The Compositional Structure of the Small Intestinal Microbial Community via Balloon-Assisted Enteroscopy

Nagasue T.a· Hirano A.a· Torisu T.a· Umeno J.a· Shibata H.b· Moriyama T.a,c· Kawasaki K.a· Fujioka S.a· Fuyuno Y.a· Matsuno Y.a· Esaki M.d· Kitazono T.a

Author affiliations

aDepartment of Medicine and Clinical Science, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
bMedical Institute of Bioregulation, Kyushu University, Fukuoka, Japan
cInternational Medical Department, Kyushu University Hospital, Fukuoka, Japan
dDivision of Gastroenterology, Department of Internal Medicine, Faculty of Medicine, Saga University, Saga, Japan

Log in to MyKarger to check if you already have access to this content.

Buy FullText & PDF Unlimited re-access via MyKarger Unrestricted printing, no saving restrictions for personal use
read more

CHF 38.00 *
EUR 35.00 *
USD 39.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.

Save over 20% compared to the individual article price.

Learn more

Rent/Cloud Rent for 48h to view Buy Cloud Access for unlimited viewing via different devices Synchronizing in the ReadCube Cloud Printing and saving restrictions apply Rental: USD 8.50
Cloud: USD 20.00

Select

Subscribe Access to all articles of the subscribed year(s) guaranteed for 5 years Unlimited re-access via Subscriber Login or MyKarger Unrestricted printing, no saving restrictions for personal use read more

Subcription rates

Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview

Abstract of Research Article

Received: July 29, 2021
Accepted: March 08, 2022
Published online: April 08, 2022

Number of Print Pages: 11
Number of Figures: 5
Number of Tables: 1

ISSN: 0012-2823 (Print)
eISSN: 1421-9867 (Online)

For additional information: https://www.karger.com/DIG

Abstract

Introduction: An association has been found between human-gut microbiota and various diseases (e.g., metabolic disease) by analyzing fecal or colonic microbiota. Despite the importance of the small intestinal microbiota, sampling difficulties prevent its full analysis. We investigated the composition and metagenomic functions of microbiota along the small intestine and compared them with the microbiota from feces and from other gastrointestinal (GI) sites. Methods: Mucosal samples from the six GI sites (stomach, duodenum, distal jejunum, proximal ileum, terminal ileum, and rectum) were collected under balloon-assisted enteroscopy. Fecal samples were collected from all participants. The microbial structures and metagenomic functions of the small intestinal mucosal microbiota were compared with those from feces and other GI sites using 16S ribosomal RNA gene sequencing. Results: We analyzed 133 samples from 29 participants. Microbial beta diversity analysis showed that the jejunum and ileum differed significantly from the lower GI tract and the feces (p < 0.001). Jejunal and duodenal microbiotas formed similar clusters. Wide clusters spanning the upper and lower GI tracts were observed with the ileal microbiota, which differed significantly from the jejunal microbiota (p < 0.001). Veillonella and Streptococcus were abundant in the jejunum but less so in the lower GI tract and feces. The metagenomic functions associated with nutrient metabolism differed significantly between the small intestine and the feces. Conclusions: The fact that the compositional structures of small intestinal microbiota differed from those of fecal and other GI microbiotas reveals that analyzing the small intestinal microbiota is necessary for association studies on metabolic diseases and gut microbiota.

© 2022 S. Karger AG, Basel

References Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904. Zeze K, Hirano A, Torisu T, Esaki M, Shibata H, Moriyama T, et al. Mucosal dysbiosis in patients with gastrointestinal follicular lymphoma. Hematol Oncol. 2020 Apr;38(2):181–8. Hirano A, Umeno J, Okamoto Y, Shibata H, Ogura Y, Moriyama T, et al. Comparison of the microbial community structure between inflamed and non-inflamed sites in patients with ulcerative colitis. J Gastroenterol Hepatol. 2018 Feb 20. Fukui A, Takagi T, Naito Y, Inoue R, Kashiwagi S, Mizushima K, et al. Higher levels of streptococcus in upper gastrointestinal mucosa associated with symptoms in patients with fFunctional dyspepsia. Digestion. 2020;101(1):38–45. Matsumoto H, Shiotani A, Katsumata R, Fukushima S, Handa Y, Osawa M, et al. Mucosa-associated microbiota in patients with irritable bowel syndrome: a comparison of subtypes. Digestion. 2021;102(1):49–56. Schroeder BO, Bäckhed F. Signals from the gut microbiota to distant organs in physiology and disease. Nat Med. 2016 Oct;22(10):1079–89. Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK. Specialized metabolites from the microbiome in health and disease. Cell Metab. 2014 Nov 4;20(5):719–30. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature. 2011 May 12;473(7346):174–80. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006 Dec 21;444(7122):1022–3. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol. 2002 Jul;68(7):3401–7. Miyauchi E, Taida T, Kawasumi M, Ohkusa T, Sato N, Ohno H. Analysis of colonic mucosa-associated microbiota using endoscopically collected lavage. Sci Rep. 2022;12(1):1758. Kastl AJ Jr, Terry NA, Wu GD, Albenberg LG. The structure and function of the human small intestinal microbiota: current understanding and future directions. Cell Mol Gastroenterol Hepatol. 2020;9(1):33–45. Zoetendal EG, Raes J, van den Bogert B, Arumugam M, Booijink CC, Troost FJ, et al. The human small intestinal microbiota is driven by rapid uptake and conversion of simple carbohydrates. ISME J. 2012 Jul;6(7):1415–26. Hartman AL, Lough DM, Barupal DK, Fiehn O, Fishbein T, Zasloff M, et al. Human gut microbiome adopts an alternative state following small bowel transplantation. Proc Natl Acad Sci U S A. 2009 Oct 6;106(40):17187–92. Hayashi H, Takahashi R, Nishi T, Sakamoto M, Benno Y. Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism. J Med Microbiol. 2005 Nov;54(Pt 11):1093–101. Yamamoto H, Kita H, Sunada K, Hayashi Y, Sato H, Yano T, et al. Clinical outcomes of double-balloon endoscopy for the diagnosis and treatment of small-intestinal diseases. Clin Gastroenterol Hepatol. 2004;2(11):1010–6. Matsumoto T. What is the clinical impact of double-balloon enteroscopy? Nat Clin Pract Gastroenterol Hepatol. 2006 May;3(5):252–3. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010 May;7(5):335–6. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010 Oct 1;26(19):2460–1. Ito K, Murphy D. Application of ggplot2 to pharmacometric graphics. CPT Pharmacometrics Syst Pharmacol. 2013 Oct 16;2:e79. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013 Sep;31(9):814–21. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014 Jan;42:D199–205. Kashiwagi S, Naito Y, Inoue R, Takagi T, Nakano T, Inada Y, et al. Mucosa-associated microbiota in the gastrointestinal tract of healthy Japanese subjects. Digestion. 2020;101(2):107–20. Vasapolli R, Schutte K, Schulz C, Vital M, Schomburg D, Pieper DH, et al. Analysis of transcriptionally active bacteria throughout the gastrointestinal tract of healthy individuals. Gastroenterology. 2019 Oct;157(4):1081–92.e3. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes. 2008 Nov;32(11):1720–4. Collado MC, Isolauri E, Laitinen K, Salminen S. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am J Clin Nutr. 2008 Oct;88(4):894–9. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010 Jan;18(1):190–5. Marchesi JR, Adams DH, Fava F, Hermes GD, Hirschfield GM, Hold G, et al. The gut microbiota and host health: a new clinical frontier. Gut. 2016 Feb;65(2):330–9. Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016 Jun 2;165(6):1332–45. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A Metagenome-Wide Association Study of gut microbiota in type 2 diabetes. Nature. 2012 Oct 4;490(7418):55–60. Karlsson FH, Tremaroli V, Nookaew I, Bergstrom G, Behre CJ, Fagerberg B, et al. Gut metagenome in European women with normal, impaired and diabetic glucose control. Nature. 2013 Jun 6;498(7452):99–103. Remely M, Aumueller E, Merold C, Dworzak S, Hippe B, Zanner J, et al. Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in type 2 diabetes and obesity. Gene. 2014 Mar 1;537(1):85–92. Wallace JL, Syer S, Denou E, de Palma G, Vong L, McKnight W, et al. Proton pump inhibitors exacerbate NSAID-induced small intestinal injury by inducing dysbiosis. Gastroenterology. 2011 Oct;141(4):1314–22 e1–5. Washio E, Esaki M, Maehata Y, Miyazaki M, Kobayashi H, Ishikawa H, et al. Proton pump inhibitors increase incidence of nonsteroidal anti-inflammatory drug-induced small bowel injury: a randomized, placebo-controlled trial. Clin Gastroenterol Hepatol. 2016 Jun;14(6):809–15.e1. Article / Publication Details

First-Page Preview

Abstract of Research Article

Received: July 29, 2021
Accepted: March 08, 2022
Published online: April 08, 2022

Number of Print Pages: 11
Number of Figures: 5
Number of Tables: 1

ISSN: 0012-2823 (Print)
eISSN: 1421-9867 (Online)

For additional information: https://www.karger.com/DIG

Copyright / Drug Dosage / Disclaimer Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

留言 (0)

沒有登入
gif