Modern approaches to the eradication of Helicobacter pylori: a spectrum of perspectives

Abstract

Helicobacter pylori is one of the most widespread infections, affecting approximately 50% of the global population, with the Russian Federation ranking among the regions with a relatively high prevalence. Eradication therapy remains the primary strategy, not only for the treatment and prevention of gastrointestinal diseases but also for reducing the risk of stomach cancer, highlighting the medical and social impact of this infection. A key factor contributing to the reduced effectiveness of eradication therapy is the microorganism’s primary or secondary resistance to antibacterial drugs, a problem recognized worldwide. It is widely acknowledged that national treatment regimens for Helicobacter pylori infection must be adapted based on systematic antimicrobial sensitivity testing to curb the rise of global antibiotic resistance. Despite decades of research and clinical practice, identifying the most effective, safe, and straightforward therapy remains a significant challenge for clinicians.

This review provides a comparative analysis of current treatment recommendations for Helicobacter pylori infection, as presented by various national and regional gastroenterological societies, including those relevant in the Russian Federation.

Keywords

Helicobacter pylori / stomach cancer / eradication therapy / antibacterial drugs

References

[1] Hooi JKY, Lai WY, Ng WK, et al. Global Prevalence of Helicobacter pylori Infection: systematic review and meta-analysis. Gastroenterology. 2017;153(2):420–429. doi: 10.1053/j.gastro.2017.04.022

[2] Hooi J.K.Y., Lai W.Y., Ng W.K., et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis // Gastroenterology. 2017. Vol. 153. P. 420–429. doi: 10.1053/j.gastro.2017.04.022

[3] Bordin D, Morozov S, Plavnik R, et al. Helicobacter pylori infection prevalence in ambulatory settings in 2017-2019 in RUSSIA: The data of real-world national multicenter trial. Helicobacter. 2022;27(5):e12924. doi: 10.1111/hel.12924

[4] Bordin D., Morozov S., Plavnik R., et al. Helicobacter pylori infection prevalence in ambulatory settings in 2017–2019 in RUSSIA: The data of real-world national multicenter trial // Helicobacter. 2022. Vol. 27, N 5. Р. е12924. doi: 10.1111/hel.12924

[5] Zakcharova NV, Simanenkov VI, Bakulin IG, et al. Prevalence of Helicobacter pylori infection in gastroenterological patients in St. Petersburg. Farmateka. 2016;5:33–39. (In Russ.)

[6] Захарова Н.В., Симаненков В.И., Бакулин И.Г., и др. Распространенность хеликобактерной инфекции у пациентов гастроэнтерологического профиля в Санкт-Петербурге // Фарматека. 2016. № 5. С. 33–39.

[7] Bakulina NV, Simanenkov VI, Bakulin IG, Ilchishina TA. Рrevalence of Нelicobacter pylori infection among physicians. Experimental and Clinical Gastroenterology. 2017;(12):20–24. EDN: YOFUPS

[8] Бакулина Н.В., Симаненков В.И., Бакулин И.Г., Ильчишина Т.А. Распространенность хеликобактерной инфекции среди врачей // Экспериментальная и клиническая гастроэнтерология. 2017. № 12(148). С. 20–24. EDN: YOFUPS

[9] Ansari S, Yamaoka Y. Helicobacter pylori virulence factors exploiting gastric colonization and its pathogenicity. Toxins (Basel). 2019;11(11):677. doi: 10.3390/toxins11110677

[10] Ansari S., Yamaoka Y. Helicobacter pylori virulence factors exploiting gastric colonization and its pathogenicity // Toxins. 2019. Vol. 11, N 11. Р. 677. doi: 10.3390/toxins11110677

[11] Bordin D, Shengelia MI, Ivanova VA, Voynovan IN. Helicobacter pylori: clinical significance and diagnostic principles. Infectious diseases: News, Opinions, Training. 2022;11:119–129. EDN: AJNUYG doi: 10.33029/2305-3496-2022-11-1-119-129

[12] Бордин Д.С., Шенгелия М.И., Иванова В.А., Войнован И.Н. Helicobacter pylori: клиническое значение и принципы диагностики // Инфекционные болезни: новости, мнения, обучение. 2022. Т. 11, № 1. С. 119–129. EDN: AJNUYG doi: 10.33029/2305-3496-2022-11-1-119-129

[13] Venerito M, Schneider C, Costanzo R, et al. Contribution of Helicobacter pylori infection to the risk of peptic ulcer bleeding in patients on nonsteroidal anti-inflammatory drugs, antiplatelet agents, anticoagulants, corticosteroids and selective serotonin reuptake inhibitors. Aliment Pharmacol Ther. 2018;47(11):1464–1471. doi: 10.1111/apt.14652

[14] Venerito M., Schneider C., Costanzo R., et al. Contribution of Helicobacter pylori infection to the risk of peptic ulcer bleeding in patients on nonsteroidal anti-inflammatory drugs, antiplatelet agents, anticoagulants, corticosteroids and selective serotonin reuptake inhibitors // Aliment Pharmacol Ther. 2018. Vol. 47, N 11. Р. 1464–1471. doi: 10.1111/apt.14652

[15] Sugano K, Tack J, Kuipers EJ, et al. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64(9):1353–1367. doi: 10.1136/gutjnl-2015-309252

[16] Sugano K., Tack J., Kuipers E.J., et al. Kyoto global consensus report on Helicobacter pylori gastritis // Gut. 2015. Vol. 64, N 9. P. 1353–1367. doi: 10.1136/gutjnl-2015-309252

[17] GBD 2017 Stomach Cancer Collaborators. The global, regional, and national burden of stomach cancer in 195 countries, 1990-2017: a systematic analysis for the Global Burden of Disease study 2017 Lancet Gastroenterol Hepatol. 2020;5(1):42–54. doi: 10.1016/S2468-1253(19)30328-0. Published correction in: Lancet Gastroenterol Hepatol. 2020;5(3):e2. doi: 10.1016/S2468-1253(20)30020-0

[18] GBD 2017 Stomach Cancer Collaborators. The global, regional, and national burden of stomach cancer in 195 countries, 1990-2017: a systematic analysis for the Global Burden of Disease study 2017 // Lancet Gastroenterol Hepatol. 2020. Vol. 5, N 1. Р. 42–54. doi: 10.1016/S2468-1253(19)30328-0

[19] Voynovan IN, Embutnieks YuV, Mareeva DV, et al. Helicobacter pylori as a risk factor for gastric cancer: the evidence and primary prevention strategy. Almanac of Clinical Medicine. 2019;47(6):535–547. EDN: CQCARD doi: 10.18786/2072-0505-2019-47-052

[20] Войнован И.Н., Эмбутниекс Ю.В., Мареева Д.В., и др. H. pylori как фактор риска рака желудка: доказательная база и стратегия первичной профилактики // Альманах клинической медицины. 2019. Т. 47, № 6. С. 535–547. EDN: CQCARD doi: 10.18786/2072-0505-2019-47-052

[21] Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis. Gastric Cancer. 2019;22(3):435–445. doi: 10.1007/s10120-018-0876-0

[22] Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis // Gastric Cancer. 2019. Vol. 22, N 3. Р. 435–445. doi: 10.1007/s10120-018-0876-0

[23] Li WQ, Ma JL, Zhang L, et al. Effects of Helicobacter pylori treatment on gastric cancer incidence and mortality in subgroups. J Natl Cancer Inst. 2014;106(7):dju116. doi: 10.1093/jnci/dju116

[24] Li W.Q., Ma J.L., Zhang L., еt al. Effects of Helicobacter pylori treatment on gastric cancer incidence and mortality in subgroups // J Natl Cancer Inst. 2014. Vol. 106, N 7. P. 116. doi: 10.1093/jnci/dju116

[25] Pimentel-Nunes P, Libânio D, Marcos-Pinto R, et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy. 2019;51(4):365–388. doi: 10.1055/a-0859-1883

[26] Pimentel-Nunes P., Libânio D., Marcos-Pinto R., еt al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019 // Endoscopy. 2019. Vol. 51, N 4. Р. 365–388. doi: 10.1055/a-0859-1883

[27] Ivashkin VT, Mayev IV, Kaprin AD, et al. Early detection of oncological diseases of the digestive system (Guidelines of the Russian Gastroenterological Association and the Russian Association of Oncologists for Primary Care Physicians). Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2019;29(5):53–74. EDN: XYHWQO doi: 10.22416/1382-4376-2019-29-5-53-74

[28] Ивашкин В.Т., Маев И.В., Каприн А.Д., и др. Раннее выявление онкологических заболеваний органов пищеварения (методическое руководство Российской гастроэнтерологической ассоциации и Ассоциации онкологов России для врачей первичного звена здравоохранения) // Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2019. Т. 29, № 5. С. 53–74. EDN: XYHWQO doi: 10.22416/1382-4376-2019-29-5-53-74

[29] Nyssen OP, Bordin D, Tepes B, et al. Hp-EuReg Investigators. European Registry on Helicobacter pylori management (Hp-EuReg): patterns and trends in first-line empirical eradication prescription and outcomes of 5 years and 21 533 patients. Gut. 2021;70(1):40–54. doi: 10.1136/gutjnl-2020-321372

[30] Nyssen O.P., Bordin D., Tepes B., еt al. Hp-EuReg Investigators. European Registry on Helicobacter pylori management (Hp-EuReg): patterns and trends in first-line empirical eradication prescription and outcomes of 5 years and 21 533 patients // Gut. 2021. Vol. 70, N 1. Р. 40–54. doi: 10.1136/gutjnl-2020-321372

[31] Nyssen OP, Vaira D, Tepes B, et al. Room for Improvement in the Treatment of Helicobacter pylori Infection: Lessons from the European Registry on H. pylori Management (Hp-EuReg). J Clin Gastroenterol. 2022;56(2):e98–e108. doi: 10.1097/MCG.0000000000001482

[32] Nyssen O.P., Vaira D., Tepes B., еt al. Room for improvement in the treatment of Helicobacter pylori infection: lessons from the European Registry on H. pylori Management (Hp-EuReg) // J Clin Gastroenterol. 2022. Vol. 56, N 2. Р. e98–e108. doi: 10.1097/MCG.0000000000001482

[33] Bakulina NV, Maev IV, Savilova IV, et al. Efficacy of H. pylori eradication depending on genetic polymorphism of CYP2C19, MDR1 and IL-1β. Terapevticheskii arkhiv. 2019;91(8):34–40. EDN: MGABBW doi: 10.26442/00403660.2019.08.000380

[34] Бакулина Н.В., Маев И.В., Савилова И.В., и др. Эффективность эрадикации Helicobacter pylori в зависимости от генетического полиморфизма CYP2C19, MDR1 и IL-1β // Терапевтический архив. 2019. Т. 91, № 8. С. 34–40. EDN: MGABBW doi: 10.26442/00403660.2019.08.000380

[35] Li M, Gao N, Wang S, et al. Bibliometric analysis of Helicobacter pylori resistance-from 2002 to 2022. Helicobacter. 2023;28(4):e12983. doi: 10.1111/hel.12983

[36] Li M., Gao N., Wang S., et al. Bibliometric analysis of Helicobacter pylori resistance-from 2002 to 2022 // Helicobacter. 2023. Vol. 28, N 4. Р. e12983. doi: 10.1111/hel.12983

[37] Savoldi A, Carrara E, Graham DY, et al. Prevalence of antibiotic resistance in Helicobacter pylori: asystematic review and meta-analysis in World Health Organization Regions. Gastroenterology. 2018;155(5):1372–1382.e17. doi: 10.1053/j.gastro.2018.07.007

[38] Savoldi A., Carrara E., Graham D.Y., et al. Prevalence of antibiotic resistance in Helicobacter pylori: a systematic review and meta-analysis in World Health Organization Regions // Gastroenterology. 2018. Vol. 155, N 5. Р. 1372–1382.e17. doi: 10.1053/j.gastro.2018.07.007

[39] Andreev DN, Maev IV, Kucheryavyy YA. Helicobacter pylori resistance in the Russian federation: a meta-analysis of studies over the past 10 years. Terapevticheskii arkhiv. 2020;92(11):24–30. EDN: GSMIBF doi: 10.26442/00403660.2020.11.000795

[40] Андреев Д.Н., Маев И.В., Кучерявый Ю.А. Резистентность Helicobacter pylori в Российской Федерации: мета-анализ исследований за последние 10 лет // Терапевтический архив. 2020. Т. 92, № 11. С. 24–30. EDN: GSMIBF doi: 10.26442/00403660.2020.11.000795

[41] Ji YH, Shi YM, Hei QW, et al. Evaluation of guidelines for diagnosis and treatment of Helicobacter pylori infection. Helicobacter. 2023;28(1):e12937. doi: 10.1111/hel.12937

[42] Ji Y.H., Shi Y.M., Hei Q.W., еt al. Evaluation of guidelines for diagnosis and treatment of Helicobacter pylori infection // Helicobacter. 2023. Vol. 28, N 1. Р. e12937. doi: 10.1111/hel.12937

[43] Ivashkin VT, Lapina TL, Maev IV, et al. Clinical Practice Guidelines of Russian Gastroenterological Association, Scientific Society for the Clinical Study of Human Microbiome, Russian Society for the Prevention of Non-Communicable Diseases, Interregional Association for Clinical Microbiology and Antimicrobial Chemotherapy for H. pylori Diagnostics and Treatment in Adults. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2022;32(6):72–93. EDN: QRQFTQ doi: 10.22416/1382-4376-2022-32-6-72-93

[44] Ивашкин В.Т., Лапина Т.Л., Маев И.В., и др. Клинические рекомендации Российской гастроэнтерологической ассоциации, Научного сообщества по содействию клиническому изучению микробиома человека, Российского общества профилактики неинфекционных заболеваний, Межрегиональной ассоциации по клинической микробиологии и антимикробной химиотерапии по диагностике и лечению H. pylori у взрослых // Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2022. Т. 32, № 6. С. 72–93. EDN: QRQFTQ doi: 10.22416/1382-4376-2022-32-6-72-93

[45] Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection. Am J Gastroenterol. 2017;112(2):212–239. doi: 10.1038/ajg.2016.563

[46] Chey W.D., Leontiadis G.I., Howden C.W., Moss S.F. ACG Clinical Guideline: Treatment of Helicobacter pylori Infection // Am J Gastroenterol. 2017. Vol. 112, N 2. Р. 212–239. doi: 10.1038/ajg.2016.563

[47] Shah SC, Iyer PG, Moss SF. AGA Clinical Practice Update on the Management of Refractory Helicobacter pylori Infection: Expert Review. Gastroenterology. 2021;160(5):1831–1841. doi: 10.1053/j.gastro.2020.11.059

[48] Shah S.C., Iyer P.G., Moss S.F. AGA Clinical Practice Update on the Management of Refractory Helicobacter pylori Infection: Expert Review // Gastroenterology. 2021. Vol. 160, N 5. Р. 1831–1841. doi: 10.1053/j.gastro.2020.11.059

[49] Malfertheiner P, Megraud F, Rokkas T, et al. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report. Gut. 2022:gutjnl-2022-327745. doi: 10.1136/gutjnl-2022-327745

[50] Malfertheiner P., Megraud F., Rokkas T., еt al. European Helicobacter and Microbiota Study group. Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report // Gut. 2022. P. gutjnl-2022-327745. doi: 10.1136/gutjnl-2022-327745

[51] Ding SZ, Du YQ, Lu H, et al. Chinese Consensus Report on Family-Based Helicobacter pylori Infection Control and Management (2021 Edition). Gut. 2022;71(2):238–253. doi: 10.1136/gutjnl-2021-325630

[52] Ding S.Z., Du Y.Q., Lu H., еt al. Chinese Consensus Report on Family-Based Helicobacter pylori Infection Control and Management (2021 Edition) // Gut. 2022. Vol. 71, N 2. Р. 238–253. doi: 10.1136/gutjnl-2021-325630

[53] Kato M, Ota H, Okuda M, et al. Guidelines for the management of Helicobacter pylori infection in Japan: 2016 Revised Edition. Helicobacter. 2019;24(4):e12597. doi: 10.1111/hel.12597

[54] Kato M., Ota H., Okuda M., еt al. Guidelines for the management of Helicobacter pylori infection in Japan: 2016 Revised Edition // Helicobacter. 2019. Vol. 24, N 4. Р. e12597. doi: 10.1111/hel.12597

[55] Jung HK, Kang SJ, Lee YC, et al. Korean College of Helicobacter and Upper Gastrointestinal Research. Evidence-Based Guidelines for the Treatment of Helicobacter pylori Infection in Korea 2020. Gut Liver. 2021;15(2):168–195. doi: 10.5009/gnl20288

[56] Jung H.K., Kang S.J., Lee Y.C., еt al. Korean College of Helicobacter and Upper Gastrointestinal Research. Evidence-Based Guidelines for the Treatment of Helicobacter pylori Infection in Korea 2020 // Gut Liver. 2021. Vol. 15, N 2. Р. 168–195. doi: 10.5009/gnl20288

[57] Alsohaibani F, Peedikayil M, Alshahrani A, et al. Practice guidelines for the management of Helicobacter pylori infection: The Saudi H. pylori Working Group recommendations. Saudi J Gastroenterol. 2023;29(6):326–346. doi: 10.4103/sjg.sjg_288_22

[58] Alsohaibani F., Peedikayil M., Alshahrani A., et al. Practice guidelines for the management of Helicobacter pylori infection: The Saudi H. pylori Working Group recommendations // Saudi J Gastroenterol. 2023. Vol. 29, N 6. P. 326–346. doi: 10.4103/sjg.sjg_288_22

[59] Kasahun GG, Demoz GT, Desta DM. Primary resistance pattern of helicobacter pylor to antibiotics in adult population: a systematic review. Infect Drug Resist. 2020;13:1567–1573. doi: 10.2147/IDR.S250200

[60] Kasahun G.G., Demoz G.T., Desta D.M. Primary resistance pattern of Helicobacter pylori to antibiotics in adult population: a systematic review // Infect Drug Resist. 2020. Vol. 13. Р. 1567–1573. doi: 10.2147/IDR.S250200

[61] Hu Y, Zhu Y, Lu NH. Primary Antibiotic Resistance of Helicobacter pylori in China. Dig Dis Sci. 2017;62(5):1146–1154. doi: 10.1007/s10620-017-4536-8

[62] Hu Y., Zhu Y., Lu N.H. Primary antibiotic resistance of Helicobacter pylori in China // Dig Dis Sci. 2017. Vol. 62, N 5. Р. 1146–1154. doi: 10.1007/s10620-017-4536-8

[63] Lee JH, Ahn JY, Choi KD, et al. Korean College of Helicobacter; Upper Gastrointestinal Research. Nationwide antibiotic resistance mapping of Helicobacter pylori in Korea: A prospective multicenter study. Helicobacter. 2019;24(4):e12592. doi: 10.1111/hel.12592

[64] Lee J.H., Ahn J.Y., Choi K.D., et al. Korean College of Helicobacter; Upper Gastrointestinal Research. Nationwide antibiotic resistance mapping of Helicobacter pylori in Korea: A prospective multicenter study // Helicobacter. 2019. Vol. 24, N 4. Р. e12592. doi: 10.1111/hel.12592

[65] Shih CA, Shie CB, Hsu PI. Update on the first-line treatment of Helicobacter pylori infection in areas with high and low clarithromycin resistances. Ther Adv Gastroenterol. 2022;15:17562848221138168. doi: 10.1177/17562848221138168

[66] Shih C.A., Shie C.B., Hsu P.I. Update on the first-line treatment of Helicobacter pylori infection in areas with high and low clarithromycin resistances // Ther Adv Gastroenterol. 2022. Vol. 15. Р. 17562848221138168. doi: 10.1177/17562848221138168

[67] Ko SW, Kim Y-J, Chung WC, Lee SJ. Bismuth supplements as the first-line regimen for Helicobacter pylori eradication therapy: Systemic review and meta-analysis. Helicobacter. 2019;24(2):e12565. doi: 10.1111/hel.12565

[68] Ko S.W., Kim Y.-J., Chung W.C., Lee S.J. Bismuth supplements as the first-line regimen for Helicobacter pylori eradication therapy: Systemic review and meta-analysis // Helicobacter. 2019. Vol. 24, N 2. Р. e12565. doi: 10.1111/hel.12565

[69] McNicholl AG, Bordin DS, Lucendo A, et al. Combination of bismuth and standard triple therapy eradicates Helicobacter pylori infection in more than 90 % of patients. Clin Gastroenterol Hepatol. 2020;18(1):89–98. doi: 10.1016/j.cgh.2019.03.048

[70] McNicholl A.G., Bordin D.S., Lucendo A., et al. Combination of bismuth and standard triple therapy eradicates Helicobacter pylori infection in more than 90 % of patients // Clin Gastroenterol Hepatol. 2020. Vol. 18, N 1. Р. 89–98. doi: 10.1016/j.cgh.2019.03.048

[71] Han Z, Li Y, Kong Q, et al. Efficacy of bismuth for antibiotic-resistant Helicobacter pylori strains eradication: A systematic review and meta-analysis. Helicobacter. 2022;27(6):e12930. doi: 10.1111/hel.12930

[72] Han Z., Li Y., Kong Q., Liu J, et al. Efficacy of bismuth for antibiotic-resistant Helicobacter pylori strains eradication: A systematic review and meta-analysis // Helicobacter. 2022. Vol. 27, N 6. Р. e12930. doi: 10.1111/hel.12930

[73] Mori H, Suzuki H. Update on quinolone-containing rescue therapies for Helicobacter pylori infection. World J Gastroenterol. 2020;26(15):1733–1744. doi: 10.3748/wjg.v26.i15.1733

[74] Mori H., Suzuki H. Update on quinolone-containing rescue therapies for Helicobacter pylori infection // World J Gastroenterol. 2020. Vol. 26, N 15. Р. 1733–1744. doi: 10.3748/wjg.v26.i15.1733

[75] Cho JH, Jin SY. Current guidelines for Helicobacter pylori treatment in East Asia 2022: Differences among China, Japan, and South Korea. World J Clin Cases. 2022;10(19):6349–6359. doi: 10.12998/wjcc.v10.i19.6349

[76] Cho J.H., Jin S.Y. Current guidelines for Helicobacter pylori treatment in East Asia 2022: Differences among China, Japan, and South Korea // World J Clin Cases. 2022. Vol. 10, N 19. Р. 6349–6359. doi: 10.12998/wjcc.v10.i19.6349

RIGHTS & PERMISSIONS

Eco-Vector