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  • Proton pump inhibitors alter gut microbiota by promoting oral microbiota translocation: a prospective interventional study

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Gut microbiota
Original research
Proton pump inhibitors alter gut microbiota by promoting oral microbiota translocation: a prospective interventional study
  1. Xue Xiao1,2,
  2. Xian Zhang2,3,
  3. Jin Wang1,2,
  4. Yuqiang Liu1,2,
  5. Hailin Yan1,2,
  6. Xiaocun Xing1,2,
  7. Jinlin Yang1,2
  1. 1 Department of Gastroenterology and Hepatology, West China Hospital of Sichuan University, Chengdu, Sichuan, China
  2. 2 Sichuan University-University of Oxford Huaxi Joint Centre for Gastrointestinal Cancer, Frontiers Science Center for Disease-Related Molecular Network, West China Hospital of Sichuan University, Chengdu, Sichuan, China
  3. 3 Department of Pathology, West China Hospital of Sichuan University, Chengdu, Sichuan, China
  1. Correspondence to Dr Xue Xiao, Department of Gastroenterology and Hepatology, West China Hospital of Sichuan University, Chengdu, Sichuan, People's Republic of China; xxuenk{at}gmail.com; xiaoxue{at}wchscu.cn; Prof Jinlin Yang, Department of Gastroenterology and Hepatology, Sichuan University West China Hospital, Chengdu, Sichuan, 610041, China; mouse-577{at}163.com

Abstract

Background The mechanism by which proton pump inhibitors (PPIs) alter gut microbiota remains to be elucidated. We aimed to learn whether PPI induced gut microbiota alterations by promoting oral microbial translocation.

Methods Healthy adult volunteers were randomly assigned: PP group (n=8, 40 mg esomeprazole daily for seven days) and PM group (n=8, 40 mg esomeprazole along with chlorhexidine mouthwash after each meal for seven days). Fecal and saliva samples were analysed using 16S ribosomal RNA sequencing. Mouse models were introduced to confirm the findings in vivo, while the effect of pH on oral bacteria proliferation activity was investigated in vitro.

Results Taxon-based analysis indicated that PPI administration increased Streptococcus abundance in gut microbiota (P<0.001), and the increased species of Streptococcus were found to be from the oral site or oral/nasal sites, in which Streptococcus anginosus was identified as the significantly changed species (P<0.004). Microbial source tracker revealed that PPI significantly increased the contribution of oral bacteria to gut microbiota (P=0.026), and no significant difference was found in PM group (P=0.467). Compared to the baseline, there was a 42-fold increase in gut abundance of Streptococcus anginosus in PP group (P=0.002), and the times decreased to 16-fold in PM group (P=0.029). Mouse models showed that combination of PPI and Streptococcus anginosus significantly increased the gut abundance of Streptococcus anginosus compared with using PPI or Streptococcus anginosus only. Furthermore, Streptococcus anginosus cannot survive in vitro at a pH lower than 5.

Conclusions PPIs altered gut microbiota by promoting oral-originated Streptococcus translocation into gut.

  • PROTON PUMP INHIBITION
  • INTESTINAL MICROBIOLOGY

Data availability statement

16S rRNA gene sequencing data were deposited to Majorbio Cloud with project number MJ20201029026-MJ-M-20201122029 (http://edu.majorbio.com). All data generated in this study are available on reasonable request.

https://doi.org/10.1136/gutjnl-2023-330883

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    Data availability statement

    16S rRNA gene sequencing data were deposited to Majorbio Cloud with project number MJ20201029026-MJ-M-20201122029 (http://edu.majorbio.com). All data generated in this study are available on reasonable request.

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    Footnotes

    • XXiao, XZ and JW are joint first authors.

    • Correction notice This article has been corrected since it published Online First. The article type has been changed to original research.

    • Contributors Study concept and design: XXiao, XZ and JW. Collecting data: YQL, HLY and XCXing. Drafting manuscript: XXiao and XZ. Critical revision: XXiao, JW and JLY. Final approval of manuscript: All authors. XXiao, XZ and JW are joint first authors.

    • Funding This work was supported by the Sichuan Science and Technology Program (2023NSFSC1623) and National Natural Science Foundation of China (No. 82173253).

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.