Characteristics of Gastric Mucosa-Associated Microbiota in Patients with Early Gastric Cancer After Successful Helicobacter pylori Eradication.


Journal

Digestive diseases and sciences
ISSN: 1573-2568
Titre abrégé: Dig Dis Sci
Pays: United States
ID NLM: 7902782

Informations de publication

Date de publication:
12 2023
Historique:
received: 24 12 2022
accepted: 10 10 2023
medline: 10 11 2023
pubmed: 25 10 2023
entrez: 24 10 2023
Statut: ppublish

Résumé

Helicobacter pylori (H. pylori) is widely recognized as a definite carcinogen in gastric cancer (GC). Although H. pylori eradication reduces the risk of GC, GC recurrence has been detected even after successful H. pylori eradication. Recently, the analysis of gut microbiota was reported. This study aimed to evaluate the correlation between gastric mucosa-associated microbiota (G-MAM) and early gastric cancer (EGC) after successful H. pylori eradication. In this pilot study, G-MAM were collected during the esophagogastroduodenoscopy of 17 patients, receiving H. pylori eradication therapy at least 5 years ago. The patients were divided into those with EGC (the EGC group, 8 patients) and those without EGC (the NGC group, 9 patients). Microbial samples in the greater curvature of the pyloric site were obtained using an endoscopic cytology brush, and the G-MAM profiles of each sample were analyzed using 16S rRNA V3-V4 gene sequencing. Between the two groups, there was no significant difference in the median age, sex, median period after successful eradication of H. pylori, the α diversity, and the average abundance at the phylum level. At the genus level, the average abundance of Unclassified Oxalobacteraceae, Capnocytophaga, and Haemophilus was significantly lower in the EGC group than in the NGC group (0.89 vs. 0.14%, P < 0.01, 0.28 vs. 0.00%, P < 0.01 and 5.84 vs. 2.16%, P = 0.034, respectively). We demonstrated alternations in the profiles of G-MAM between the two groups. Our results suggest that G-MAM may influence carcinogenesis after successful H. pylori eradication.

Sections du résumé

BACKGROUND
Helicobacter pylori (H. pylori) is widely recognized as a definite carcinogen in gastric cancer (GC). Although H. pylori eradication reduces the risk of GC, GC recurrence has been detected even after successful H. pylori eradication. Recently, the analysis of gut microbiota was reported.
AIMS
This study aimed to evaluate the correlation between gastric mucosa-associated microbiota (G-MAM) and early gastric cancer (EGC) after successful H. pylori eradication.
METHODS
In this pilot study, G-MAM were collected during the esophagogastroduodenoscopy of 17 patients, receiving H. pylori eradication therapy at least 5 years ago. The patients were divided into those with EGC (the EGC group, 8 patients) and those without EGC (the NGC group, 9 patients). Microbial samples in the greater curvature of the pyloric site were obtained using an endoscopic cytology brush, and the G-MAM profiles of each sample were analyzed using 16S rRNA V3-V4 gene sequencing.
RESULTS
Between the two groups, there was no significant difference in the median age, sex, median period after successful eradication of H. pylori, the α diversity, and the average abundance at the phylum level. At the genus level, the average abundance of Unclassified Oxalobacteraceae, Capnocytophaga, and Haemophilus was significantly lower in the EGC group than in the NGC group (0.89 vs. 0.14%, P < 0.01, 0.28 vs. 0.00%, P < 0.01 and 5.84 vs. 2.16%, P = 0.034, respectively).
CONCLUSIONS
We demonstrated alternations in the profiles of G-MAM between the two groups. Our results suggest that G-MAM may influence carcinogenesis after successful H. pylori eradication.

Identifiants

pubmed: 37875607
doi: 10.1007/s10620-023-08154-2
pii: 10.1007/s10620-023-08154-2
doi:

Substances chimiques

RNA, Ribosomal, 16S 0
Anti-Bacterial Agents 0

Banques de données

UMIN-CTR
['UMIN000025702']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4398-4406

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

International Agency for Research on Cancer. Schistosomes liver flukes and Helicobacter pylori IARC working group on the evaluation of carcinogenic risks to humans. Monogr Eval Carcinog Risks Hum 1994;61:1–241.
Uemura N, Okamoto S, Yamamoto S et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001;345:784–789.
pubmed: 11556297
Ford AC, Forman D, Hunt RH, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomised controlled trials. Bmj 2014;348:g3174.
pubmed: 24846275 pmcid: 4027797
Fukase K, Kato M, Kikuchi S et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008;372:392–397.
pubmed: 18675689
Kamada T, Hata J, Sugiu K et al. Clinical features of gastric cancer discovered after successful eradication of Helicobacter pylori: results from a 9-year prospective follow-up study in Japan. Aliment Pharmacol Ther 2005;21:1121–1126.
pubmed: 15854174
Majima A, Handa O, Naito Y et al. Early-stage gastric cancer can be found in improved atrophic mucosa over time from successful Helicobacter pylori eradication. Digestion 2017;95:194–200.
pubmed: 28288471
Take S, Mizuno M, Ishiki K et al. The long-term risk of gastric cancer after the successful eradication of Helicobacter pylori. J Gastroenterol 2011;46:318–324.
pubmed: 21103997
Malfertheiner P, Megraud F, O’Morain CA et al. Management of Helicobacter pylori infection–the Maastricht IV/florence consensus report. Gut J 2012;61:646–664.
Mori G, Nakajima T, Asada K et al. Incidence of and risk factors for metachronous gastric cancer after endoscopic resection and successful Helicobacter pylori eradication: results of a large-scale, multicenter cohort study in Japan. Gastric Cancer 2016;19:911–918.
pubmed: 26420267
Shichijo S, Hirata Y, Niikura R et al. Histologic intestinal metaplasia and endoscopic atrophy are predictors of gastric cancer development after Helicobacter pylori eradication. Gastrointest Endosc 2016;84:618–624.
pubmed: 26995689
Shao D, Vogtmann E, Liu A et al. Microbial characterization of esophageal squamous cell carcinoma and gastric cardia adenocarcinoma from a high-risk region of China. Cancer 2019;125:3993–4002.
pubmed: 31355925
Mima K, Nishihara R, Qian ZR et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 2016;65:1973–1980.
pubmed: 26311717
Takagi T, Inoue R, Oshima A et al. Typing of the gut microbiota community in Japanese subjects. Microorganisms 2022;10:664.
pubmed: 35336239 pmcid: 8954045
Coker OO, Dai Z, Nie Y et al. Mucosal microbiome dysbiosis in gastric carcinogenesis. Gut 2018;67:1024–1032.
pubmed: 28765474
Kashiwagi S, Naito Y, Inoue R et al. Mucosa-associated microbiota in the gastrointestinal tract of healthy Japanese subjects. Digestion 2020;101:107–120.
pubmed: 30721900
Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 2011;14:101–112.
Inoue R, Sakaue Y, Sawai C et al. A preliminary investigation on the relationship between gut microbiota and gene expressions in peripheral mononuclear cells of infants with autism spectrum disorders. Biosci Biotechnol Biochem 2016;80:2450–2458.
pubmed: 27581276
Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011;27:2957–2963.
pubmed: 21903629 pmcid: 3198573
Caporaso JG, Kuczynski J, Stombaugh J et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335–336.
pubmed: 20383131 pmcid: 3156573
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010;26:2460–2461.
pubmed: 20709691
Edgar R. UCHIME2: improved chimera prediction for amplicon sequencing. bioRxiv. 2016
Wang Q, Garrity GM, Tiedje JM et al. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007;73:5261–5267.
pubmed: 17586664 pmcid: 1950982
Sung JJY, Coker OO, Chu E et al. Gastric microbes associated with gastric inflammation, atrophy and intestinal metaplasia 1 year after Helicobacter pylori eradication. Gut 2020;69:1572–1580.
pubmed: 31974133
Li TH, Qin Y, Sham PC et al. Alterations in gastric microbiota after H. pylori eradication and in different histological stages of gastric carcinogenesis. Sci Rep 2017;7:44935.
pubmed: 28322295 pmcid: 5359573
Dicksved J, Lindberg M, Rosenquist M et al. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol 2009;58:509–516.
pubmed: 19273648
Mager DL, Haffajee AD, Devlin PM et al. The salivary microbiota as a diagnostic indicator of oral cancer: a descriptive, non-randomized study of cancer-free and oral squamous cell carcinoma subjects. J Transl Med 2005;3:27.
pubmed: 15987522 pmcid: 1226180
Galvão-Moreira LV, da Cruz MC. Oral microbiome, periodontitis and risk of head and neck cancer. Oral Oncol 2016;53:17–19.
pubmed: 26684542
Wei Q, Zhang Q, Wu Y et al. Analysis of bacterial diversity and community structure in gastric juice of patients with advanced gastric cancer. Discov Oncol 2023;14:7.
pubmed: 36662326 pmcid: 9860007
Zhang X, Li C, Cao W, Zhang Z. Alterations of gastric microbiota in gastric cancer and precancerous stages. Front Cell Infect Microbiol 2021;11:559148.
pubmed: 33747975 pmcid: 7966516
Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R et al. Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep 2014;4:4202.
pubmed: 24569566 pmcid: 3935187
Huse SM, Young VB, Morrison HG et al. Comparison of brush and biopsy sampling methods of the ileal pouch for assessment of mucosa-associated microbiota of human subjects. Microbiome 2014;2:5.
pubmed: 24529162 pmcid: 3931571
Nishino K, Nishida A, Inoue R et al. Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J Gastroenterol 2018;53:95–106.
pubmed: 28852861
Takagi T, Naito Y, Inoue R et al. Differences in gut microbiota associated with age, sex, and stool consistency in healthy Japanese subjects. J Gastroenterol 2019;54:53–63.
pubmed: 29926167
Hatayama K, Kono K, Okuma K et al. Sex differences in intestinal microbiota and their association with some diseases in a Japanese population observed by analysis using a large dataset. Biomedicines 2023;11:376.
pubmed: 36830915 pmcid: 9953495
Tahara T, Yamamoto E, Suzuki H et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res 2014;74:1311–1318.
pubmed: 24385213 pmcid: 4396185
Nakajima T, Maekita T, Oda I et al. Higher methylation levels in gastric mucosae significantly correlate with higher risk of gastric cancers. Cancer Epidemiol Biomarkers Prev 2006;15:2317–2321.
pubmed: 17119066
Nakajima T, Enomoto S, Yamashita S et al. Persistence of a component of DNA methylation in gastric mucosae after Helicobacter pylori eradication. J Gastroenterol 2010;45:37–44.
pubmed: 19821005
Hollister EB, Gao C, Versalovic J. Compositional and functional features of the gastrointestinal microbiome and their effects on human health. Gastroenterology 2014;146:1449–1458.
pubmed: 24486050
Ezoe Y, Muto M, Uedo N et al. Magnifying narrowband imaging is more accurate than conventional white-light imaging in diagnosis of gastric mucosal cancer. Gastroenterology 2011;141:2017–2025.e2013.
pubmed: 21856268
Dohi O, Yagi N, Naito Y et al. Blue laser imaging-bright improves the real-time detection rate of early gastric cancer: a randomized controlled study. Gastrointest Endosc 2019;89:47–57.
pubmed: 30189197
Ono S, Kato M, Tsuda M et al. Lavender color in linked color imaging enables noninvasive detection of gastric intestinal metaplasia. Digestion 2018;98:222–230.
pubmed: 30045046
Majima A, Dohi O, Takayama S et al. Linked color imaging identifies important risk factors associated with gastric cancer after successful eradication of Helicobacter pylori. Gastrointest Endosc 2019;90:763–769.
pubmed: 31299258

Auteurs

Takahiro Nakano (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.
Department of Gastroenterology and Hepatology, Japanese Red Cross Society Kyoto Daiichi Hospital, Kyoto, Japan.

Osamu Dohi (O)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan. osamu-d@koto.kpu-m.ac.jp.

Tomohisa Takagi (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Yuji Naito (Y)

Department of Human Immunology and Nutrition Science, Kyoto Prefectural University of Medicine, Kyoto, Japan.

Hayato Fukui (H)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Hajime Miyazaki (H)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Takeshi Yasuda (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Takuma Yoshida (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Yuka Azuma (Y)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Tsugitaka Ishida (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Hiroaki Kitae (H)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Shinya Matsumura (S)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Shun Takayama (S)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Naoki Mizuno (N)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Saori Kashiwagi (S)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Katsura Mizushima (K)

Department of Human Immunology and Nutrition Science, Kyoto Prefectural University of Medicine, Kyoto, Japan.

Ryo Inoue (R)

Laboratory of Animal Science, Department of Applied Biological Sciences, Faculty of Agriculture, Setsunan University, Osaka, Japan.

Toshifumi Doi (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Ryohei Hirose (R)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Ken Inoue (K)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Naohisa Yoshida (N)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Kazuhiro Kamada (K)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Kazuhiko Uchiyama (K)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Takeshi Ishikawa (T)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Hideyuki Konishi (H)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Yoshito Itoh (Y)

Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, 465 Kawaramachi Hirokoji Kamigyo-ku, Kyoto, 602-8566, Japan.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH