Systemic sclerosis and primary biliary cholangitis: Longitudinal data to determine the outcomes

Gemma Lepri; Paolo Airò; Oliver Distler; Kristofer Andréasson; Yolanda Braun-Moscovici; Eric Hachulla; Alexandra Balbir-Gurman; Ellen De Langhe; Simona Rednic; Francesca Ingegnoli; Edoardo Rosato; Laura Groseanu; Ruxandra Ionescu; Silvia Bellando-Randone; Liudmila Garzanova; Lorenzo Beretta; Chiara Bellocchi; Sergey Moiseev; Pavel Novikov; Iulia Szabo; Dorota Krasowska; Veronica Codullo; Ulrich A Walker; Chrysoula Manolaraki; Serena Guiducci; Marie-Elise Truchetet; Florenzo Iannone; Lorenzo Tofani; Cosimo Bruni; Vanessa Smith; Giovanna Cuomo; Martin Krusche; Marco Matucci-Cerinic; Yannick Allanore

doi:10.1177/23971983231155948

Systemic sclerosis and primary biliary cholangitis: Longitudinal data to determine the outcomes

J Scleroderma Relat Disord. 2023 Oct;8(3):210-220. doi: 10.1177/23971983231155948. Epub 2023 Apr 4.

Authors

Gemma Lepri¹, Paolo Airò², Oliver Distler³, Kristofer Andréasson⁴, Yolanda Braun-Moscovici⁵, Eric Hachulla⁶, Alexandra Balbir-Gurman⁵, Ellen De Langhe⁷, Simona Rednic⁸, Francesca Ingegnoli⁹, Edoardo Rosato¹⁰, Laura Groseanu¹¹, Ruxandra Ionescu¹¹, Silvia Bellando-Randone¹, Liudmila Garzanova¹², Lorenzo Beretta¹³, Chiara Bellocchi¹³, Sergey Moiseev¹⁴, Pavel Novikov¹⁴, Iulia Szabo⁸, Dorota Krasowska¹⁵, Veronica Codullo¹⁶, Ulrich A Walker¹⁷, Chrysoula Manolaraki¹⁷, Serena Guiducci¹, Marie-Elise Truchetet¹⁸, Florenzo Iannone¹⁹, Lorenzo Tofani¹, Cosimo Bruni^{1

3}, Vanessa Smith²⁰, Giovanna Cuomo²¹, Martin Krusche²², Marco Matucci-Cerinic^{1

13}, Yannick Allanore²³

Affiliations

¹ Division of Rheumatology, Department of Experimental and Clinical Medicine, University of Florence, Florence, Italy.
² Rheumatology and Clinical Immunology, Spedali Civili of Brescia, Brescia, Italy.
³ Department of Rheumatology, University Hospital Zurich, University of Zurich, Zürich, Switzerland.
⁴ Section of Rheumatology, Department of Clinical Sciences, Lund University, Lund, Sweden.
⁵ Rheumatology Department, Rambam Health Care Campus, Rappaport Faculty of Medicine, Technion, Haifa, Israel.
⁶ Department of Internal Medicine, Hôpital Claude Huriez, Lille, France.
⁷ ERN ReCONNET, Division of Rheumatology, University Hospitals Leuven, Leuven, Belgium.
⁸ Department of Rheumatology, Emergency County Teaching Hospital, University of Medicine and Pharmacy Iuliu Hatieganu, Cluj-Napoca, Romania.
⁹ Clinical Rheumatology Unit, ASST Pini-CTO, Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milano, Italy.
¹⁰ Department of Translational and Precision Medicine, Sapienza University of Rome, Rome, Italy.
¹¹ Carol Davila University of Medicine and Pharmacy, Bucharest, Romania.
¹² Laboratory of Microcirculation and Inflammation, VA Nasonova Institute of Rheumatology, Moscow, Russian Federation.
¹³ Scleroderma Unit, Referral Center for Systemic Autoimmune Diseases, La Fondazione IRCCS Ca' Granda Ospedale Maggiore di Milano Policlinico, Milano, Italy.
¹⁴ Tareev Clinic of Internal Diseases, Sechenov First Moscow State Medical University, Moscow, Russian Federation.
¹⁵ Department of Dermatology, Venereology and Pediatric Dermatology, Medical University of Lublin, Lublin, Poland.
¹⁶ Rheumatology, Policlinico San Matteo, Pavia, Italy.
¹⁷ Department of Rheumatology, Universitätsspital Basel, Basel, Switzerland.
¹⁸ Rheumatology Department, Bordeaux University Hospital, Bordeaux, France.
¹⁹ Rheumatology Unit - DETO, School of Medicine, University of Bari, Bari, Italy.
²⁰ Department of Rheumatology, Ghent University Hospital and Department of Internal Medicine, Ghent University, Unit for Molecular Immunology and Inflammation, VIB Inflammation Research Center (IRC), Ghent, Belgium.
²¹ Department of Precision of Medicine, University of Campania - L. Vanvitelli, Naples, Italy.
²² Division of Rheumatology and Systemic Inflammatory Diseases, University Hospital Hamburg-Eppendorf (UKE), Hamburg, Germany.
²³ Rheumatology, Cochin Hospital, APHP, Paris Cité University, Paris, France.

PMID: 37744053
PMCID: PMC10515998 (available on 2024-10-01)
DOI: 10.1177/23971983231155948

Abstract

Background: Several studies described the cross-sectional characteristics of systemic sclerosis patients and coexisting primary biliary cholangitis, but longitudinal prognostic data are lacking.

Aims: To describe the systemic sclerosis-primary biliary cholangitis phenotype, including baseline characteristics and outcomes.

Methods: We performed a multicentre the European Scleroderma Trials and Research Group study of systemic sclerosis patients with primary biliary cholangitis or with primary biliary cholangitis-specific antibodies, matched with systemic sclerosis controls free from hepatobiliary involvement matched for disease duration and cutaneous subset. Data were recorded at baseline and at the last available visit.

Results: A total of 261 patients were enrolled (115 primary biliary cholangitis-systemic sclerosis, 161 systemic sclerosis). At baseline, systemic sclerosis-primary biliary cholangitis patients had a higher prevalence of anti-centromere antibodies (p = 0.0023) and a lower prevalence of complete absence of digital ulcers. The milder vascular involvement was confirmed at follow-up when crucial differences emerged in the percentage of patients experiencing digital ulcers; a significantly higher number of patients who never experienced digital ulcers were observed among primary biliary cholangitis-systemic sclerosis patients (p = 0.0015). Moreover, a greater incidence of pulmonary arterial hypertension (p < 0.001) and of conduction blocks (p = 0.0256) was observed in systemic sclerosis patients without primary biliary cholangitis. Patients with primary biliary cholangitis had higher levels of liver enzymes at baseline than systemic sclerosis patients; a significant decrease in liver enzymes was observed at follow-up. Out of 18 patients with cholangitis, one received a liver transplant at follow-up.

Conclusion: Our data show that systemic sclerosis-primary biliary cholangitis exhibit a mild systemic sclerosis and primary biliary cholangitis phenotype with outcomes being in general favourable.

Keywords: Systemic sclerosis; autoimmunity; fibrotic diseases; outcomes; overlap syndrome; primary biliary cholangitis.