Clinical Gastroenterology and Hepatology. 2004;2(11):997–1002.
    1. Saad RJ, Schoenfeld P, Kim HM, Chey WD. Levofloxacin-based triple therapy versus bismuth-based quadruple therapy for persistent Helicobacter pylori infection: a meta-analysis. American Journal of Gastroenterology. 2006;101(3):488–496.
    1. Gisbert JP, Bermejo F, Castro-Fernández M, et al. Second-line rescue therapy with levofloxacin after H. pylori treatment failure: a Spanish multicenter study of 300 patients. American Journal of Gastroenterology. 2008;103(1):71–76.
    1. Gisbert JP. Second-line rescue therapy of Helicobacter pylori infection. Therapeutic Advances in Gastroenterology. 2009;2(6):331–356.
    1. Gisbert JP, Gisbert JL, Marcos S, Moreno-Otero R, Pajares JM. Third-line rescue therapy with levofloxacin is more effective than rifabutin rescue regimen after two Helicobacter pylori treatment failures. Alimentary Pharmacology & Therapeutics. 2006;24(10):1469–1474.
    1. Nishizawa T, Suzuki H, Hibi T. Quinolone-based third-line therapy for Helicobacter pylori eradication. Journal of Clinical Biochemistry and Nutrition. 2009;44(2):119–124.
    1. Karatapanis S, Skorda L, Georgopoulos SD, et al. Levofloxacin-based triple therapy versus bismuth-based quadruple therapy as a second line treatment for the eradication of H. pylori infection. Annals of Gastroenterology. 2009;22(4):263–267.
    1. Krystallis C, Kamberoglou D, Pistiolas D, et al. A new second-line sequential regimen for Helicobacter pylori eradication based on levofloxacin: a pilot study. Digestive Diseases and Sciences. 2010;55(12):3630–3631.
    1. Pontone S, Standoli M, Angelini R, Pontone P. Efficacy of H. pylori eradication with a sequential regimen followed by rescue therapy in clinical practice. Digestive and Liver Disease. 2010;42(8):541–543.
    1. Graham DY, Osato MS, Hoffman J, et al. Metronidazole containing quadruple therapy for infection with metronidazole resistant Helicobacter pylori: a prospective study. Alimentary Pharmacology & Therapeutics. 2000;14(6):745–750.
    1. Lee BH, Kim N, Hwang TJ, et al. Bismuth-containing quadruple therapy as second-line treatment for Helicobacter pylori infection: effect of treatment duration and antibiotic resistance on the eradication rate in Korea. Helicobacter. 2010;15(1):38–45.
    1. Sun Q, Liang X, Zheng Q, et al. High efficacy of 14-day triple therapy-based, bismuth-containing quadruple therapy for initial Helicobacter pylori eradication. Helicobacter. 2010;15(3):233–238.
    1. Graham DY, Javed SU, Keihanian S, Abudayyeh S, Opekun AR. Dual proton pump inhibitor plus amoxicillin as an empiric anti-H. pylori therapy: studies from the United States. Journal of Gastroenterology. 2010;45(8):816–820.
    1. Rimbara E, Fischbach LA, Graham DY. Optimal therapy for Helicobacter pylori infections. Nature Reviews Gastroenterology and Hepatology. 2011;8(2):79–88.
    1. Gisbert JP, Calvet X. Review article: rifabutin in the treatment of refractory Helicobacter pylori infection. Alimentary Pharmacology & Therapeutics. 2012;35(2):209–221.
    1. Treiber G, Ammon S, Malfertheiner P, Klotz U. Impact of furazolidone-based quadruple therapy for eradication of Helicobacter pylori after previous treatment failures. Helicobacter. 2002;7(4):225–231.
    1. Malfertheiner P, Megraud F, O’Morain CA, et al. Management of Helicobacter pylori infection—the Maastricht IV/ Florence Consensus Report. Gut. 2012;61(5):646–664.

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