Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis

ObjectiveThe present study aims to investigate the effect of Helicobacter pylori (Hp) infection on gastric mucosal microbiota in patients with chronic gastritis.MethodsHere recruited a population of 193 patients with both chronic gastritis and positive rapid urease, including 124 patients with chron...

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Main Authors: Zhaolai Hua, Le Xu, Jiahui Zhu, Ling Xiao, Bin Lu, Jianping Wu, Zhenfeng Wu, Qihai Zhou, Junfeng Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1221433/full
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author Zhaolai Hua
Zhaolai Hua
Le Xu
Jiahui Zhu
Ling Xiao
Bin Lu
Jianping Wu
Zhenfeng Wu
Qihai Zhou
Junfeng Zhang
author_facet Zhaolai Hua
Zhaolai Hua
Le Xu
Jiahui Zhu
Ling Xiao
Bin Lu
Jianping Wu
Zhenfeng Wu
Qihai Zhou
Junfeng Zhang
author_sort Zhaolai Hua
collection DOAJ
description ObjectiveThe present study aims to investigate the effect of Helicobacter pylori (Hp) infection on gastric mucosal microbiota in patients with chronic gastritis.MethodsHere recruited a population of 193 patients with both chronic gastritis and positive rapid urease, including 124 patients with chronic atrophic gastritis (CAG) and 69 patients with chronic non-atrophic gastritis (nCAG). Immunoblotting was used to detect four serum Hp antibodies (UreA, UreB, VacA and CagA) to determine the types of virulent Hp-I and avirulent Hp-II infections. Gastric microbiota was profiled by 16S rRNA gene V3-V4 region, and R software was used to present the relationship between the microbial characteristics and the type of Hp infection.ResultsIn the stomach of patients with Hp-positive gastritis, the dominant gastric bacterial genera included Ralstonia (23.94%), Helicobacter (20.28%), Pseudonocardia (9.99%), Mesorhizobium (9.21%), Bradyrhizobium (5.05%), and Labrys (4.75%). The proportion of Hp-I infection was significantly higher in CAG patients (91.1%) than in nCAG patients (71.0%) (P < 0.001). The gastric microbiota richness index (observed OTUs, Chao) was significantly lower in CAG patients than in nCAG patients (P <0.05). Compared with avirulent Hp-II infection, virulent Hp-I infection significantly decreased the Shannon index in CAG patients (P <0.05). In nCAG patients, Hp-I infected patients had lower abundances of several dominant gastric bacteria (Aliidiomarina, Reyranella, Halomonas, Pseudomonas, Acidovorax) than Hp-II infected patients. Meanwhile, in CAG patients, Hp-I infected patients occupied lower abundances of several dominant oral bacteria (Neisseria, Staphylococcus and Haemophilus) than Hp-II infected patients. In addition, bile reflux significantly promoted the colonization of dominant oral microbiota (Veillonella, Prevotella 7 and Rothia) in the stomach of CAG patients. There was no significant symbiotic relationship between Helicobacter bacteria and non-Helicobacter bacteria in the stomach of nCAG patients, while Helicobacter bacteria distinctly linked with the non-Helicobacter bacteria (Pseudolabrys, Ralstonia, Bradyrhizobium, Mesorhizobium and Variovorax) in CAG patients.ConclusionsVirulent Hp infection alters the gastric microbiota, reduces microbial diversity, and enhances the symbiotic relationship between the Helicobacter bacteria and non-Helicobacter bacteria in patients with chronic gastritis. The data provides new evidence for treating Hp infection by improving the gastric microbiota.
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spelling doaj.art-450bcddab6a74eda8c916cd3d3e8ac432023-08-18T07:03:48ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-08-011310.3389/fcimb.2023.12214331221433Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritisZhaolai Hua0Zhaolai Hua1Le Xu2Jiahui Zhu3Ling Xiao4Bin Lu5Jianping Wu6Zhenfeng Wu7Qihai Zhou8Junfeng Zhang9Guangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University, Guilin, ChinaInstitute of Tumor Prevention and Control, People’s Hospital of Yangzhong City, Yangzhong, ChinaSchool of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, ChinaSchool of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, ChinaSchool of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Oncology, People’s Hospital of Yangzhong City, Yangzhong, ChinaSchool of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, ChinaDepartment of Surgical Oncology, Jiangsu Province Hospital of Chinese Medicine, Affiliated Hospital of Nanjing University of Chinese Medicine, Nanjing, ChinaGuangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University, Guilin, ChinaSchool of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing, ChinaObjectiveThe present study aims to investigate the effect of Helicobacter pylori (Hp) infection on gastric mucosal microbiota in patients with chronic gastritis.MethodsHere recruited a population of 193 patients with both chronic gastritis and positive rapid urease, including 124 patients with chronic atrophic gastritis (CAG) and 69 patients with chronic non-atrophic gastritis (nCAG). Immunoblotting was used to detect four serum Hp antibodies (UreA, UreB, VacA and CagA) to determine the types of virulent Hp-I and avirulent Hp-II infections. Gastric microbiota was profiled by 16S rRNA gene V3-V4 region, and R software was used to present the relationship between the microbial characteristics and the type of Hp infection.ResultsIn the stomach of patients with Hp-positive gastritis, the dominant gastric bacterial genera included Ralstonia (23.94%), Helicobacter (20.28%), Pseudonocardia (9.99%), Mesorhizobium (9.21%), Bradyrhizobium (5.05%), and Labrys (4.75%). The proportion of Hp-I infection was significantly higher in CAG patients (91.1%) than in nCAG patients (71.0%) (P < 0.001). The gastric microbiota richness index (observed OTUs, Chao) was significantly lower in CAG patients than in nCAG patients (P <0.05). Compared with avirulent Hp-II infection, virulent Hp-I infection significantly decreased the Shannon index in CAG patients (P <0.05). In nCAG patients, Hp-I infected patients had lower abundances of several dominant gastric bacteria (Aliidiomarina, Reyranella, Halomonas, Pseudomonas, Acidovorax) than Hp-II infected patients. Meanwhile, in CAG patients, Hp-I infected patients occupied lower abundances of several dominant oral bacteria (Neisseria, Staphylococcus and Haemophilus) than Hp-II infected patients. In addition, bile reflux significantly promoted the colonization of dominant oral microbiota (Veillonella, Prevotella 7 and Rothia) in the stomach of CAG patients. There was no significant symbiotic relationship between Helicobacter bacteria and non-Helicobacter bacteria in the stomach of nCAG patients, while Helicobacter bacteria distinctly linked with the non-Helicobacter bacteria (Pseudolabrys, Ralstonia, Bradyrhizobium, Mesorhizobium and Variovorax) in CAG patients.ConclusionsVirulent Hp infection alters the gastric microbiota, reduces microbial diversity, and enhances the symbiotic relationship between the Helicobacter bacteria and non-Helicobacter bacteria in patients with chronic gastritis. The data provides new evidence for treating Hp infection by improving the gastric microbiota.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1221433/fullHelicobacter pylorichronic gastritisgastric mucosamicrobiotasymbiotic relationship
spellingShingle Zhaolai Hua
Zhaolai Hua
Le Xu
Jiahui Zhu
Ling Xiao
Bin Lu
Jianping Wu
Zhenfeng Wu
Qihai Zhou
Junfeng Zhang
Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
Frontiers in Cellular and Infection Microbiology
Helicobacter pylori
chronic gastritis
gastric mucosa
microbiota
symbiotic relationship
title Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
title_full Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
title_fullStr Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
title_full_unstemmed Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
title_short Helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
title_sort helicobacter pylori infection altered gastric microbiota in patients with chronic gastritis
topic Helicobacter pylori
chronic gastritis
gastric mucosa
microbiota
symbiotic relationship
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1221433/full
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