Healthy Cotwins Share Gut Microbiome Signatures With Their Inflammatory Bowel Disease Twins and Unrelated Patients.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
05 2021
Historique:
received: 07 08 2020
revised: 06 01 2021
accepted: 07 01 2021
pubmed: 22 1 2021
medline: 8 9 2021
entrez: 21 1 2021
Statut: ppublish

Résumé

It is currently unclear whether reported changes in the gut microbiome are cause or consequence of inflammatory bowel disease (IBD). Therefore, we studied the gut microbiome of IBD-discordant and -concordant twin pairs, which offers the unique opportunity to assess individuals at increased risk of developing IBD, namely healthy cotwins from IBD-discordant twin pairs. Fecal samples were obtained from 99 twins (belonging to 51 twin pairs), 495 healthy age-, sex-, and body mass index-matched controls, and 99 unrelated patients with IBD. Whole-genome metagenomic shotgun sequencing was performed. Taxonomic and functional (pathways) composition was compared among healthy cotwins, IBD-twins, unrelated patients with IBD, and healthy controls with multivariable (ie, adjusted for potential confounding) generalized linear models. No significant differences were observed in the relative abundance of species and pathways between healthy cotwins and their IBD-twins (false discovery rate <0.10). Compared with healthy controls, 13, 19, and 18 species, and 78, 105, and 153 pathways were found to be differentially abundant in healthy cotwins, IBD-twins, and unrelated patients with IBD, respectively (false discovery rate <0.10). Of these, 8 (42.1%) of 19 and 1 (5.6%) of 18 species, and 37 (35.2%) of 105 and 30 (19.6%) of 153 pathways overlapped between healthy cotwins and IBD-twins, and healthy cotwins and unrelated patients with IBD, respectively. Many of the shared species and pathways have previously been associated with IBD. The shared pathways include potentially inflammation-related pathways, for example, an increase in propionate degradation and L-arginine degradation pathways. The gut microbiome of healthy cotwins from IBD-discordant twin pairs displays IBD-like signatures. These IBD-like microbiome signatures might precede the onset of IBD. However, longitudinal follow-up studies are needed to infer a causal relationship.

Sections du résumé

BACKGROUND & AIMS
It is currently unclear whether reported changes in the gut microbiome are cause or consequence of inflammatory bowel disease (IBD). Therefore, we studied the gut microbiome of IBD-discordant and -concordant twin pairs, which offers the unique opportunity to assess individuals at increased risk of developing IBD, namely healthy cotwins from IBD-discordant twin pairs.
METHODS
Fecal samples were obtained from 99 twins (belonging to 51 twin pairs), 495 healthy age-, sex-, and body mass index-matched controls, and 99 unrelated patients with IBD. Whole-genome metagenomic shotgun sequencing was performed. Taxonomic and functional (pathways) composition was compared among healthy cotwins, IBD-twins, unrelated patients with IBD, and healthy controls with multivariable (ie, adjusted for potential confounding) generalized linear models.
RESULTS
No significant differences were observed in the relative abundance of species and pathways between healthy cotwins and their IBD-twins (false discovery rate <0.10). Compared with healthy controls, 13, 19, and 18 species, and 78, 105, and 153 pathways were found to be differentially abundant in healthy cotwins, IBD-twins, and unrelated patients with IBD, respectively (false discovery rate <0.10). Of these, 8 (42.1%) of 19 and 1 (5.6%) of 18 species, and 37 (35.2%) of 105 and 30 (19.6%) of 153 pathways overlapped between healthy cotwins and IBD-twins, and healthy cotwins and unrelated patients with IBD, respectively. Many of the shared species and pathways have previously been associated with IBD. The shared pathways include potentially inflammation-related pathways, for example, an increase in propionate degradation and L-arginine degradation pathways.
CONCLUSIONS
The gut microbiome of healthy cotwins from IBD-discordant twin pairs displays IBD-like signatures. These IBD-like microbiome signatures might precede the onset of IBD. However, longitudinal follow-up studies are needed to infer a causal relationship.

Identifiants

pubmed: 33476671
pii: S0016-5085(21)00097-4
doi: 10.1053/j.gastro.2021.01.030
pii:
doi:

Substances chimiques

Antigens, Bacterial 0
Siderophores 0
enterobacterial common antigen 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1970-1985

Investigateurs

Bas Oldenburg (B)
Femke van Wijk (F)
Eelco C Brand (EC)
Pieter Honkoop (P)
Rutger J Jacobs (RJ)
Cyriel Y Ponsioen (CY)
Nanne K H de Boer (NKH)
Yasser A Alderlieste (YA)
Margot A van Herwaarden (MA)
Sebastiaan A C van Tuyl (SAC)
Maurice W Lutgens (MW)
C Janneke van der Woude (C)
Wout G M Mares (WGM)
Daan B de Koning (DB)
Joukje H Bosman (JH)
Juda Vecht (J)
Anneke M P de Schryver (AMP)
Andrea E van der Meulen-de Jong (AE)
Marieke J Pierik (MJ)
Paul J Boekema (PJ)
Robert J Verburg (RJ)
Bindia Jharap (B)
Gonneke Willemsen (G)
Dorret I Boomsma (DI)
Jeroen M Jansen (JM)
Pieter C F Stokkers (PCF)
Frank Hoentjen (F)
Rutger Quispel (R)
Carmen S Horjus Talabur Horje (CS)
Paul C van de Meeberg (PC)
Nofel Mahmmod (N)
Rachel L West (RL)
Marleen Willems (M)
Itta M Minderhoud (IM)
Herma H Fidder (HH)
Fiona D M van Schaik (FDM)
Meike M C Hirdes (MMC)
Nynke A Boontje (NA)
Bart L M Müskens (BLM)
Rinse K Weersma (RK)
Marielle J L Romberg-Camps (MJL)

Informations de copyright

Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.

Auteurs

Eelco C Brand (EC)

Department of Gastroenterology and Hepatology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands; Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands.

Marjolein A Y Klaassen (MAY)

Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands; Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Ranko Gacesa (R)

Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands; Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Arnau Vich Vila (A)

Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands; Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Hiren Ghosh (H)

Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands; Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Marcel R de Zoete (MR)

Department of Medical Microbiology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands.

Dorret I Boomsma (DI)

Department of Biological Psychology, Behavioral and Movement Sciences, Vrije Universiteit, Amsterdam, the Netherlands; Amsterdam Public Health Research Institute, Vrije Universiteit Medical Center, Amsterdam, the Netherlands.

Frank Hoentjen (F)

Department of Gastroenterology and Hepatology, Radboud University Medical Center, Nijmegen, the Netherlands.

Carmen S Horjus Talabur Horje (CS)

Crohn & Colitis Center Rijnstate, Department of Gastroenterology and Hepatology, Rijnstate Hospital, Arnhem, the Netherlands.

Paul C van de Meeberg (PC)

Department of Gastroenterology & Hepatology, Slingeland Hospital, Doetinchem, the Netherlands.

Gonneke Willemsen (G)

Department of Biological Psychology, Behavioral and Movement Sciences, Vrije Universiteit, Amsterdam, the Netherlands; Amsterdam Public Health Research Institute, Vrije Universiteit Medical Center, Amsterdam, the Netherlands.

Jingyuan Fu (J)

Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands; Department of Pediatrics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Cisca Wijmenga (C)

Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Femke van Wijk (F)

Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands.

Alexandra Zhernakova (A)

Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands.

Bas Oldenburg (B)

Department of Gastroenterology and Hepatology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands. Electronic address: b.oldenburg@umcutrecht.nl.

Rinse K Weersma (RK)

Department of Gastroenterology and Hepatology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands; Department of Genetics, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands. Electronic address: r.k.weersma@umcg.nl.

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Classifications MeSH