Gastric Microbiota in Patients with Dyspepsia: Metatranscriptomic Analysis
https://doi.org/10.22416/1382-4376-2024-34-2-72-82
Abstract
Aim: to assess the composition of the microbiota of the mucous membrane of the body and the antrum of the stomach.
Materials and methods. Sixty patients with dyspeptic symptoms were included into the study. Two biopsy samples of the gastric mucosa (from the body of the stomach and the antrum) were obtained from each patient. The presence of H. pylori infection was confirmed by PCR; RNA was isolated and then libraries were prepared for metatranscriptomic analysis of the 16S rRNA gene. Sequencing was performed on MiSeq (Illumina, USA) using MiSeq Reagent Kit v3 (600-cycle) (Illumina, USA).
Results. The bacterial diversity decreases with the predominance of Helicobacter pylori species in H. pylori-positive patients. These results were confirmed by the Shannon index, the average value of which was 3.6 in the H. pylori-positive group and 5.4 in the H. pylori-negative group. In H. pylori-negative patients an increase in the representation of Streptococcus, Prevotella and Alloprevotella genera was observed. The level of H. pylori contamination of the gastric mucosa varies in the antrum and body of the stomach, in some cases reaching a 3.5-fold difference. Representation of other bacteria in the body and antrum of the stomach does not differ significantly.
Conclusion. The bacterial composition of the stomach is dependent on the presence of H. pylori. H. pylori leads to the decrease of the bacterial diversity with the predominance of H. pylori in gastric microbiome.
About the Authors
Е. А. KupriyanovaRussian Federation
Elena A. Kupriyanova — Researcher, Laboratory of Multiomics Technologies of Living Systems, Institute of Fundamental Medicine and Biology
420008, Kazan, Kremlyovskaya str., 18
М. I. Markelova
Russian Federation
Maria I. Markelova — Researcher, Laboratory of Multiomics Technologies of Living Systems, Institute of Fundamental Medicine and Biology
420008, Kazan, Kremlyovskaya str., 18
Е. А. Ziyatdinova
Russian Federation
Elvira A. Ziyatdinova — Head of the Clinical Diagnostic Laboratory No. 1 of the Medical-Sanitary Unit
420043, Kazan, Chekhov str., 1а
D. D. Safina
Russian Federation
Dilyara D. Safina — Cand. Sci. (Med.), Senior Lecturer at the Department of Internal Medicine, Institute of Fundamental Medicine and Biology
420008, Kazan, Kremlyovskaya str., 18
A. G. Safin
Russian Federation
Airat G. Safin — Endoscopist, Head of the Endoscopy Department No. 2, Medical-Sanitary Unit
420043, Kazan, Chekhova str., 1а
I. М. Alieva
Russian Federation
Ilmira M. Alieva — Cand. Sci. (Med.), Endoscopist at the Medical-Sanitary Unit
420043, Kazan, Chekhova str., 1a
R. К. Zalyalov
Russian Federation
Ramil K. Zalyalov — Endoscopist, Acting Head of the Endoscopy Department No. 1 of the Medical-Sanitary Unit
420043, Kazan, Chekhova str., 1a
R. А. Abdulkhakov
Russian Federation
Rustam A. Abdulkhakov — Dr. Sci. (Med.), Professor, Professor at the Department of Hospital Therapy; Honored Doctor of the Republic of Tatarstan
420012, Kazan, Butlerova str., 49
Т. V. Grigoryeva
Russian Federation
Tatiana V. Grigoryeva — Cand. Sci. (Biol.), Leading Researcher at the Research Laboratory of Genetics of Microorganisms
420008, Kazan, Kremlyovskaya str., 18
S. R. Abdulkhakov
Russian Federation
Sayar R. Abdulkhakov — Cand. Sci. (Med.), Docent, Head of the Department of Internal Disease, Institute of Fundamental Medicine and Biology; Associate Professor at the Department
of Outpatient Therapy and General Medical Practice
420008, Kazan, Kremlyovskaya str., 18
References
1. Prakash S., Rodes L., Coussa-Charley M., TomaroDuchesneau C. Gut microbiota: Next frontier inunderstanding human health and development of biotherapeutics. Biologics. 2011;5:71–86. DOI: 10.2147/BTT.S19099
2. Sekirov I., Russell S.L., Antunes L.C., Finlay B.B. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904. DOI: 10.1152/physrev.00045.2009
3. Petra C.V., Rus A., Dumitraşcu D.L. Gastric microbiota: Tracing the culprit. Clujul Med. 2017;90(4):369–76. DOI: 10.15386/cjmed-854
4. Uemura N., Okamoto S., Yamamoto S., Matsumura N., Yamaguchi S., Yamakido M., et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med. 2001;345(11):784–9. DOI: 10.1056/NEJMoa001999
5. International Agency for Research on Cancer, World Health Organization. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7–14. IARC Monogr Eval Carcinog Risks Hum. 1994;61:1–241.
6. Bik E.M., Eckburg P.B., Gill S.R., Nelson K.E., Purdom E.A., Francois F., et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA. 2006;103(3):732–7. DOI: 10.1073/pnas.0506655103
7. Hunt R.H., Yaghoobi M. The esophageal and gastric microbiome in health and disease. Gastroenterol Clin North Am. 2017;46(1):121–41. DOI: 10.1016/j.gtc.2016.09.009
8. Rajilic-Stojanovic M., Figueiredo C., Smet A., Hansen R., Kupcinskas J., Rokkas T., et al. Systematic review: Gastric microbiota in health and disease. Aliment Pharmacol Ther. 2020;51(6):582–602. DOI: 10.1111/apt.15650
9. Ivashkin V.T., Lapina T.L., Maev I.V., Drapkina O.M., Kozlov R.S., Sheptulin A.A., 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 Н. pylori diagnostics and treatment in adults. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2022;32(6):72–93. (In Russ.). DOI: 10.22416/1382-4376-2022-32-6-72-93
10. Doohan D., Rezkitha Y., Waskito L., Vilaichone R., Yamaoka Y., Miftahussurur M. Integrating microbiome, transcriptome and metabolome data to investigate gastric disease pathogenesis: A concise review. Expert Reviews in Molecular Medicine. 2021;23:e9. DOI: 10.1017/erm.2021.8
11. Rumyantseva D.E., Trukhmanov A.S., Kudryavtseva A.V., Krasnov G.S., Paraskevova A.V., Storonova O.A., et al. Microbiota of the esophagus and stomach in patients with gastroesophageal reflux disease and healthy volunteers. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2018;28(4):36–46. (In Russ.). DOI: 10.22416/1382-4376-2018-28-4-36-46
12. Amir I., Konikoff F.M., Oppenheim M., Gophna U., Half E.E. Gastric microbiota is altered in oesophagitis and Barrett’s oesophagus and further modified by proton pump inhibitors. Environ Microbiol. 2014;16(9):2905–14. DOI: 10.1111/1462-2920.12285
13. Parks D.H., Chuvochina M., Waite D.W., Rinke C., Skarshewski A., Chaumeil P.A., et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol. 2018;36(10):996– 1004. DOI: 10.1038/nbt.4229
14. Miao R., Wan C., Wang Z. The relationship of gastric microbiota and Helicobacter pylori infection in pediatrics population. Helicobacter. 2020;25(1):e12676. DOI: 10.1111/hel.12676
15. Vasapolli R., Schütte K., Schulz C., Vital M., Schomburg D., Pieper D.H., et al. Analysis of transcriptionally active bacteria throughout the gastrointestinal tract of healthy individuals. Gastroenterology. 2019;157(4):1081– 92.e3. DOI: 10.1053/j.gastro.2019.05.068
16. Maldonado-Contreras A., Goldfarb K.C., Godoy-Vitorino F., Karaoz U., Contreras M., Blaser M.J., et al. Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J. 2011;5(4):574–9. DOI: 10.1038/ismej.2010.149
17. Chen C.C., Liou J.M., Lee Y.C., Hong T.C., ElOmar E.M., Wu M.S. The interplay between Helicobacter pylori and gastrointestinal microbiota. Gut Microbes. 2021;13(1):1–22. DOI: 10.1080/19490976.2021.1909459
18. Parsons B.N., Ijaz U.Z., D’Amore R., Burkitt M.D., Eccles R., Lenzi L., et al. Comparison of the human gastric microbiota in hypochlorhydric states arising as a result of Helicobacter pylori-induced atrophic gastritis, autoimmune atrophic gastritis and proton pump inhibitor use. PLoS Pathog. 2017;13(11):e1006653. DOI: 10.1371/journal.ppat.1006653
19. Shao D., Vogtmann E., Liu A., Qin J., Chen W., Abnet C.C., et al. Microbial characterization of esophageal squamous cell carcinoma and gastric cardia adenocarcinoma from a high-risk region of China. Cancer. 2019;125(2):3993–4002. DOI: 10.1002/cncr.32403
20. Dai D., Yang Y., Yu J., Dang T., Qin W., Teng L., et al. Interactions between gastric microbiota and metabolites in gastric cancer. Cell Death Dis. 2021;12(12):1104. DOI: 10.1038/s41419-021-04396-y
21. Coker O.O., Dai Z., Nie Y., Zhao G., Cao L., Nakatsu G., et al. Mucosal microbiome dysbiosis in gastric carcinogenesis. Gut. 2018;67(6):1024–32. DOI: 10.1136/gutjnl-2017-314281
22. Qi Y.F., Sun J.N., Ren L.F., Cao X.L., Dong J.H., Tao K., et al. Intestinal microbiota is altered in patients with gastric cancer from Shanxi Province, China. Dig Dis Sci. 2019;64(5):1193–203. DOI: 10.1007/s10620-018-5411-y
23. Guo Y., Cao X.S., Zhou M.G., Yu B. Gastric microbiota in gastric cancer: Different roles of Helicobacter pylori and other microbes. Front Cell Infect Microbiol. 2023;12:1105811. DOI: 10.3389/fcimb.2022.1105811
24. Gantuya B., El-Serag H.B., Matsumoto T., Ajami N.J., Oyuntsetseg K., Azzaya D., et al. Gastric microbiota in Helicobacter pylori-negative and -positive gastritis among high incidence of gastric cancer area. Cancers (Basel). 2019;11(4):504. DOI: 10.3390/cancers11040504
25. He C., Peng C., Wang H., Ouyang Y., Zhu Z., Shu X., et al. The eradication of Helicobacter pylori restores rather than disturbs the gastrointestinal microbiota in asymptomatic young adults. Helicobacter. 2019;24(4):e12590. DOI: 10.1111/hel.12590
26. Li T.H., Qin Y., Sham P.C., Lau K.S., Chu K.M., Leung W.K. Alterations in gastric microbiota after H. pylori eradication and in different histological stages of gastric carcinogenesis. Sci Rep. 2017;7:44935. DOI: 10.1038/srep44935
27. Sung J.J.Y., Coker O.O., Chu E., Szeto C.H., Luk S.T.Y., Lau H.C.H., et al. Gastric microbes associated with gastric inflammation, atrophy and intestinal metaplasia 1 year after Helicobacter pylori eradication. Gut. 2020;69(9):1572–81. DOI: 10.1136/gutjnl-2019-319826
Supplementary files
Review
For citations:
Kupriyanova Е.А., Markelova М.I., Ziyatdinova Е.А., Safina D.D., Safin A.G., Alieva I.М., Zalyalov R.К., Abdulkhakov R.А., Grigoryeva Т.V., Abdulkhakov S.R. Gastric Microbiota in Patients with Dyspepsia: Metatranscriptomic Analysis. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2024;34(2):72-82. https://doi.org/10.22416/1382-4376-2024-34-2-72-82