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Patient Age, Sex, and Inflammatory Bowel Disease Phenotype Associate With Course of Primary Sclerosing Cholangitis
Open accessAbstract
Background & aims Primary sclerosing cholangitis (PSC) is an orphan hepatobiliary disorder associated with inflammatory bowel disease (IBD). We aimed to estimate the risk of disease progression based on distinct clinical phenotypes in a large international cohort of patients with PSC.Methods We performed a retrospective outcome analysis of patients diagnosed with PSC from 1980 through 2010 at 37 centers in Europe, North America, and Australia. For each patient, we collected data on sex, clinician-reported age at and date of PSC and IBD diagnoses, phenotypes of IBD and PSC, and date and indication of IBD-related surgeries. The primary and secondary endpoints were liver transplantation or death (LTD) and hepatopancreatobiliary malignancy, respectively. Cox proportional hazards models were applied to determine the effects of individual covariates on rates of clinical events, with time-to-event analysis ascertained through Kaplan-Meier estimates.Results Of the 7121 patients in the cohort, 2616 met the primary endpoint (median time to event of 14.5 years) and 721 developed hepatopancreatobiliary malignancy. The most common malignancy was cholangiocarcinoma (n = 594); patients of advanced age at diagnosis had an increased incidence compared with younger patients (incidence rate: 1.2 per 100 patient-years for patients younger than 20 years old, 6.0 per 100 patient-years for patients 21-30 years old, 9.0 per 100 patient-years for patients 31-40 years old, 14.0 per 100 patient-years for patients 41-50 years old, 15.2 per 100 patient-years for patients 51-60 years old, and 21.0 per 100 patient-years for patients older than 60 years). Of all patients with PSC studied, 65.5% were men, 89.8% had classical or large-duct disease, and 70.0% developed IBD at some point. Assessing the development of IBD as a time-dependent covariate, Crohn's disease and no IBD (both vs ulcerative colitis) were associated with a lower risk of LTD (unadjusted hazard ratio [HR], 0.62; P < .001 and HR, 0.90; P = .03, respectively) and malignancy (HR, 0.68; P = .008 and HR, 0.77; P = .004, respectively). Small-duct PSC was associated with a lower risk of LTD or malignancy compared with classic PSC (HR, 0.30 and HR, 0.15, respectively; both P < .001). Female sex was also associated with a lower risk of LTD or malignancy (HR, 0.88; P = .002 and HR, 0.68; P < .001, respectively). In multivariable analyses assessing the primary endpoint, small-duct PSC characterized a low-risk phenotype in both sexes (adjusted HR for men, 0.23; P < .001 and adjusted HR for women, 0.48; P = .003). Conversely, patients with ulcerative colitis had an increased risk of liver disease progression compared with patients with Crohn's disease (HR, 1.56; P < .001) or no IBD (HR, 1.15; P = .002).Conclusions In an analysis of data from individual patients with PSC worldwide, we found significant variation in clinical course associated with age at diagnosis, sex, and ductal and IBD subtypes. The survival estimates provided might be used to estimate risk levels for patients with PSC and select patients for clinical trials.
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In the citing paper
“The close relationship with IBD is likely relevant, as shown by variable disease behaviour depending on the clinical presentation of IBD.6,8”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“An important feature of PSC is the inherent risk of neoplasia at the affected mucosal surfaces, most commonly in the form of cholangiocarcinoma (CCA) and colorectal cancer.[5][6][7]”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“CCA is very rarely seen in patients with small duct PSC.6”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“most people with PSC have benign strictures leading to end-stage disease and will not develop hepatobiliary malignancy.6”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“Data supporting that IBD (and its inflammatory activity) is important for PSC progression is that UC, as opposed to no IBD 368 or Crohns disease, is associated with faster PSC progression.6”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“In a large, multicentre international retrospective study including 781 children and young people diagnosed with PSC, 67% fulfilled the diagnostic criteria for AIH, in contrast to 6.6% in a similar study including 7,121 adults, suggesting higher prevalence in the paediatric population.6,427”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“In the retrospective outcome analysis of patients diagnosed with PSC from 1980 through 2010 at 37 centres in Europe, North America, and Australia including 7,121 patients, the incidence of CCA in 940 patients < -20 years-old was 1.2/100 patient-years increasing with age to 21/100 patientyears for those over the age of 60. 6”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
In the citing paper
“Patients with associated UC were at higher risk of developing CCA.”
From EASL Clinical Practice Guidelines on sclerosing cholangitis (2022) · cites this paper as [6]
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Self-citation
Metadata
- Authors
- Weismüller, T. J., Trivedi, P. J., Bergquist, A., Imam, M., Lenzen, H., Ponsioen, C. Y., Holm, K., Gotthardt, D., Färkkilä, M. A., Marschall, H.-U., Thorburn, D., Weersma, R. K., Fevery, J., Mueller, T., Chazouillères, O., Schulze, K., Lazaridis, K. N., Almer, S., Pereira, S. P., Levy, C., Mason, A., Naess, S., Bowlus, C. L., Floreani, A., Halilbasic, E., Yimam, K. K., Milkiewicz, P., Beuers, U., Huynh, D. K., Pares, A., Manser, C. N., Dalekos, G. N., Eksteen, B., Invernizzi, P., Berg, C. P., Kirchner, G. I., Sarrazin, C., Zimmer, V., Fabris, L., Braun, F., Marzioni, M., Juran, B. D., Said, K., Rupp, C., Jokelainen, K., Benito de Valle, M., Saffioti, F., Cheung, A., Trauner, M., Schramm, C., Chapman, R. W., Karlsen, T. H., Schrumpf, E., Strassburg, C. P., Manns, M. P., Lindor, K. D., Hirschfield, G. M., Hansen, B. E., & Boberg, K. M.
- Affiliations
- University of Bonn (DE)
- Queen Elizabeth Hospital Birmingham (GB)
- Karolinska University Hospital (SE)
- Mayo Clinic (US)
- Medizinische Hochschule Hannover (DE)
- Amsterdam UMC Location University of Amsterdam (NL)
- Oslo University Hospital (NO)
- University Hospital Heidelberg (DE)
- University of Helsinki (FI)
- University of Gothenburg (SE)
- The Royal Free Hospital (GB)
- University Medical Center Groningen (NL)
- Universitair Ziekenhuis Leuven (BE)
- Charité – Universitätsmedizin Berlin (DE)
- Assistance Publique – Hôpitaux de Paris (FR)
- University Medical Center Hamburg-Eppendorf (DE)
- Linköping University (SE)
- University College London (GB)
- University of Miami (US)
- University of Alberta (CA)
- University of California, Davis (US)
- University of Padua (IT)
- Medical University of Vienna (AT)
- California Pacific Medical Center (US)
- Medical University of Warsaw (PL)
- Royal Adelaide Hospital (AU)
- University Hospital Zurich (CH)
- University of Calgary (CA)
- University of Milan (IT)
- University of Tübingen (DE)
- University Hospital Regensburg (DE)
- Goethe University Frankfurt (DE)
- Universitätsklinikum des Saarlandes (DE)
- University Hospital Schleswig-Holstein (DE)
- Marche Polytechnic University (IT)
- John Radcliffe Hospital (GB)
- National Institute for Health and Care Research (GB)
- University of Toronto (CA)
- Corresponding author
- Weismüller, Tobias J.
- Boberg, Kirsten M.
- ORCID
- Weismüller, Tobias J.
- Trivedi, Palak J.
- Bergquist, Annika
- Imam, Mohamad
- Lenzen, Henrike
- Ponsioen, Cyriel Y.
- Holm, Kristian
- Gotthardt, Daniel
- Färkkilä, Martti A.
- Marschall, Hanns-Ulrich
- Thorburn, Douglas
- Weersma, Rinse K.
- Fevery, Johan
- Mueller, Tobias
- Chazouillères, Olivier
- Schulze, Kornelius
- Lazaridis, Konstantinos N.
- Almer, Sven
- Pereira, Stephen P.
- Levy, Cynthia
- Mason, Andrew
- Bowlus, Christopher L.
- Floreani, Annarosa
- Halilbasic, Emina
- Milkiewicz, Piotr
- Beuers, Ulrich
- Eksteen, Bertus
- Invernizzi, Pietro
- Berg, Christoph P.
- Zimmer, Vincent
- Fabris, Luca
- Braun, Felix
- Marzioni, Marco
- Said, Karouk
- Rupp, Christian
- Saffioti, Francesca
- Cheung, Angela
- Trauner, Michael
- Schramm, Christoph
- Chapman, Roger W.
- Karlsen, Tom H.
- Strassburg, Christian P.
- Manns, Michael P.
- Lindor, Keith D.
- Hirschfield, Gideon M.
- Hansen, Bettina E.
- Boberg, Kirsten M.
- Venue
- Gastroenterology
- Publisher
- Elsevier BV
- Published
- 2017-06
- Volume
- 152
- Issue
- 8
- Pages
- 1975-1984.e8
- ISSN
- 0016-5085 (ISSN-L)
- PMC
- PMC5546611
- OpenAlex
- W2594589478
- Cited by
- 533
- References
- 74
- Citations by year
- 2026: 49 · 2025: 58 · 2024: 60 · 2023: 65 · 2022: 59 · 2021: 68 · 2020: 55 · 2019: 43 · 2018: 49 · 2017: 24
- FWCI
- 28.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Gastroenterology (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- BOA (University of Milano-Bicocca) (submittedVersion, other-oa)
- Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, cc-by-nc-nd)
- UCL Discovery (University College London) (submittedVersion)
- University of Regensburg Publication Server (University of Regensburg) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Työväentutkimus Vuosikirja (submittedVersion, other-oa)
- University of Thessaly Institutional Repository (University of Thessaly) (submittedVersion)
- Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by-nc-nd)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Funders
- Wellcome Trust
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK084960)
- Topics
- Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Health Sciences › Medicine › Surgery › Pediatric Hepatobiliary Diseases and Treatments
- Keywords
- primary sclerosing cholangitis, inflammatory bowel disease, cholangiocarcinoma, liver transplantation, disease progression, age at diagnosis, sex differences, Crohn's disease, ulcerative colitis, IBD surgery, mortality
- MeSH terms
- Adult, Australia, Colitis, Ulcerative, Crohn Disease, Europe, Female, Humans, Male, Middle Aged, North America, Phenotype, Prognosis, Retrospective Studies, Risk Factors, Time Factors, Cholangitis, Sclerosing, Incidence, Multivariate Analysis, Chi-Square Distribution, Proportional Hazards Models, Liver Transplantation, Age Distribution, Sex Distribution, Disease Progression, Risk Assessment, Kaplan-Meier Estimate, Young Adult
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