Helicobacter pylori: clinical significance and diagnostic principles


Helicobacter pylori is one of the most significant human pathogens. H. pylori causes chronic gastritis in all infected individuals, which can lead to peptic ulcer disease, atrophic gastritis, gastric adenocarcinoma, or gastric MALT lymphoma. Eradication of H. pylori leads to the cure of gastritis, which is the basis for the prevention of the development or recurrence of these diseases. For the primary diagnosis of H. pylori, non-invasive methods are preferred - 13C-urease breath test and stool H. pylori antigen test. Recent studies have demonstrated the ability of artificial intelligence to predict H. pylori status with high accuracy based on endoscopic images. The article presents the main factors of H. pylori virulence and their role in the pathogenic mechanism. The review presents modern methods for the diagnosis of H. pylori, their advantages and disadvantages in various clinical situations.

Keywords:Helicobacter pylori; virulence factors; CagA; gastric cancer; diagnostic methods; artificial intelligence; 13C-urease breath test

Funding. The work was done without sponsorship.

Conflict of interest. The author declares that they have no conflicts of interest.

Contribution. All authors made an equivalent contribution to the preparation of the article materials.

For citation: Bordin D.S., Shengelia M.I., Ivanova V.A., Voynovan I.N. Helicobacter pylori: clinical significance and diagnostic principles. Infektsionnye bolezni: novosti, mneniya, obuchenie [Infectious Diseases: News, Opinions, Training]. 2022; 11 (1): 119-29. DOI: https://doi.org/10.33029/2305-3496-2022-11-1-119-129


1. Hooi J.K.Y., Lai W.Y., Ng W.K., Suen M.M.Y., et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017; 153: 420–9. DOI: https://doi.org/10.1053/j.gastro.2017.04.022

2. Graham D.Y. History of Helicobacter pylori, duodenal ulcer, gastric ulcer and gastric cancer. World J Gastroenterol. 2014; 20: 5191–204. DOI: https://doi.org/10.3748/wjg.v20.i18.5191

3. Plavnik R., Nevmerzhitskiy V., Embutniex Yu., Voynovan I., et al. The prevalence of Helicobacter pylori in Russia. Helicobacter. 2018; 23 (1): 24.

4. Bordin D.S., Plavnik R.G., Nevmerzhitskiy V.I., Butorova L.I., et al. Prevalence of Helicobacter pylori among medical workers in Moscow and Kazan according to the 13C-urease breath test. Al'manakh klinicheskoy meditsiny [Almanac of Clinical Medicine]. 2018; 46 (1): 40–9. DOI: https://doi.org/10.18786/2072-0505-2018-46-1-40-49 (in Russian)

5. Bakulina N.V., Simanenkov V.I., Bakulin I.G., Ilchishina T.A. The prevalence of H. pylori infection among doctors. Eksperimental'naya i klinicheskaya gastroenterologiya [Experimental and Clinical Gastroenterology]. 2017; 12 (148): 20–4. (in Russian)

6. Malfertheiner P., Megraud F., O'Morain C.A. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut. 2017; 66 (1): 630. DOI: https://doi.org/10.1136/gutjnl-2016-312288

7. Simanenkov V.I., Mayev I.V., Tkacheva O.N., Alekseenko S.A., et al. Syndrome of increased epithelial permeability in clinical practice. Multidisciplinary National Consensus. Kardiovaskulyarnaya terapiya i profilaktika [Cardiovascular Therapy and Prevention]. 2021; 20 (1): 2758. DOI: https://doi.org/10.15829/1728-8800-2021-2758 (in Russian)

8. Khomeriki S.G. Helicobacter pylori inducer and effector of oxidative stress in the gastric mucosa: traditional concepts and new data. Eksperimental'naya i klinicheskaya gastroenterologiya [Experimental and Clinical Gastroenterology]. 2006; (1): 3746. PMID: 16866245. (in Russian)

9. Shiota S., Suzuki R., Yamaoka Y. The significance of virulence factors in Helicobacter pylori. J Dig Dis. 2013; 14 (3): 341–9. DOI: https://doi.org/10.1111/1751-2980.12054

10. Ansari S., Yamaoka Y. Helicobacter pylori Virulence Factors Exploiting Gastric Colonization and its Pathogenicity. Toxins. 2019; 11 (11): 677. DOI: https://doi.org/10.3390/toxins11110677

11. Novikov V.V., Lapin V.A., Melent'ev D.A., Mokhonova E.V. Features of the human immune response to Helicobacter pylori infection. Zhurnal MediAl' [Journal of MediAl]. 2019; 2: 55–69. DOI: https://doi.org/10.21145/2225-0026-2019-2-55-69 (in Russian)

12. Nagashima H., Iwatani S., Cruz M., Jiménez Abreu J.A. Toll-like receptor 10 in Helicobacter pylori infection. J Infect Dis. 2015; 212 (10): 1666–76. DOI: https://doi.org/10.1093/infdis/jiv270

13. Crabtree J.E., Shallcross T.M., Heatley R.V., Wyatt J.I. Mucosal tumour necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut. 1991; 32: 1473–7. DOI: https://doi.org/10.1136/gut.32.12.1473

14. Peng C., Ouyang Y., Lu N., Li N. The NF-κB signaling pathway, the microbiota, and gastrointestinal tumorigenesis: recent advances. Front Immunol. 2020; 11: 1387. DOI: https://doi.org/10.3389/fimmu.2020.01387

15. Diaconu S., Predescu A., Moldoveanu A., Pop C.S., Fierbințeanu-Braticevici C. Helicobacter pylori infection: old and new. J Med Life. 2017; 10 (2): 112–7.

16. Rawla P., Barsouk A. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz Gastroenterol. 2019; 14 (1): 26–38. DOI: https://doi.org/10.5114/pg.2018.80001

17. Voynovan I.N., Embutnieks Yu.V., Mareeva D.V., Kolbasnikov S.V., Bordin D.S.H. pylori as a risk factor for stomach cancer: evidence base and primary prevention strategy. Al'manakh klinicheskoy meditsiny [Almanac of Clinical Medicine]. 2019; 47 (6): 53547. DOI: https://doi.org/10.18786/2072-0505-2019-47-052 (in Russian)

18. Bordin D.S., Voynovan I.N., Kolbasnikov S.V., Embutnieks Yu.V. Methods for diagnosing Helicobacter pylori infection in clinical practice. Terapevticheskii arkhiv [Therapeutic Archive]. 2018; 90 (12): 1339. DOI: https://doi.org/10.26442/00403660.2018.12.000020 (in Russian)

19. Wang Y.K., Kuo F.C., Liu C.J., et al. Diagnosis of Helicobacter pylori infection: Current options and developments. World J Gastroenterol. 2015; 21 (40): 11221–35. DOI: https://doi.org/10.3748/wjg.v21.i40.11221

20. Patel S.K., Pratap C.B., Jain A.K., Gulati A.K., Nath G. Diagnosis of Helicobacter pylori: what should be the gold standard? World J Gastroenterol. 2014; 20: 12847–59. DOI: https://doi.org/10.3748/wjg.v20.i36.12847

21. Lee J.Y., Kim N. Diagnosis of Helicobacter pylori by invasive test: histology. Ann Transl Med. 2015; 3 (1): 10. DOI: https://doi.org/10.3978/j.issn.2305-5839.2014.11.03

22. Lopes A.I., Vale F.F., Oleastro M. Helicobacter pylori infection – recent developments in diagnosis. World J Gastroenterol. 2014; 20 (28): 9299–313. DOI: https://doi.org/10.3748/wjg.v20.i28.9299

23. Tian X.Y., Zhu H., Zhao J., She Q., Zhang G.X. 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: https://doi.org/10.1097/MCG.0b013e318249c4cd

24. Tonkic A., Vukovic J., Vrebalov Cindro P., Pesutic Pisac V., Tonkic M. Diagnosis of Helicobacter pylori infection: A short review. Wien Klin Wochenschr. 2018; 130 (17-18): 530–534. DOI: https://doi.org/10.1007/s00508-018-1356-6

25. Benoit A., Hoyeau N., Fléjou J.F. Diagnosis of Helicobacter pylori infection on gastric biopsies: standard stain, special stain or immunohistochemistry? Ann Pathol. 2018; 38 (6): 363–9. DOI: https://doi.org/10.1016/j.annpat.2018.03.009

26. Makristathis A., Hirschl A.M., Mégraud F., Bessède E. Review: diagnosis of Helicobacter pylori infection. Helicobacter. 2019; 24 (1): e12641. DOI: https://doi.org/10.1111/hel.12641

27. Vaira D., Vakil N., Gatta L., Ricci C., et al. Accuracy of a new ultrafast rapid urease test to diagnose Helicobacter pylori infection in 1000 consecutive dyspeptic patients. Aliment Pharmacol Ther. 2010; 31: 331–8. DOI: https://doi.org/10.1111/j.1365-2036.2009.04196.x

28. Pohl D., Keller P.M., Bordier V., Wagner K. Review of current diagnostic methods and advances in Helicobacter pylori diagnostics in the era of next generation sequencing. World J Gastroenterol. 2019; 25 (32): 4629–60. DOI: https://doi.org/10.3748/wjg.v25.i32.4629

29. Leszczyńska K., Namiot A., Namiot Z. et al. Patient factors affecting culture of Helicobacter pylori isolated from gastric mucosal specimens. Adv Med Sci. 2010; 55: 161–6. DOI: https://doi.org/10.2478/v10039-010-0028-1

30. Nakashima H., Kawahira H., Kawachi H., Sakaki N. Artificial intelligence diagnosis of Helicobacter pylori infection using blue laser imaging-bright and linked color imaging: a single-center prospective study. Ann Gastroenterol. 2018; 31 (4): 462–8. DOI: https://doi.org/10.20524/aog.2018.0269

31. Dohi O., Yagi N., Onozawa Y., et al. Linked color imaging improves endoscopic diagnosis of active Helicobacter pylori infection. Endosc Int Open. 2016; 4 (7): E800–5. DOI: https://doi.org/10.1055/s-0042-109049

32. Tahara T., Shibata T., Nakamura M., Yoshioka D., et al. Gastric mucosal pattern by using magnifying narrow-band imaging endoscopy clearly distinguishes histological and serological severity of chronic gastritis. Gastrointest Endosc. 2009; 70 (2): 246–53. DOI: https://doi.org/10.1016/j.gie.2008.11.046

33. Bessède E., Arantes V., Mégraud F., Coelho L.G. Diagnosis of Helicobacter pylori infection. Helicobacter. 2017; 22 (1). DOI: https://doi.org/10.1111/hel.12404

34. Sakhibgareeva M.V., Zaozersky A.Yu. Developing an artificial intelligence-based system for medical prediction. Vestnik Rossiyskogo gosudarstvennogo meditsinskogo universiteta [Bulletin of Russian State Medical University]. 2017; 6: 40–4. DOI: https://doi.org/10.24075/brsmu.2017-06-07 (in Russian)

35. Bang C.S., Lee J.J., Baik G.H. Artificial intelligence for the prediction of Helicobacter pylori infection in endoscopic images: systematic review and meta-analysis of diagnostic test accuracy. J Med Internet Res. 2020; 22 (9): e21983. DOI: https://doi.org/10.2196/21983

36. Leal Y.A., Flores L.L., Fuentes-Pananá E.M., 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: https://doi.org/10.1111/j.1523-5378.2011.00863.x

37. Peng N.J., Lai K.H., Liu R.S., Lee S.C., et al. Clinical significance of oral urease in diagnosis of Helicobacter pylori infection by [13C]urea breath test. Dig Dis Sci. 2001; 46 (8): 1772–8.

38. Dalla Nora M., Hörner R., De Carli D.M., Rocha M.P., et al. Is the immunocromatographic fecal antigen test effective for primary diagnosis of Helicobacter pylori infection in dyspeptic patients? Arq Gastroenterol. 2016; 53 (4): 224–7. DOI: https://doi.org/10.1590/S0004-28032016000400003

39. Godbole G., Mégraud F., Bessède E. Review: diagnosis of Helicobacter pylori infection. Helicobacter. 2020; 25, Suppl 1: e12735. DOI: https://doi.org/10.1111/hel.12735

40. Zhou X., Su J., Xu G., Zhang G. Accuracy of stool antigen test for the diagnosis of Helicobacter pylori infection in children: a meta-analysis. Clin Res Hepatol Gastroenterol. 2014; 38: 629–38. DOI: https://doi.org/10.1016/j.clinre.2014.02.001

41. Yan J., Yamaguchi T., Odaka T., Suzuki T., et al. Stool antigen test is a reliable method to detect Helicobacter pylori in the gastric remnant after distal gastrectomy for gastric cancer. J Clin Gastroenterol. 2010; 44: 73–4. DOI: https://doi.org/10.1097/MCG.0b013e3181aae65e

42. El-Shabrawi M., El-Aziz N.A., El-Adly T.Z., Hassanin F., et al. Stool antigen detection versus 13C-urea breath test for non-invasive diagnosis of pediatric Helicobacter pylori infection in a limited resource setting. Arch Med Sci. 2018; 14 (1): 69–73. DOI: https://doi.org/10.5114/aoms.2016.61031

43. Best L.M., Takwoingi Y., Siddique S., Selladurai A., et al. Non-invasive diagnostic tests for Helicobacter pylori infection. Cochrane Database Syst Rev. 2018; 3 (3): CD012080. DOI: https://doi.org/10.1002/14651858.CD012080.pub2

44. Kayali S., Aloe R., Bonaguri C., Gaiani F., et al. Non-invasive tests for the diagnosis of helicobacter pylori: state of the art. Acta Biomed. 2018; 89 (8-S): 5864. DOI: https://doi.org/10.23750/abm.v89i8-S.7910

45. Szymczak A., Ferenc S., Majewska J., Miernikiewicz P., et al. Application of 16S rRNA gene sequencing in Helicobacter pylori detection. PeerJ. 2020; 8: e9099. DOI: https://doi.org/10.7717/peerj.9099

46. Nezami B.G, Jani M., Alouani D., Rhoads D.D., Sadri N. Helicobacter pylori mutations detected by next-generation sequencing in formalin-fixed, paraffin-embedded gastric biopsy specimens are associated with treatment failure. J Clin Microbiol. 2019; 57 (7): e01834–18. DOI: https://doi.org/10.1128/JCM.01834-18

47. Khadangi F., Yassi M., Kerachian M.A. Review: diagnostic accuracy of PCR-based detection tests for Helicobacter Pylori in stool samples. Helicobacter. 2017; 22 (6). DOI: https://doi.org/10.1111/hel.12444

48. McNicholl A.G., O'Morain C.A., Megraud F., Gisbert J.P. As Scientific Committee of the HpEureg on Behalf of the National Coordinators Protocol of the European Registry on the management of Helicobacter pylori infection (Hp-EuReg). Helicobacter. 2019; 24 (5). DOI: https://doi.org/10.1111/hel.12630

49. Bordin D.S., Embutnieks Yu.V., Vologzhanina L.G., Ilchishina T.A., et al. European register of Helicobacter pylori (HP-EUREG): how clinical practice has changed in Russia from 2013 to 2018. Terapevticheskii arkhiv [Therapeutic Archive]. 2019; 91 (2): 16–24. DOI: https://doi.org/10.26442/00403660.2019.02.000156 (in Russian)

50. Nyssen O.P., Vaira D., Tepes B., Kupcinskas L., Bordin D., Pérez-Aisa Á., 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. 2021. Publish Ahead of Print. DOI: https://doi.org/10.1097/MCG.0000000000001482

Yushchuk Nikolay Dmitrievich
Academician of the Russian Academy of Sciences, Professor, head of the Infectious Diseases and Epidemiology Department, President of the Moscow State University of Medicine and Dentistry named after A.I. Evdokimov, Board member of the National Scientific Infectiologists? Society.
Medicine today

II Всероссийская конференция с международным участием "Воспаление глаза" 12 ноября 2022 года, Москва Воспалительные заболевания глаза - широко распространенная и многогранная проблема, с которой может столкнуться в своей практике любой специалист. Найти оптимальные алгоритмы...

Масштабное событие в области дерматовенерологии и косметологии - II конференция InteDeCo 2022 "Интегративная дерматовенерология и косметология. Новые стандарты взаимодействия" - состоится 16-17 декабря 2022 года. Программа мероприятия пройдет на современной...

VIII Московский Городской Съезд педиатров с межрегиональным и международным участием "Трудный диагноз в педиатрии" Приглашаем педиатров, детских эндокринологов, реаниматологов, гинекологов, неонатологов, кардиологов, хирургов, урологов, психологов, специалистов по лучевой...

Journals of «GEOTAR-Media»