Observational Study
Copyright ©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Jun 28, 2024; 30(24): 3076-3085
Published online Jun 28, 2024. doi: 10.3748/wjg.v30.i24.3076
Helicobacter pylori infection alters gastric microbiota structure and biological functions in patients with gastric ulcer or duodenal ulcer
Ling-Xiao Jin, Yu-Peng Fang, Chen-Mei Xia, Teng-Wei Cai, Qian-Qian Li, Yu-Yin Wang, Hai-Fan Yan, Xia Chen
Ling-Xiao Jin, Yu-Peng Fang, Chen-Mei Xia, Teng-Wei Cai, Qian-Qian Li, Yu-Yin Wang, Hai-Fan Yan, Xia Chen, Department of Gastroenterology, Wenling Hospital of Wenzhou Medical University (The First People’s Hospital of Wenling), Wenling 317500, Zhejiang Province, China
Co-first authors: Ling-Xiao Jin and Yu-Peng Fang.
Author contributions: Jin LX and Fang YP contributed equally to this work; Jin LX and Fang YP were involved in the study concept, design, and data collection; Jin LX, Chen X, and Cai TW were involved in securing funding for the project; Xia CM and Li QQ were involved in the interpretation of data; Wang YY and Yan HF were involved in the collection and analysis of data; Fang YP, Xia CM, Cai TW, Li QQ, Wang YY, and Yan HF were involved in drafting the initial manuscript; Jin LX, Fang YP, and Chen X were involved with the critical revision of the manuscript for important intellectual content and study supervision; all the authors have reviewed and approved the final manuscript.
Supported by Wenling Science and Technology Program, China, No. 2020S0180101; and Science and Technology Program of Traditional Chinese Medicine in Zhejiang Province, China, No. 2023ZL784.
Institutional review board statement: The study was reviewed and approved by the Wenling Hospital of Wenzhou Medical University (The First People’s Hospital of Wenling) Institutional Review Board (Approval No. KY-2020-1016-01).
Informed consent statement: All study participants, or their legal guardians, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: Technical appendix, statistical code, and dataset available from the corresponding author at werla@sina.com.
STROBE statement: The authors have read the STROBE Statement - checklist of items, and the manuscript was prepared and revised according to the STROBE Statement - checklist of items.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: Https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Xia Chen, MM, Chief Physician, Department of Gastroenterology, Wenling Hospital of Wenzhou Medical University (The First People’s Hospital of Wenling), No. 333 Chuan’an South Road, Chengxi Street, Wenling 317500, Zhejiang Province, China. werla@sina.com
Received: March 22, 2024
Revised: May 21, 2024
Accepted: May 31, 2024
Published online: June 28, 2024
Processing time: 95 Days and 9.2 Hours
Abstract
BACKGROUND

Helicobacter pylori (H. pylori) infection is closely associated with gastrointestinal diseases. Our preliminary studies have indicated that H. pylori infection had a significant impact on the mucosal microbiome structure in patients with gastric ulcer (GU) or duodenal ulcer (DU).

AIM

To investigate the contributions of H. pylori infection and the mucosal microbiome to the pathogenesis and progression of ulcerative diseases.

METHODS

Patients with H. pylori infection and either GU or DU, and healthy individuals without H. pylori infection were included. Gastric or duodenal mucosal samples was obtained and subjected to metagenomic sequencing. The compositions of the microbial communities and their metabolic functions in the mucosal tissues were analyzed.

RESULTS

Compared with that in the healthy individuals, the gastric mucosal microbiota in the H. pylori-positive patients with GU was dominated by H. pylori, with significantly reduced biodiversity. The intergroup differential functions, which were enriched in the H. pylori-positive GU patients, were all derived from H. pylori, particularly those concerning transfer RNA queuosine-modification and the synthesis of demethylmenaquinones or menaquinones. A significant enrichment of the uibE gene was detected in the synthesis pathway. There was no significant difference in microbial diversity between the H. pylori-positive DU patients and healthy controls.

CONCLUSION

H. pylori infection significantly alters the gastric microbiota structure, diversity, and biological functions, which may be important contributing factors for GU.

Keywords: Helicobacter pylori; Gastric ulcer; Duodenal ulcer; Metagenomic sequencing; Transfer RNA queuosine-modification; Menaquinones

Core Tip: In this study, we explored the influence and mechanism of action of Helicobacter pylori (H. pylori) on the development of gastric ulcer and duodenal ulcer, which are currently inconclusive. Metagenomic sequencing was performed on mucosal samples from H. pylori-infected patients with gastric ulcer or duodenal ulcer and healthy individuals. Mucosal flora structure, differentially functional genes, and metabolic pathways were analyzed to explore the role that H. pylori plays in the development of gastric ulcer and duodenal ulcer. Ultimately, two key metabolic pathways and related genes contributed from H. pylori were identified.