Helicobacter pylori as a risk factor for gastric cancer: the evidence and primary prevention strategy

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Abstract

Russia is a country with a high prevalence of Helicobacter pylori (HP) infection, a high incidence of gastric cancer, and its late diagnosis. HР infection has been recognized as the leading manageable risk factor for gastric cancer. Accurate diagnostic tests must be used to identify and control the effectiveness of HP eradication, and effective schemes must be implemented for HP eradication. The aim of this article was to analyze the latest consensus documents, systematic reviews and meta-analyzes that reflected the role of HP as a risk factor for the development of gastric cancer, as well as measures for the risk reduction. We describe in detail the diagnostic methods for HP infection, provide data on their use in the Russian Federation, and analyze the efficacy of eradication regimens. In all HPinfected individuals, HP leads to chronic inflammation in the gastric mucosa and launches a precancerous cascade (Correa's cascade). The risk of gastric cancer increases with severe atrophy, intestinal metaplasia and dysplasia. Primary prevention of gastric cancer is most effective if the eradication is performed before atrophic gastritis develops. The available consensus documents underline the importance of HP infection identification by accurate diagnostics at this stage of chronic gastritis. In Russia, the primary HP diagnosis is based on histology (37.7%), rapid urease test (29.2%), and serology (29.7%). HP stool antigen test (31.3%), 13C-urea breath test (23.4%) and the histological method (23.3%) are most often used to control eradication. Currently, the first line of eradication therapy is recommended as triple therapy with clarithromycin prescribed for 14 days. It is recommended to use double dose of proton pump inhibitors and bismuth to increase the effectiveness of this scheme. A 14-days triple regimen enhanced by bismuth has been recommended as the first-line therapy in the Russian Federation.

About the authors

I. N. Voynovan

Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department

Email: i.voynovan@mknc.ru
ORCID iD: 0000-0002-5584-8514

Irina N. Voynovan – Junior Research Fellow, Division of Pathology of Upper Digestive Tract

86 Shosse Entuziastov, Moscow, 111123

Россия

Yu. V. Embutnieks

Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department

Email: y.embutnieks@mknc.ru
ORCID iD: 0000-0002-6479-9515

Yuliya V. Embutnieks – MD, PhD, Head of the Division of Pathology of Upper Digestive Tract

86 Shosse Entuziastov, Moscow, 111123

Россия

D. V. Mareeva

Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department

Email: dmareeva@mail.ru
ORCID iD: 0000-0002-4172-8482

Dariya V. Mareeva – MD, PhD, Gastroenterologist, Clinical and Diagnostic Department

86 Shosse Entuziastov, Moscow, 111123

Россия

S. V. Kolbasnikov

Tver State Medical University

Email: kabinet208@mail.ru
ORCID iD: 0000-0002-9223-0457

Sergey V. Kolbasnikov – MD, PhD, Professor, Head of the Chair of General Medical Practice (Family Medicine), Faculty of Postgraduate Studies

4 Sovetskaya ul., Tver, 170100

Россия

D. S. Bordin

Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department;
Tver State Medical University;
A.I. Yevdokimov Moscow State University of
Medicine and Dentistry

Author for correspondence.
Email: d.bordin@mknc.ru
ORCID iD: 0000-0003-2815-3992

Dmitry S. Bordin – MD, PhD, Head of Division of Pathology of the Pancreas, Biliary Tract and Upper Digestive Tract Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department; Professor of Chair of General Medical Practice (Family Medicine), Faculty of Postgraduate Studies Tver State Medical University; Professor of Chair of Internal Diseases Propedeutics and Gastroenterology A.I. Yevdokimov Moscow State University of Medicine and Dentistry

86 Shosse Entuziastov, Moscow, 111123

 

Россия

References

  1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6): 394–424. doi: 10.3322/caac.21492.
  2. Rawla P, Barsouk A. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz Gastroenterol. 2019;14(1): 26–38. doi: 10.5114/pg.2018.80001.
  3. Каприн АД, Старинский ВВ, Петрова ГВ, ред. Злокачественные новообразования в России в 2017 году (заболеваемость и смертность) [Интернет]. М.: МНИОИ им. П.А. Герцена – филиал ФГБУ «НМИЦ радиологии» Минздрава России; 2018. 250 с. Доступно на: http://www.oncology.ru/service/statistics/malignant_tumors/2017.pdf.
  4. Liou JM, Lee YC, El-Omar EM, Wu MS. Efficacy and Long-Term Safety of H. pylori Eradication for Gastric Cancer Prevention. Cancers (Basel). 2019;11(5). pii: E593. doi: 10.3390/cancers11050593.
  5. Karimi P, Islami F, Anandasabapathy S, Freedman ND, Kamangar F. Gastric cancer: descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Biomarkers Prev. 2014;23(5): 700–13. doi: 10.1158/1055-9965.EPI-13-1057.
  6. McLean MH, El-Omar EM. Genetics of gastric cancer. Nat Rev Gastroenterol Hepatol. 2014;11(11): 664–74. doi: 10.1038/nrgastro.2014.143.
  7. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017;153(2): 420–9. doi: 10.1053/j.gastro.2017.04.022.
  8. Nagy P, Johansson S, Molloy-Bland M. Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA. Gut Pathog. 2016;8:8. doi: 10.1186/s13099-016-0091-7.
  9. Graham DY. History of Helicobacter pylori, duodenal ulcer, gastric ulcer and gastric cancer. World J Gastroenterol. 2014;20(18): 5191–204. doi: 10.3748/wjg.v20.i18.5191.
  10. Plavnik R, Nevmerzhitskiy V, Embutniex Yu, Voynovan I, Kondrasheva E, Abdulova M, Bordin D. The prevalence of Helicobacter pylori in Russia. Helicobacter. 2018;23(S1): 24.
  11. Бордин ДС, Плавник РГ, Невмержицкий ВИ, Буторова ЛИ, Абдулхаков РА, Абдулхаков СР, Войнован ИН, Эмбутниекс ЮВ. Распространенность Helicobacter pylori среди медицинских работников Москвы и Казани по данным ¹³С-уреазного дыхательного теста. Альманах клинической медицины. 2018;46(1): 40–9. doi: 10.18786/2072-0505-2018-46-1-40-49.
  12. Бакулина НВ, Симаненков ВИ, Бакулин ИГ, Ильчишина ТА. Распространенность хеликобактерной инфекции среди врачей. Экспериментальная и клиническая гастроэнтерология. 2017;12(148): 20–4.
  13. Sugano K, Tack J, Kuipers EJ, Graham DY, El-Omar EM, Miura S, Haruma K, Asaka M, Uemura N, Malfertheiner P; faculty members of Kyoto Global Consensus Conference. Kyoto global consensus report on Helicobacter pylori gastritis. Gut. 2015;64(9): 1353–67. doi: 10.1136/gutjnl-2015-309252.
  14. Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, Hunt R, Moayyedi P, Rokkas T, Rugge M, Selgrad M, Suerbaum S, Sugano K, El-Omar EM; European Helicobacter and Microbiota Study Group and Consensus panel. Management of Helicobacter pylori infection – the Maastricht V/Florence Consensus Report. Gut. 2017;66(1): 6–30. doi: 10.1136/gutjnl-2016-312288.
  15. Hirayama Y, Kawai T, Otaki J, Kawakami K, Harada Y. Prevalence of Helicobacter pylori infection with healthy subjects in Japan. J Gastroenterol Hepatol. 2014;29 Suppl 4:16–9. doi: 10.1111/jgh.12795.
  16. Díaz P, Valenzuela Valderrama M, Bravo J, Quest AFG. Helicobacter pylori and Gastric Cancer: Adaptive Cellular Mechanisms Involved in Disease Progression. Front Microbiol. 2018;9:5. doi: 10.3389/fmicb.2018.00005.
  17. Cheung KS, Leung WK. Risk of gastric cancer development after eradication of Helicobacter pylori. World J Gastrointest Oncol. 2018;10(5): 115–23. doi: 10.4251/wjgo.v10.i5.115.
  18. Graham DY. Helicobacter pylori update: gastric cancer, reliable therapy, and possible benefits. Gastroenterology. 2015;148(4): 719–31.e3. doi: 10.1053/j.gastro.2015.01.040.
  19. Horridge DN, Begley AA, Kim J, Aravindan N, Fan K, Forsyth MH. Outer inflammatory protein a (OipA) of Helicobacter pylori is regulated by host cell contact and mediates CagA translocation and interleukin-8 response only in the presence of a functional cag pathogenicity island type IV secretion system. Pathog Dis. 2017;75(8). doi: 10.1093/femspd/ftx113.
  20. Xue H, Lin B, Ni P, Xu H, Huang G. Interleukin-1B and interleukin-1 RN polymorphisms and gastric carcinoma risk: a meta-analysis. J Gastroenterol Hepatol. 2010;25(10): 1604–17. doi: 10.1111/j.1440-1746.2010.06428.x.
  21. Song H, Ekheden IG, Zheng Z, Ericsson J, Nyrén O, Ye W. Incidence of gastric cancer among patients with gastric precancerous lesions: observational cohort study in a low risk Western population. BMJ. 2015;351:h3867. doi: 10.1136/bmj.h3867.
  22. Sugano K. Effect of Helicobacter pylori eradication on the incidence of gastric cancer: a systematic review and meta-analysis. Gastric Cancer. 2019;22(3): 435–45. doi: 10.1007/s10120-018-0876-0.
  23. Chen HN, Wang Z, Li X, Zhou ZG. Helicobacter pylori eradication cannot reduce the risk of gastric cancer in patients with intestinal metaplasia and dysplasia: evidence from a meta-analysis. Gastric Cancer. 2016;19(1): 166–75. doi: 10.1007/s10120-015-0462-7.
  24. Wang J, Xu L, Shi R, Huang X, Li SW, Huang Z, Zhang G. Gastric atrophy and intestinal metaplasia before and after Helicobacter pylori eradication: a meta-analysis. Digestion. 2011;83(4): 253–60. doi: 10.1159/000280318.
  25. Li WQ, Ma JL, Zhang L, Brown LM, Li JY, Shen L, Pan KF, Liu WD, Hu Y, Han ZX, Crystal-Mansour S, Pee D, Blot WJ, Fraumeni JF Jr, You WC, Gail MH. Effects of Helicobacter pylori treatment on gastric cancer incidence and mortality in subgroups. J Natl Cancer Inst. 2014;106(7). pii: dju116. doi: 10.1093/jnci/dju116.
  26. Yoon SB, Park JM, Lim CH, Cho YK, Choi MG. Effect of Helicobacter pylori eradication on metachronous gastric cancer after endoscopic resection of gastric tumors: a meta-analysis. Helicobacter. 2014;19(4): 243–8. doi: 10.1111/hel.12146.
  27. Choi IJ, Kook MC, Kim YI, Cho SJ, Lee JY, Kim CG, Park B, Nam BH. Helicobacter pylori Therapy for the Prevention of Metachronous Gastric Cancer. N Engl J Med. 2018;378(12): 1085–95. doi: 10.1056/NEJMoa1708423.
  28. Rugge M, Correa P, Di Mario F, El-Omar E, Fiocca R, Geboes K, Genta RM, Graham DY, Hattori T, Malfertheiner P, Nakajima S, Sipponen P, Sung J, Weinstein W, Vieth M. OLGA staging for gastritis: a tutorial. Dig Liver Dis. 2008;40(8): 650–8. doi: 10.1016/j.dld.2008.02.030.
  29. Бордин ДС, Машарова АА, Хомерики СГ. Хронический гастрит: современный взгляд на старую проблему. Экспериментальная и клиническая гастроэнтерология. 2012;(5): 99–106.
  30. Yue H, Shan L, Bin L. The significance of OLGA and OLGIM staging systems in the risk assessment of gastric cancer: a systematic review and meta-analysis. Gastric Cancer. 2018;21(4): 579–87. doi: 10.1007/s10120-018-0812-3.
  31. Бордин ДС, Бяхов МЮ, Федуленкова ЛВ. «Серологическая биопсия» и скрининг рака желудка. Злокачественные опухоли. 2014;2(9): 30–6.
  32. Pimentel-Nunes P, Libânio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, Garrido M, Kikuste I, Megraud F, Matysiak-Budnik T, Annibale B, Dumonceau JM, Barros R, Fléjou JF, Carneiro F, van Hooft JE, Kuipers EJ, Dinis-Ribeiro M. 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): 365–88. doi: 10.1055/a-0859-1883.
  33. Бордин ДС, Войнован ИН, Колбасников СВ, Эмбутниекс ЮВ. Методы диагностики инфекции Helicobacter pylori в клинической практике. Терапевтический архив. 2018;90(12): 133–9. doi: 10.26442/00403660.2018.12.000020.
  34. Moayyedi P, Lacy BE, Andrews CN, Enns RA, Howden CW, Vakil N. ACG and CAG Clinical Guideline: Management of Dyspepsia. Am J Gastroenterol. 2017;112(7): 988–1013. doi: 10.1038/ajg.2017.154.
  35. Mukaisho K, Nakayama T, Hagiwara T, Hattori T, Sugihara H. Two distinct etiologies of gastric cardia adenocarcinoma: interactions among pH, Helicobacter pylori, and bile acids. Front Microbiol. 2015;6:412. doi: 10.3389/fmicb.2015.00412.
  36. Kayali S, Aloe R, Bonaguri C, Gaiani F, Manfredi M, Leandro G, Fornaroli F, Di Mario F, De' Angelis GL. Non-invasive tests for the diagnosis of helicobacter pylori: state of the art. Acta Biomed. 2018;89(8 Suppl):58–64. doi: 10.23750/abm.v89i8-S.7910.
  37. Lee YC, Tseng PH, Liou JM, Chen MJ, Chen CC, Tu CH, Chiang TH, Chiu HM, Lai CF, Ho JC, Wu MS. Performance of a one-step fecal sample-based test for diagnosis of Helicobacter pylori infection in primary care and mass screening settings. J Formos Med Assoc. 2014;113(12): 899–907. doi: 10.1016/j.jfma.2012.05.014.
  38. Lee JY, Kim N. Diagnosis of Helicobacter pylori by invasive test: histology. Ann Transl Med. 2015;3(1): 10. doi: 10.3978/j.issn.2305-5839.2014.11.03.
  39. Lan HC, Chen TS, Li AF, Chang FY, Lin HC. Additional corpus biopsy enhances the detection of Helicobacter pylori infection in a background of gastritis with atrophy. BMC Gastroenterol. 2012;12:182. doi: 10.1186/1471-230X-12-182.
  40. Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SS, Wu JY, Kuo CH, Huang YK, Wu DC. Diagnosis of Helicobacter pylori infection: Current options and developments. World J Gastroenterol. 2015;21(40): 11221–35. doi: 10.3748/wjg.v21.i40.11221.
  41. Graham DY, Miftahussurur M. Helicobacter pylori urease for diagnosis of Helicobacter pylori infection: A mini review. J Adv Res. 2018;13:51–7. doi: 10.1016/j.jare.2018.01.006.
  42. Ferwana M, Abdulmajeed I, Alhajiahmed A, Madani W, Firwana B, Hasan R, Altayar O, Limburg PJ, Murad MH, Knawy B. Accuracy of urea breath test in Helicobacter pylori infection: meta-analysis. World J Gastroenterol. 2015;21(4): 1305–14. doi: 10.3748/wjg.v21.i4.1305.
  43. Tian XY, Zhu H, Zhao J, She Q, Zhang GX. Diagnostic performance of urea breath test, rapid urea test, and histology for Helicobacter pylori infection in patients with partial gastrectomy: a meta-analysis. J Clin Gastroenterol. 2012;46(4): 285–92. doi: 10.1097/MCG.0b013e318249c4cd.
  44. Leal YA, Flores LL, Fuentes-Pananá EM, Cedillo-Rivera R, Torres J. 13C-urea breath test for the diagnosis of Helicobacter pylori infection in children: a systematic review and meta-analysis. Helicobacter. 2011;16(4): 327–37. doi: 10.1111/j.1523-5378.2011.00863.x.
  45. Leal YA, Cedillo-Rivera R, Simón JA, Velázquez JR, Flores LL, Torres J. Utility of stool sample-based tests for the diagnosis of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr. 2011;52(6): 718–28. doi: 10.1097/MPG.0b013e3182077d33.
  46. Kuloğlu Z, Kansu A, Kirsaçlioğlu CT, Ustündağ G, Aysev D, Ensari A, Küçük NO, Girgin N. A rapid lateral flow stool antigen immunoassay and (14)C-urea breath test for the diagnosis and eradication of Helicobacter pylori infection in children. Diagn Microbiol Infect Dis. 2008;62(4): 351–6. doi: 10.1016/j.diagmicrobio.2008.07.006.
  47. Маев ИВ, Сайфутдинов РГ, Самсонов АА, Гречушников ВБ. Результаты открытого мультицентрового исследования эффективности дыхательных тестов в диагностике H. pylori. Дневник казанской медицинской школы. 2013;(5): 21–3.
  48. Агеева ЕА, Харитонова ТИ, Гуляко ЛФ, Зайнулина ЗУ, Васильева АВ, Воробьева ВА, Никитин ОН. Диагностические возможности уреазного дыхательного (Хелик) теста в оценке эрадикации Helicobacter pylori-инфекции. Дальневосточный медицинский журнал. 2010;(4): 12–5.
  49. McNicholl AG, Bordin DS, Lucendo A, Fadeenko G, Fernandez MC, Voynovan I, Zakharova NV, Sarsenbaeva AS, Bujanda L, Perez-Aisa Á, Vologzhanina L, Zaytsev O, Ilchishina T, Coba C, Lasala JP, Alekseenko S, Modolell I, Molina-Infante J, Ruiz-Zorrilla Lopez R, Alonso-Galan H, Moreno NF, Hinojosa J, Santaella I, Varela P, Gonzalez-Cordero PL, Barrio J, Dominguez-Jimenez JL, Nuñez O, Alcedo J, Nyssen OP, Caldas M, Donday MG, Shvetz O, Megraud F, O'Morain C, Gisbert JP. Combination of Bismuth and Standard Triple Therapy Eradicates Helicobacter pylori Infection in More than 90% of Patients. Clin Gastroenterol Hepatol. 2019 Apr 10. pii: S1542-3565(19)30369-6. doi: 10.1016/j.cgh.2019.03.048. [Epub ahead of print].
  50. Бордин ДС, Эмбутниекс ЮВ, Вологжанина ЛГ, Ильчишина ТА, Войнован ИН, Сарсенбаева АС, Алексеенко СА, Зайцев ОВ, Абдулхаков РА, Осипенко МФ, Ливзан МА, Цуканов ВВ, Бурков СГ, Бакулина НВ, Дехнич НН, Тарасова ЛВ, Плотникова ЕЮ, Маев ИВ, Кучерявый ЮА, Барышникова НВ, Бутов МА, Колбасников СВ, Пахомова АЛ, Жесткова ТВ, Барановский АЮ, Абдулхаков СР, Агеева ЕА, Лялюкова ЕА, Васютин АВ, Голубев НН, Савилова ИН, Морковкина ЛВ, Кононова АГ, Megraud F, O'morain C, Ramas M, Nyssen OP, McNicholl AG, Gisbert JP. Анализ данных 2360 больных, получавших терапию первой линии в России. Терапевтический архив. 2018;90(2): 35–42. doi: 10.26442/terarkh201890235-42.
  51. Лазебник ЛБ, Бордин ДС. Диагностика и лечение заболеваний, ассоциированных с Helicobacter pylori, в условиях реальной клинической практики: результаты наблюдательной программы «ПАРАД». Вестник практического врача. 2014;3(3): 31–42.
  52. Бордин ДС, Эмбутниекс ЮВ, Вологжанина ЛГ, Ильчишина ТА, Войнован ИН, Сарсенбаева АС, Зайцев ОВ, Алексеенко СА, Абдулхаков РА, Дехнич НН, Осипенко МФ, Ливзан МА, Цуканов ВВ, Бурков СГ, Бакулина НВ, Плотникова ЕЮ, Тарасова ЛВ, Маев ИВ, Кучерявый ЮА, Барышникова НВ, Бутов МА, Колбасников СВ, Пахомова АЛ, Жесткова ТВ, Барановский АЮ, Абдулхаков СР, Агеева ЕА, Лялюкова ЕА, Васютин АВ, Голубев НН, Савилова ИВ, Морковкина ЛВ, Кононова АГ, Megraud F, O'Morain C, Ramas M, Nyssen OP, McNicholl AG, Gisbert JP. Европейский регистр Helicobacter pylori (Hp-EuReg): как изменилась клиническая практика в России с 2013 по 2018 г. Терапевтический архив. 2019;91(2): 16–24. doi: 10.26442/00403660.2019.02.000156.
  53. Graham DY, Lee YC, Wu MS. Rational Helicobacter pylori therapy: evidence-based medicine rather than medicine-based evidence. Clin Gastroenterol Hepatol. 2014;12(2): 177–86.e3; discussion e12–3. doi: 10.1016/j.cgh.2013.05.028.
  54. Лазебник ЛБ, Ткаченко ЕИ, Абдулганиева ДИ, Абдулхаков РА, Абдулхаков СР, Авалуева ЕБ, Ардатская МД, Ахмедов ВА, Бордин ДС, Бурков СГ, Бутов МА, Голованова ЕВ, Голофеевский ВЮ, Гриневич ВБ, Джулай ГС, Добрица ВП, Еремина ЕЮ, Жигалова ТН, Иваников ИО, Исаков ВА, Казюлин АН, Калинин АВ, Козлова ИВ, Комиссаренко ИА, Корниенко ЕА, Корочанская НВ, Курилович СА, Кучерявый ЮА, Ли ЕД, Ли ИА, Левченко СВ, Ливзан МА, Логинов АФ, Лоранская ИД, Маев ИВ, Максимов ВА, Миллер ДА, Минушкин ОН, Низов АА, Орешко ЛС, Осипенко МФ, Пальцев АИ, Пасечников ВД, Радченко ВГ, Рустамов МН, Саблин ОА, Сагынбаева ВЭ, Сайфутдинов РГ, Самсонов АА, Сарсенбаева АС, Селиверстов ПВ, Симаненков ВИ, Ситкин СИ, Старостин БД, Суворов АН, Тарасова ЛВ, Ткачев АВ, Успенский ЮП, Хлынова ОВ, Хомерики НМ, Хомерики СГ, Цуканов ВВ, Чернин ВВ, Чернышев АЛ, Шархун ОО, Щербаков ПЛ, Яковенко ЭП. VI национальные рекомендации по диагностике и лечению кислотозависимых и ассоциированных с Helicobacter pylori заболеваний (VI Московские соглашения). Экспериментальная и клиническая гастроэнтерология. 2017;2(138): 3–21.
  55. Бордин ДС, Янова ОБ, Войнован ИН, Шапошникова НА, Оробей ЮА, Березина ОИ, Ковалева ОИ, Калашникова НГ, Дубцова ЕА. Эффективность и безопасность тройной антихеликобактерной терапии с добавлением висмута: кларитромицин vs джозамицин. Эффективная фармакотерапия. 2015;(51): 6–10.
  56. Маев ИВ, Самсонов АА, Коровина ТИ, Гречушников ВБ, Андреев НГ. Висмута трикалия дицитрат повышает эффективность антихеликобактерной терапии первой линии. Экспериментальная и клиническая гастроэнтерология. 2012;(8): 92–7.
  57. Sun Q, Liang X, Zheng Q, Liu W, Xiao S, Gu W, Lu H. High efficacy of 14-day triple therapy-based, bismuth-containing quadruple therapy for initial Helicobacter pylori eradication. Helicobacter. 2010;15(3): 233–8. doi: 10.1111/j.1523-5378.2010.00758.x.
  58. Zhang W, Chen Q, Liang X, Liu W, Xiao S, Graham DY, Lu H. Bismuth, lansoprazole, amoxicillin and metronidazole or clarithromycin as first-line Helicobacter pylori therapy. Gut. 2015;64(11): 1715–20. doi: 10.1136/gutjnl-2015-309900.
  59. Plavnik R, Nevmerzhitskiy V, Embutniex Yu, Voynovan I, Kondrasheva E, Abdulova M, Bordin D. The effectiveness of eradication therapy in Russia. Helicobacter. 2018;23(S1): 37–8.

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