Systemic Inflammation in Preclinical Ulcerative Colitis.


Journal

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

Informations de publication

Date de publication:
11 2021
Historique:
received: 03 12 2020
revised: 12 07 2021
accepted: 12 07 2021
pubmed: 24 7 2021
medline: 18 1 2022
entrez: 23 7 2021
Statut: ppublish

Résumé

Preclinical ulcerative colitis is poorly defined. We aimed to characterize the preclinical systemic inflammation in ulcerative colitis, using a comprehensive set of proteins. We obtained plasma samples biobanked from individuals who developed ulcerative colitis later in life (n = 72) and matched healthy controls (n = 140) within a population-based screening cohort. We measured 92 proteins related to inflammation using a proximity extension assay. The biologic relevance of these findings was validated in an inception cohort of patients with ulcerative colitis (n = 101) and healthy controls (n = 50). To examine the influence of genetic and environmental factors on these markers, a cohort of healthy twin siblings of patients with ulcerative colitis (n = 41) and matched healthy controls (n = 37) were explored. Six proteins (MMP10, CXCL9, CCL11, SLAMF1, CXCL11 and MCP-1) were up-regulated (P < .05) in preclinical ulcerative colitis compared with controls based on both univariate and multivariable models. Ingenuity Pathway Analyses identified several potential key regulators, including interleukin-1β, tumor necrosis factor, interferon-gamma, oncostatin M, nuclear factor-κB, interleukin-6, and interleukin-4. For validation, we built a multivariable model to predict disease in the inception cohort. The model discriminated treatment-naïve patients with ulcerative colitis from controls with leave-one-out cross-validation (area under the curve = 0.92). Consistently, MMP10, CXCL9, CXCL11, and MCP-1, but not CCL11 and SLAMF1, were significantly up-regulated among the healthy twin siblings, even though their relative abundances seemed higher in incident ulcerative colitis. A set of inflammatory proteins are up-regulated several years before a diagnosis of ulcerative colitis. These proteins were highly predictive of an ulcerative colitis diagnosis, and some seemed to be up-regulated already at exposure to genetic and environmental risk factors.

Sections du résumé

BACKGROUND & AIMS
Preclinical ulcerative colitis is poorly defined. We aimed to characterize the preclinical systemic inflammation in ulcerative colitis, using a comprehensive set of proteins.
METHODS
We obtained plasma samples biobanked from individuals who developed ulcerative colitis later in life (n = 72) and matched healthy controls (n = 140) within a population-based screening cohort. We measured 92 proteins related to inflammation using a proximity extension assay. The biologic relevance of these findings was validated in an inception cohort of patients with ulcerative colitis (n = 101) and healthy controls (n = 50). To examine the influence of genetic and environmental factors on these markers, a cohort of healthy twin siblings of patients with ulcerative colitis (n = 41) and matched healthy controls (n = 37) were explored.
RESULTS
Six proteins (MMP10, CXCL9, CCL11, SLAMF1, CXCL11 and MCP-1) were up-regulated (P < .05) in preclinical ulcerative colitis compared with controls based on both univariate and multivariable models. Ingenuity Pathway Analyses identified several potential key regulators, including interleukin-1β, tumor necrosis factor, interferon-gamma, oncostatin M, nuclear factor-κB, interleukin-6, and interleukin-4. For validation, we built a multivariable model to predict disease in the inception cohort. The model discriminated treatment-naïve patients with ulcerative colitis from controls with leave-one-out cross-validation (area under the curve = 0.92). Consistently, MMP10, CXCL9, CXCL11, and MCP-1, but not CCL11 and SLAMF1, were significantly up-regulated among the healthy twin siblings, even though their relative abundances seemed higher in incident ulcerative colitis.
CONCLUSIONS
A set of inflammatory proteins are up-regulated several years before a diagnosis of ulcerative colitis. These proteins were highly predictive of an ulcerative colitis diagnosis, and some seemed to be up-regulated already at exposure to genetic and environmental risk factors.

Identifiants

pubmed: 34298022
pii: S0016-5085(21)03277-7
doi: 10.1053/j.gastro.2021.07.026
pii:
doi:

Substances chimiques

Biomarkers 0
Blood Proteins 0
CCL11 protein, human 0
CCL2 protein, human 0
CXCL11 protein, human 0
CXCL9 protein, human 0
Chemokine CCL11 0
Chemokine CCL2 0
Chemokine CXCL11 0
Chemokine CXCL9 0
Inflammation Mediators 0
Proteome 0
SLAMF1 protein, human 0
Signaling Lymphocytic Activation Molecule Family Member 1 169535-43-7
MMP10 protein, human EC 3.4.24.22
Matrix Metalloproteinase 10 EC 3.4.24.22

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1526-1539.e9

Subventions

Organisme : Medical Research Council
ID : G0701898
Pays : United Kingdom

Investigateurs

Ian D Arnott (ID)
Monica Bayes (M)
Ferdinando Bonfiglio (F)
Ray K Boyapati (RK)
Adam Carstens (A)
Christina Casén (C)
Ewa Ciemniejewska (E)
Fredrik A Dahl (FA)
Trond Espen Detlie (TE)
Hazel E Drummond (HE)
Gunn S Ekeland (GS)
Daniel Ekman (D)
Anna B Frengen (AB)
Mats Gullberg (M)
Ivo G Gut (IG)
Marta Gut (M)
Simon C Heath (SC)
Fredrik Hjelm (F)
Henrik Hjortswang (H)
Gwo-Tzer Ho (GT)
Daisy Jonkers (D)
Johan Söderholm (J)
Nicholas A Kennedy (NA)
Charles W Lees (CW)
Torbjørn Lindahl (T)
Mårten Lindqvist (M)
Angelika Merkel (A)
Eddie Modig (E)
Aina E F Moen (AEF)
Hilde Nilsen (H)
Elaine R Nimmo (ER)
Colin L Noble (CL)
Niklas Nordberg (N)
Kate R O'Leary (KR)
Anette Ocklind (A)
Christine Olbjørn (C)
Erik Pettersson (E)
Marieke Pierik (M)
None Dominique

Informations de copyright

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

Auteurs

Daniel Bergemalm (D)

Department of Gastroenterology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden. Electronic address: daniel.bergemalm@regionorebrolan.se.

Erik Andersson (E)

Department of Gastroenterology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.

Johan Hultdin (J)

Department of Medical Biosciences, Division of Clinical Chemistry, Umeå University, Umeå, Sweden.

Carl Eriksson (C)

Department of Gastroenterology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.

Stephen T Rush (ST)

School of Medical Sciences, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.

Rahul Kalla (R)

Medical Research Council Centre for Inflammation Research, Queens Medical Research Institute, University of Edinburgh, Edinburgh, United Kingdom.

Alex T Adams (AT)

Translational Gastroenterology Unit, Nuffield Department of Medicine, Experimental Medicine Division, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom.

Åsa V Keita (ÅV)

Department of Biomedical and Clinical Sciences, Linköping University, Linköping, Sweden.

Mauro D'Amato (M)

CIC bioGUNE Basque Research and Technology Alliance and Basque Science Foundation, Bilbao, Spain; Division of Clinical Epidemiology, Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden.

Fernando Gomollon (F)

Hospital Clinico Universitario Lozano Blesa, IIS Aragón, Zaragoza, Spain.

Jørgen Jahnsen (J)

Department of Gastroenterology, Akershus University Hospital, Lørenskog, Norway; Institute of Clinical Medicine, University of Oslo, Oslo, Norway.

Petr Ricanek (P)

Department of Gastroenterology, Akershus University Hospital, Lørenskog, Norway.

Jack Satsangi (J)

Translational Gastroenterology Unit, Nuffield Department of Medicine, Experimental Medicine Division, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom; Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh, United Kingdom.

Dirk Repsilber (D)

School of Medical Sciences, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.

Pontus Karling (P)

Department of Public Health and Clinical Medicine, Division of Medicine, Umeå University, Umeå, Sweden.

Jonas Halfvarson (J)

Department of Gastroenterology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden.

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Classifications MeSH