Preview

Russian Journal of Gastroenterology, Hepatology, Coloproctology

Advanced search

Serological Tests for Detection of Gastric Precancerous Lesions and Gastric Cancer

https://doi.org/10.22416/1382-4376-2025-35-5-85-99

Abstract

Aim: to present current information on serological screening approaches for precancerous gastric diseases and early gastric cancer.

Key points. Gastric cancer is one of the most common malignant tumors. Advanced stage of the tumor at the time of diagnosis determines an unfavorable prognosis in a significant proportion of patients. A real strategy for reducing both the incidence of gastric cancer and mortality rate is the introduction of cost-effective screening methods for atrophic gastritis associated with Helicobacter pylori (H. pylori) as a precancerous condition of the stomach. As an alternative to endoscopic examination of the stomach, approaches based on the evaluation of serological markers associated with H. pylori infection and reflecting the state of the gastric mucosa are currently proposed for laboratory screening: serum levels of antibodies to H. pylori, pepsinogen I, pepsinogen II and gastrin 17. Tests combining these markers, GastroPanel®, ABC and New ABC methods, as well as some of their modifications, are currently being widely studied as a tool for atrophic gastritis or gastric cancer risk group selection for further endoscopic examination.

Conclusion. An ensemble of serological markers, pepsinogen I, pepsinogen II, gastrin 17, and antibodies to H. pylori, allows for identifying atrophic gastritis with relatively high reliability, and considering additional factors, a high-risk group for the presence of gastric cancer. To achieve optimal medical and economic efficiency, it is necessary to improve the criteria for interpreting test results and including subjects in screening programs.

About the Authors

N. S. Sergeeva
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Russian Federation

Natalia S. Sergeeva — Dr.  Sci. (Biol.), Professor, Head of the Department of Prediction of the Effectiveness of Conservative Treatment

125284, Moscow, 2nd Botkinsky lane, 3



V. I. Ryabtseva
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Russian Federation

Valeriia I. Ryabtseva — Clinical Resident at the Endoscopy Department

125284, Moscow, 2nd Botkinsky lane, 3



S. S. Pirogov
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Russian Federation

Sergey S. Pirogov — Dr. Sci. (Med.), Head of the Endoscopy Department

125284, Moscow, 2nd Botkinsky lane, 3



T. A. Karmakova
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Russian Federation

Tatiana A. Karmakova — Dr. Sci. (Biol.), Leading Researcher of the Department of Prediction of the Effectiveness of Conservative Treatment

125284, Moscow, 2nd Botkinsky lane, 3



I. I. Alentov
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Russian Federation

Igor I. Alentov — Cand. Sci. (Biol.), Senior  Researcher of the Department of Prediction of the Effectiveness of Conservative Treatment

125284, Moscow, 2nd Botkinsky lane, 3

 



N. V. Marshutina
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre
Russian Federation

Nina V. Marshutina — Cand. Sci. (Biol.), Researcher of the Department of Prediction of the Effectiveness of Conservative Treatment

125284, Moscow, 2nd Botkinsky lane, 3



A. D. Kaprin
P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre; National Medical Research Radiological Centre; Peoples’ Friendship University of Russia named after Patrice Lumumba
Russian Federation

Andrey D. Kaprin — Dr. Sci. (Med.), Professor, Academician of Russian Academy of Sciences, Academician of the Russian Academy of Education, Director, P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre; General Director, National Medical Research Radiological Centre; Head of the Department of Oncology and Roentgenology named after V.P. Kharchenko, Peoples’ Friendship University of Russia named after Patrice Lumumba

249036, Obninsk, Koroleva str., 4



References

1. Kaprin A.D., Starinskij V.V., Shakhzadova A.O. (eds). Malignant neoplasms in Russia in 2023 (incidence and mortality). Moscow: P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre of the Ministry of Health of the Russian Federation, 2024. (In Russ.).

2. Bray F., Laversanne M., Sung H., Ferlay J., Siegel R.L., Soerjomataram I., et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2024;74(3):229–63. DOI: 10.3322/caac.21834

3. Karimi P., Islami F., Anandasabapathy S., Freedman N.D., Kamangar F. Gastric cancer: Descriptive epidemiology, risk factors, screening, and prevention. Cancer Epidemiol Prevent Biomarkers. 2014;23(5):700–13. DOI: 10.1158/1055-9965.EPI-13-1057

4. Hamashima C. Current issues and future perspectives of gastric cancer screening. World J Gastroenterol. 2014;20(38):13767–74. DOI: 10.3748/wjg.v20.i38.13767

5. Higashi T., Machii R., Aoki A., Hamashima C., Saito H. Evaluation and revision of checklists for screening facilities and municipal governmental programs for gastric cancer and colorectal cancer screening in Japan. Jpn J Clin Oncol. 2010;40(11):1021–30. DOI: 10.1093/jjco/hyq091

6. Kaprin A.D., Starinskij V.V., Shakhzadova A.O. (eds). The state of oncology care in Russia in 2023. Moscow: P. Hertsen Moscow Oncology Research Institute — Branch of the National Medical Research Radiological Centre of the Ministry of Health of the Russian Federation; 2024. (In Russ.).

7. Chiarello M.M., Fico V., Pepe G., Tropeano G., Adams N.J., Altieri G., et al. Early gastric cancer: A challenge in Western countries. World J Gastroenterol. 2022;28(7):693–703. DOI: 10.3748/wjg.v28.i7.693

8. Moss S.F. The clinical evidence linking Helicobacter pylori to gastric cancer. Cell Mol Gastroenterol Hepatol. 2016;3(2):183–91. DOI: 10.1016/j.jcmgh.2016.12.001

9. Duan Y., Xu Y., Dou Y., Xu D. Helicobacter pylori and gastric cancer: Mechanisms and new perspectives. J Hematol Oncol. 2025;18(1):10. DOI: 10.1186/s13045-024-01654-2

10. Waldum H., Mjønes P. The central role of gastrin in gastric cancer. Front Oncol. 2023;13:1176673. DOI: 10.3389/fonc.2023.1176673

11. Correa P., Piazuelo M.B. The gastric precancerous cascade. J Dig Dis. 2012;13(1):2–9. DOI: 10.1111/j.1751-2980.2011.00550.x

12. Shichijo S., Uedo N., Michida T. Detection of early gastric cancer after Helicobacter pylori eradication. Digestion. 2022;103(1):54–61. DOI: 10.1159/000519838

13. Loor A., Dumitraşcu D.L. Helicobacter pylori infection, gastric cancer and Gastropanel. Rom J Intern Med. 2016;54(3):151–6. DOI: 10.1515/rjim-2016-0025

14. Mäki M., Söderström D., Paloheimo L., Hendolin P., Suovaniemi O., Syrjänen K. Helicobacter pylori (Hp) IgG ELISA of the new-generation GastroPanel® is highly accurate in diagnosis of Hp-infection in gastroscopy referral patients. Anticancer Res. 2020;40(11):6387–98. DOI: 10.21873/anticanres.14660

15. Koivurova O.P., Koskela R., Blomster T., Ala-Rämi A., Lumme H., Kettunen O., et al. Serological biomarker panel in diagnosis of atrophic gastritis and Helicobacter pylori infection in gastroscopy referral patients: Clinical validation of the new-generation GastroPanel® test. Anticancer Res. 2021;41(11):5527–37. DOI: 10.21873/anticanres.15366

16. Tu H., Sun L., Dong X., Gong Y., Xu Q., Jing J., et al. A serological biopsy using five stomach-specific circulating biomarkers for gastric cancer risk assessment: A multiphase study. Am J Gastroenterol. 2017;112(5):704–15. DOI: 10.1038/ajg.2017.55

17. Lee S.Y., Ahn Y.S., Moon H.W. Comparison between the GastroPanel test and the serum pepsinogen assay interpreted with the ABC method-A prospective study. Helicobacter. 2024;29(1):e13056. DOI: 10.1111/hel.13056

18. Syrjänen K., Eskelinen M., Peetsalu A., Sillakivi T., Sipponen P., Härkönen M., et al. GastroPanel® biomarker assay: The most comprehensive test for Helicobacter pylori infection and its clinical sequelae. A critical review. Anticancer Res. 2019;39(3):1091–104. DOI: 10.21873/anticanres.13218

19. Storskrubb T., Aro P., Ronkainen J., Sipponen P., Nyhlin H., Talley N.J., et al. Serum biomarkers provide an accurate method for diagnosis of atrophic gastritis in a general population: The Kalixanda study. Scand J Gastroenterol. 2008;43(12):1448–55. DOI: 10.1080/00365520802273025

20. Duan S., Rico K., Merchant J.L. Gastrin: From physiology to gastrointestinal malignancies. Function (Oxf). 2021;3(1):zqab062. DOI: 10.1093/function/zqab062

21. Syrjänen K. A panel of serum biomarkers (GastroPanel®) in non-invasive diagnosis of atrophic gastritis. Systematic review and meta-analysis. Anticancer Res. 2016;36(10):5133–44. DOI: 10.21873/anticanres.11083

22. Xu Y., Miremadi A., Link A., Malfertheiner P., Fitzgerald R.C., Bornschein J. Feasibility of combined screening for upper gastrointestinal adenocarcinoma risk by serology and Cytosponge testing: The SUGAR study. J Clin Pathol. 2019;72(12):825–9. DOI: 10.1136/jclinpath-2019-205700

23. Paloheimo L., Tiusanen T., Suovaniemi O., SyrjÄnen K. Serological biomarker test (GastroPanel®) in the diagnosis of functional gastric disorders, Helicobacter pylori and atrophic gastritis in patients examined for dyspeptic symptoms. Anticancer Res. 2021;41(2):811–9. DOI: 10.21873/anticanres.14833

24. Belkovets A.V., Kurilovich S.A., Reshetnikov O.V., Ragino Yu., Scherbakova L.V. Prevalence and peculiarity of corpus atrophic gastritis in population with high level of Helicobacter pylori infection. Experimental & Clinical Gastroenterology. 2016;9:8–13 (In Russ.).

25. Bakulina N., Tikhonov S., Malkov V., Vorobyev S., Belyakov I., Peshkova N., et al. Non-invasive screening of autoimmune atrophic gastritis in asymptomatic subjects by serological biomarker test (GastroPanel®). Anticancer Res. 2022;42(3):1517–26. DOI: 10.21873/anticanres.15624

26. Zagari R.M., Rabitti S., Greenwood D.C., Eusebi L.H., Vestito A., Bazzoli F. Systematic review with meta-analysis: Diagnostic performance of the combination of pepsinogen, gastrin-17 and anti-Helicobacter pylori antibodies serum assays for the diagnosis of atrophic gastritis. Aliment Pharmacol Ther. 2017;46(7):657–67. DOI: 10.1111/apt.14248

27. Romańczyk M., Osmola M., Link A., Druet A., Hémont C., Martin J., et al. Non-invasive markers for the detection of gastric precancerous conditions. Cancers (Basel). 2024;16(12):2254. DOI: 10.3390/cancers16122254

28. Chapelle N., Petryszyn P., Blin J., Leroy M., Le BerreScoul C., Jirka I., et al. A panel of stomach-specific biomarkers (GastroPanel®) for the diagnosis of atrophic gastritis: A prospective, multicenter study in a low gastric cancer incidence area. Helicobacter. 2020;25(5):e12727. DOI: 10.1111/hel.12727

29. Lombardo L., Leto R., Molinaro G., Migliardi M., Ravarino N., Rocca R., et al. Prevalence of atrophic gastritis in dyspeptic patients in Piedmont. A survey using the GastroPanel test. Clin Chem Lab Med. 2010;48(9):1327–32. DOI: 10.1515/CCLM.2010.256

30. Tu H., Sun L., Dong X., Gong Y., Xu Q., Jing J., et al. Temporal changes in serum biomarkers and risk for progression of gastric precancerous lesions: A longitudinal study. Int J Cancer. 2015;136(2):425–34. DOI: 10.1002/ijc.29005

31. Roman L.D., Lukyanchuk R., Sablin O.A., Araslanova E.I., Eklund C., Hendolin P., et al. Prevalence of H. pylori infection and atrophic gastritis in a population-based screening with serum biomarker panel (GastroPanel®) in St. Petersburg. Anticancer Res. 2016;36(8):4129–38.

32. Sánchez-López J.Y., Díaz-Herrera L.C., Rizo-de la Torre L.D.C. Pepsinogen I, pepsinogen II, gastrin-17, and Helicobacter pylori serological biomarkers in the diagnosis of precursor lesions of gastric cancer. Arch Med Sci. 2024;20(3):1016–21. DOI: 10.5114/aoms/189971

33. Grad C., Pop A., Gaborean E., Grad S., Dumitrascu D. Value of GastroPanel in the diagnosis of atrophic gastritis. Exp Ther Med. 2021;22(5):1347. DOI: 10.3892/etm.2021.10782

34. Valle Muñoz J., Artaza Varasa T., López Pardo R., Rodríguez Merlo R., Pérez Grueso M.J., Martín Escobedo R., et al. Serological diagnosis of atrophic gastritis with a combination of pepsinogen I and II, gastrin-17 and anti-Helicobacter pylori antibodies. Gastroenterol Hepatol. 2007;30(10):567–71. (In Spanish). DOI: 10.1157/13112584

35. McNicholl A.G., Forné M., Barrio J., De la Coba C., González B., Rivera R., et al.; Helicobacter pylori Study Group of Asociación Española de Gastroenterología (AEG). Accuracy of GastroPanel for the diagnosis of atrophic gastritis. Eur J Gastroenterol Hepatol. 2014;26(9):941–8. DOI: 10.1097/MEG.0000000000000132

36. Taniyama Y., Katanoda K., Charvat H., Hori M., Ohno Y., Sasazuki S., et al. Estimation of lifetime cumulative incidence and mortality risk of gastric cancer. Jpn J Clin Oncol. 2017;47(11):1097–102. DOI: 10.1093/jjco/hyx128

37. Coelho M.C.F., Ribeiro H.G., Gomes C.G.O., Marinho F.P., Barbosa A.J.A., Coelho L.G.V. Helicobacter pylori chronic gastritis on patients with premalignant conditions: OLGA and OLGIM evaluation and serum biomarkers performance. Arq Gastroenterol. 2021;58(1):39– 47. DOI: 10.1590/S0004-2803.202100000-08

38. Ogutmen Koc D., Bektas S. Serum pepsinogen levels and OLGA/OLGIM staging in the assessment of atrophic gastritis types. Postgrad Med J. 2022;98(1160):441–5. DOI: 10.1136/postgradmedj-2020-139183

39. Peitz U., Wex T., Vieth M., Stolte M., Willich S., Labenz J., et al. Correlation of serum pepsinogens and gastrin-17 with atrophic gastritis in gastroesophageal reflux patients: A matched-pairs study. J Gastroenterol Hepatol. 2011;26(1):82–9. DOI: 10.1111/j.1440-1746.2010.06413.x

40. Belkovets A.V., Kurilovich S.A., Ragino Yu.I., Scherbakova L.V., Cheremisina О.В., Cherdyntseva N.V., et al. Biomarkers of gastric atrophy at stomach cancer. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2018;28(2):24–32. (In Russ.). DOI: 10.22416/1382-4376-2018-28-2-24-32

41. Gašenko E., Bogdanova I., Sjomina O., Aleksandraviča I., Kiršners A., Ancāns G., et al. Assessing the utility of pepsinogens and gastrin-17 in gastric cancer detection. Eur J Cancer Prev. 2023;32(5):478–84. DOI: 10.1097/CEJ.0000000000000791

42. Dondov G., Amarbayasgalan D., Batsaikhan B., Badamjav T., Batbaatar B., Tuvdenjamts B., et al. Diagnostic performances of pepsinogens and gastrin-17 for atrophic gastritis and gastric cancer in Mongolian subjects. PLoS One. 2022;17(10):e0274938. DOI: 10.1371/journal.pone.0274938

43. Nejadi-Kelarijani F., Roshandel G., Semnani S., Ahmadi A., Faghani B., Besharat S., et al. Diagnostic values of serum levels of pepsinogens and gastrin-17 for screening gastritis and gastric cancer in a high risk area in northern Iran. Asian Pac J Cancer Prev. 2014;15(17):7433–6. DOI: 10.7314/apjcp.2014.15.17.7433

44. Kurilovich S., Belkovets A., Reshetnikov O., Openko T., Malyutina S., Ragino Y., et al. Stomach-specific iomarkers (GastroPanel) can predict the development of gastric cancer in a Caucasian population: A longitudinal nested case-control study in Siberia. Anticancer Res. 2016;36(1):247–53.

45. Terasawa T., Nishida H., Kato K., Miyashiro I., Yoshikawa T., Takaku R., et al. Prediction of gastric cancer development by serum pepsinogen test and Helicobacter pylori seropositivity in eastern Asians: A systematic review and meta-analysis. PLoS One. 2014;9(10):e109783. DOI: 10.1371/journal.pone.0109783

46. Kim G.H., Bang S.J., Ende A.R., Hwang J.H. Is screening and surveillance for early detection of gastric cancer needed in Korean Americans? Korean J Int Med. 2015;30(6):747–58. DOI: 10.3904/kjim.2015.30.6.747

47. Chen W., Zheng R., Baade P.D., Zhang S., Zeng H., Bray F., et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–32. DOI: 10.3322/caac.21338

48. Miki K. Gastric cancer screening by combined assay for serum anti-Helicobacter pylori IgG antibody and serum pepsinogen levels — “ABC method”. Proc Jpn Acad Ser B Phys Biol Sci. 2011;87(7):405–14. DOI: 10.2183/pjab.87.405

49. Kishikawa H., Kimura K., Takarabe S., Kaida S., Nishida J. Helicobacter pylori antibody titer and gastric cancer screening. Dis Markers. 2015;2015:156719. DOI: 10.1155/2015/156719

50. Kishino T., Oyama T., Tomori A., Takahashi A., Shinohara T. Usefulness and limitations of a serum screening system to predict the risk of gastric cancer. Intern Med. 2020;59(12):1473–80. DOI: 10.2169/internalmedicine.3521-19

51. Kishikawa H., Nakamura K., Takarabe S., Katayama T., Sasaki A., Miura S., et al. Clinical characteristics of patients with previous Helicobacter pylori infectioninduced atrophic gastritis. Cureus. 2024;16(6):e63368. DOI: 10.7759/cureus.63368

52. Kotachi T., Ito M., Yoshihara M., Boda T., Kiso M., Masuda K., et al. Serological evaluation of gastric cancer risk based on pepsinogen and Helicobacter pylori antibody: Relationship to endoscopic findings. Digestion. 2017;95(4):314–8. DOI: 10.1159/000477239

53. Cho J.H., Jin S.Y., Park S. Scoring model for discriminating gastric cancer risk in patients with negative serum pepsinogen and anti-Helicobacter pylori antibody results. J Gastroenterol Hepatol. 2021;36(12):3345–53. DOI: 10.1111/jgh.15630

54. Nagasaki N., Ito M., Boda T., Kotachi T., Takigawa H., Oka S., et al. Identification of Helicobacter pylori-related gastric cancer risk using serological gastritis markers and endoscopic findings: A large-scale retrospective cohort study. BMC Gastroenterol. 2022;22(1):299. DOI: 10.1186/s12876-022-02381-z

55. Ni D.Q., Lyu B., Bao H.B., Jin H.F., Zhao J., Xu Y., et al. Comparison of different serological methods in screening early gastric cancer. Zhonghua Nei Ke Za Zhi. 2019;1;58(4):294–300. [In Chinese]. DOI: 10.3760/cma.j.issn.0578-1426.2019.04.011

56. Yamaguchi Y., Nagata Y., Hiratsuka R., Kawase Y., Tominaga T., Takeuchi S., et al. Gastric cancer screening by combined assay for serum anti-Helicobacter pylori IgG antibody and serum pepsinogen levels — The ABC method. Digestion. 2016;93(1):13–8. DOI: 10.1159/000441742

57. Baek S.M., Kim N., Kwon Y.J., Lee H.S., Kim H.Y., Lee J., et al. Role of serum pepsinogen II and Helicobacter pylori status in the detection of diffuse-type early gastric cancer in young individuals in South Korea. Gut Liver. 2020;14(4):439–49. DOI: 10.5009/gnl19091

58. Li P., Li Z., Linghu E., Ji J.; Society of Digestive Endoscopy of the Chinese Medical Association, Colorectal Surgery Group of the Chinese Medical Association, Chinese Association of Gastroenterologists & Hepatologists, National Clinical Research Center for Digestive Diseases, Chinese Medical Journal Clinical Practice Guideline Collaborative. Chinese national clinical practice guidelines on the prevention, diagnosis, and treatment of early gastric cancer. Chin Med J (Engl). 2024;137(8):887–908. DOI: 10.1097/CM9.0000000000003101

59. Chinese Society of Digestive Endoscopy. Consensus on screening and endoscopic diagnosis and treatment of early gastric cancer in China (Changsha, 2014). Zhong hua Xiao Hua Nei Jing Za Zhi. 2014;31(7):361–77.

60. Hu Y., Bao H., Jin H., Zhao J., Xu Y., Huang X., et al. Performance evaluation of four prediction models for risk stratification in gastric cancer screening among a high-risk population in China. Gastric Cancer. 2021;24(6):1194– 202. DOI: 10.1007/s10120-021-01204-6

61. Li M.Y., Zhang D.Q., Lu X., Chen W.C. Comparison of two serological methods in screening gastric cancer and its precancerous condition. Zhonghua Nei Ke Za Zhi. 2018;57(12):907–11. [In Chinese]. DOI: 10.3760/cma.j.issn.0578-1426.2018.12.006

62. Liu X.M., Ma X.Y., Liu F., Liu Z.L., Tang X.Y., Ji M.Z., et al. Gastric cancer screening methods: A comparative study of the Chinese New Gastric Cancer Screening Score and Kyoto classification of gastritis. Gastroenterol Res Pract. 2022;2022:7639968. DOI: 10.1155/2022/7639968

63. Cai Q., Zhu C., Yuan Y., Feng Q., Feng Y., Hao Y., et al.; Gastrointestinal Early Cancer Prevention & Treatment Alliance of China (GECA). Development and validation of a prediction rule for estimating gastric cancer risk in the Chinese high-risk population: A nationwide multicentre study. Gut. 2019;68(9):1576–87. DOI: 10.1136/gutjnl-2018-317556

64. Li L., Ni J., Sun S., Zha X., Li R., He C. Clinical applicability of a new scoring system for population-based screening and risk factors of gastric cancer in the Wannan region. BMC Gastroenterol. 2022;22(1):306. DOI: 10.1186/s12876-022-02384-w


Supplementary files

Review

For citations:


Sergeeva N.S., Ryabtseva V.I., Pirogov S.S., Karmakova T.A., Alentov I.I., Marshutina N.V., Kaprin A.D. Serological Tests for Detection of Gastric Precancerous Lesions and Gastric Cancer. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2025;35(5):85-99. https://doi.org/10.22416/1382-4376-2025-35-5-85-99

Views: 19


ISSN 1382-4376 (Print)
ISSN 2658-6673 (Online)