Comprehensive association analyses of extraintestinal manifestations in inflammatory bowel disease.

Inflammatory bowel disease extraintestinal manifestations genetics serology

Journal

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

Informations de publication

Date de publication:
27 Feb 2024
Historique:
received: 16 07 2022
revised: 11 02 2024
accepted: 13 02 2024
medline: 16 3 2024
pubmed: 16 3 2024
entrez: 15 3 2024
Statut: aheadofprint

Résumé

Patients with IBD frequently develop extraintestinal manifestations (EIM) that significantly contribute to morbidity. We assembled the largest multi-cohort dataset to-date to investigate the clinical, serological, and genetic factors associated with EIM complications in IBD. Data were available in 12,083 unrelated European ancestry IBD cases with presence/absence of EIMs (ankylosing spondylitis (AS-SI), primary sclerosing cholangitis (PSC), peripheral arthritis, and skin and ocular manifestations) across four cohorts (Cedars-Sinai Medical Center, NIDDK IBD Genetics Consortium, SHARE Consortium, and RISK cohort). Clinical and serological parameters were analyzed by univariable and multivariable regression analyses using a mixed-effects model. Within-case logistic regression was performed to assess genetic associations. Most EIMs occurred more commonly in patients with female sex (overall EIM: P=9.0E-05, OR=1.2 [1.1-1.4]), CD (especially colonic disease location; P=9.8E-09, OR=1.7 [1.4-2.0]), and in subjects who required surgery (both CD and UC; P=3.6E-19, OR=1.7 [1.5-1.9]). Smoking increased risk of EIMs except for PSC where there was a 'protective' effect. Multiple serological associations were observed including with PSC (ANCA, ASCA, anti-CBir1) and any EIM (ANCA, ASCA, anti-I2). We identified genome-wide significant associations within MHC (AS-SI P=1.4E-15, OR=2.5 [2.0-3.1]; PSC P=2.7E-10, OR=2.8 [2.0-3.8]; ocular P=2E-08, OR=3.6 [2.3-5.6]; and overall EIM P=8.4E-09, OR=2.2 [1.7-2.9]) and CPEB4 (SKIN P=2.7E-08, OR=1.5 [1.3-1.8]). Genetic associations implicated TNF, JAK-STAT and IL6 as potential targets for EIMs. Contrary to previous reports, only 2% of our subjects had multiple EIMs and most co-occurrences were negatively correlated. We have identified demographic, clinical and genetic associations with EIMs that reveal underlying mechanisms and implicate novel and existing drug targets: important steps towards more personalized approach to IBD management.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
Patients with IBD frequently develop extraintestinal manifestations (EIM) that significantly contribute to morbidity. We assembled the largest multi-cohort dataset to-date to investigate the clinical, serological, and genetic factors associated with EIM complications in IBD.
METHODS METHODS
Data were available in 12,083 unrelated European ancestry IBD cases with presence/absence of EIMs (ankylosing spondylitis (AS-SI), primary sclerosing cholangitis (PSC), peripheral arthritis, and skin and ocular manifestations) across four cohorts (Cedars-Sinai Medical Center, NIDDK IBD Genetics Consortium, SHARE Consortium, and RISK cohort). Clinical and serological parameters were analyzed by univariable and multivariable regression analyses using a mixed-effects model. Within-case logistic regression was performed to assess genetic associations.
RESULTS RESULTS
Most EIMs occurred more commonly in patients with female sex (overall EIM: P=9.0E-05, OR=1.2 [1.1-1.4]), CD (especially colonic disease location; P=9.8E-09, OR=1.7 [1.4-2.0]), and in subjects who required surgery (both CD and UC; P=3.6E-19, OR=1.7 [1.5-1.9]). Smoking increased risk of EIMs except for PSC where there was a 'protective' effect. Multiple serological associations were observed including with PSC (ANCA, ASCA, anti-CBir1) and any EIM (ANCA, ASCA, anti-I2). We identified genome-wide significant associations within MHC (AS-SI P=1.4E-15, OR=2.5 [2.0-3.1]; PSC P=2.7E-10, OR=2.8 [2.0-3.8]; ocular P=2E-08, OR=3.6 [2.3-5.6]; and overall EIM P=8.4E-09, OR=2.2 [1.7-2.9]) and CPEB4 (SKIN P=2.7E-08, OR=1.5 [1.3-1.8]). Genetic associations implicated TNF, JAK-STAT and IL6 as potential targets for EIMs. Contrary to previous reports, only 2% of our subjects had multiple EIMs and most co-occurrences were negatively correlated.
CONCLUSION CONCLUSIONS
We have identified demographic, clinical and genetic associations with EIMs that reveal underlying mechanisms and implicate novel and existing drug targets: important steps towards more personalized approach to IBD management.

Identifiants

pubmed: 38490347
pii: S0016-5085(24)00232-4
doi: 10.1053/j.gastro.2024.02.026
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

Copyright © 2024 AGA Institute. Published by Elsevier Inc. All rights reserved.

Auteurs

Michelle Khrom (M)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Millie Long (M)

Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC.

Shishir Dube (S)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Lori Robbins (L)

Palmetto Digestive Health Specialists, Charleston, SC.

Gregory J Botwin (GJ)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Shaohong Yang (S)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Emebet Mengesha (E)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Dalin Li (D)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Takeo Naito (T)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Nirupama N Bonthala (NN)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Christina Ha (C)

Inflammatory Bowel Disease Center, Cedars-Sinai Medical Center, LA, CA.

Gil Melmed (G)

Inflammatory Bowel Disease Center, Cedars-Sinai Medical Center, LA, CA.

Shervin Rabizadeh (S)

Department of Pediatrics, Pediatric Inflammatory Bowel Disease Program, Cedars-Sinai Medical Center, LA, CA.

Gaurav Syal (G)

Inflammatory Bowel Disease Center, Cedars-Sinai Medical Center, LA, CA.

Eric Vasiliauskas (E)

Inflammatory Bowel Disease Center, Cedars-Sinai Medical Center, LA, CA.

David Ziring (D)

Inflammatory Bowel Disease Center, Cedars-Sinai Medical Center, LA, CA.

Steven R Brant (SR)

Division of Gastroenterology and Hepatology, Department of Medicine, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ.

Judy Cho (J)

Icahn School of Medicine at Mount Sinai, Dr Henry D. Janowitz Division of Gastroenterology, New York, NY.

Richard H Duerr (RH)

Division of Gastroenterology, Hepatology and Nutrition, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA.

John Rioux (J)

Department of Medicine, Université de Montréal and Research Center, Montreal Heart Institute, Montréal, Québec, Canada.

Phil Schumm (P)

Department of Public Health Sciences, University of Chicago, Chicago, IL.

Mark Silverberg (M)

University of Toronto, Samuel Lunenfeld-Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada.

Ashwin N Ananthakrishnan (AN)

Gastroenterology, Massachusetts General Hospital, Boston, MA.

William A Faubion (WA)

Mayo Clinic, Rochester, MN.

Bana Jabri (B)

University of Chicago, Pritzker School of Medicine, Chicago, IL.

Sergio A Lira (SA)

Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY.

Rodney D Newberry (RD)

Department of Internal Medicine, Washington University School of Medicine, St. Louis, MO.

Robert S Sandler (RS)

Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC.

Ramnik J Xavier (RJ)

Broad Institute of MIT and Harvard, Cambridge, MA.

Subra Kugathasan (S)

Children's Healthcare of Atlanta Combined Center for Pediatric Inflammatory Bowel Disease, Atlanta, GA; Emory School of Medicine, Atlanta, GA.

David Hercules (D)

Emory School of Medicine, Atlanta, GA.

Stephan R Targan (SR)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

R Balfour Sartor (RB)

Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC.

Talin Haritunians (T)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA.

Dermot P B McGovern (DPB)

F. Widjaja Inflammatory Bowel Disease Institute, Cedars-Sinai Medical Center, LA, CA. Electronic address: Dermot.McGovern@cshs.org.

Classifications MeSH