{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,12]],"date-time":"2026-05-12T22:22:04Z","timestamp":1778624524816,"version":"3.51.4"},"reference-count":46,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2022,6,30]],"date-time":"2022-06-30T00:00:00Z","timestamp":1656547200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"University of Medicine and Pharmacy of Craiova, Romania"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Data about the association between primary sclerosing cholangitis (PSC) and metabolic bone disease are still unclear. PSC is a chronic cholestatic liver disease (CCLD) which affects the biliary tract, and it has a highly variable natural history. We systematically searched until 28 February 2022 MEDLINE, Cochrane Central Register of Controlled Trials, the ISI Web of Science, and SCOPUS, for studies in patients with PSC. We identified 343 references to potential studies. After screening them, we included eight studies (893 PSC patients, 398 primary biliary cirrhosis (PBC) patients, and 673 healthy controls) for the present meta-analysis. Pooled analyses found no difference in BMD-LS (Z = 0.02, p-value = 0.98) between PSC patients and healthy controls. BMD-LS was statistically lower in PBC patients than in PSC patients (Mean Difference, MD, 0.06, 95% CI 0.03 to 0.09, p-value = 0.0007). The lumbar spine T-score was higher in the PSC patients compared with PBC patients (MD 0.23, 95% CI 0.04 to 0.42, p-value = 0.02). Given the limited literature available, better designed, and larger scale primary studies will be required to confirm our conclusion.<\/jats:p>","DOI":"10.3390\/jcm11133807","type":"journal-article","created":{"date-parts":[[2022,7,1]],"date-time":"2022-07-01T00:21:50Z","timestamp":1656634910000},"page":"3807","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["A Systematic Review and Meta-Analysis on Metabolic Bone Disease in Patients with Primary Sclerosing Cholangitis"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5675-1741","authenticated-orcid":false,"given":"Claudiu Marinel","family":"Ionele","sequence":"first","affiliation":[{"name":"Doctoral School, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1374-276X","authenticated-orcid":false,"given":"Adina","family":"Turcu-Stiolica","sequence":"additional","affiliation":[{"name":"Department of Pharmacoeconomics, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mihaela Simona","family":"Subtirelu","sequence":"additional","affiliation":[{"name":"Department of Pharmacoeconomics, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bogdan Silviu","family":"Ungureanu","sequence":"additional","affiliation":[{"name":"Research Center of Gastroenterology and Hepatology, University of Medicine and Pharmacy of Craiova, 200638 Craiova, Romania"},{"name":"Department of Gastroenterology, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"George Ovidiu","family":"Cioroianu","sequence":"additional","affiliation":[{"name":"Doctoral School, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ion","family":"Rogoveanu","sequence":"additional","affiliation":[{"name":"Research Center of Gastroenterology and Hepatology, University of Medicine and Pharmacy of Craiova, 200638 Craiova, Romania"},{"name":"Department of Gastroenterology, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,6,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1587","DOI":"10.1016\/S0140-6736(13)60096-3","article-title":"Primary sclerosing cholangitis","volume":"382","author":"Hirschfield","year":"2013","journal-title":"Lancet"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1097\/00054725-200501000-00009","article-title":"Primary sclerosing cholangitis","volume":"11","author":"Talwalkar","year":"2005","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1053\/jhep.2001.20533","article-title":"Hepatic osteodystrophy","volume":"33","author":"Rouillard","year":"2001","journal-title":"Hepatology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/S0168-8278(00)80061-6","article-title":"Serum autoantibodies in patients with primary sclerosing cholangitis","volume":"32","author":"Angulo","year":"2000","journal-title":"J. Hepatol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3781","DOI":"10.3748\/wjg.14.3781","article-title":"Autoantibodies in primary sclerosing cholangitis","volume":"14","author":"Hov","year":"2008","journal-title":"World J. Gastroenterol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"S123","DOI":"10.1016\/S0168-8278(20)31043-6","article-title":"Projection of liver transplant activity per indication in France and United Kingdom","volume":"73","author":"Connolly","year":"2020","journal-title":"J. Hepatol."},{"key":"ref_7","first-page":"e19922","article-title":"Risk of hepatobiliary-gastrointestinal malignancies and appropriate cancer surveillance in patients with primary sclerosing cholangitis","volume":"13","author":"Yadlapati","year":"2021","journal-title":"Cureus"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1016\/0016-5085(94)90227-5","article-title":"Low bone mineral density in Crohn\u2019s disease, but not in ulcerative colitis, at diagnosis","volume":"107","author":"Ghosh","year":"1994","journal-title":"Gastroenterology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"300","DOI":"10.4254\/wjh.v3.i12.300","article-title":"Hepatic osteodystrophy: An important matter for consideration in chronic liver disease","volume":"3","author":"Lucendo","year":"2011","journal-title":"World J. Hepatol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1111\/cen.12780","article-title":"The risk of osteoporosis in patients with liver cirrhosis: A meta-analysis of literature studies","volume":"84","author":"Lupoli","year":"2016","journal-title":"Clin. Endocrinol."},{"key":"ref_11","first-page":"OC31","article-title":"Study of Hepatic Osteodystrophy in Patients with Chronic Liver Disease","volume":"10","author":"Karoli","year":"2016","journal-title":"J. Clin. Diagn. Res."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"818","DOI":"10.52312\/jdrs.2021.25","article-title":"Common musculoskeletal disorders in chronic liver disease patients","volume":"32","author":"Ranjan","year":"2021","journal-title":"Jt. Dis. Relat. Surg."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1136\/gut.46.2.176","article-title":"Fracture risk is increased in Crohn\u2019s disease, but not in ulcerative colitis","volume":"46","author":"Vestergaard","year":"2000","journal-title":"Gut"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1111\/jgh.13746","article-title":"Risk of secondary osteoporosis due to lobular cholestasis in non-cirrhotic primary biliary cholangitis","volume":"32","author":"Seki","year":"2017","journal-title":"J. Gastroenterol. Hepatol."},{"key":"ref_15","first-page":"1397","article-title":"Osteoporosis in patients with primary biliary cirrhosis","volume":"22","author":"Wariaghli","year":"2010","journal-title":"Eur. J. Gastroenterol. Hepatol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.jhep.2004.11.035","article-title":"Severity of cholestasis and advanced histological stage but not menopausal status are the major risk factors for osteoporosis in primary biliary cirrhosis","volume":"42","author":"Ros","year":"2005","journal-title":"J. Hepatol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1007\/s00296-009-1071-8","article-title":"Osteoporosis in chronic liver disease: A case-control study","volume":"30","author":"Wariaghli","year":"2010","journal-title":"Rheumatol. Int."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1111\/j.1478-3231.2005.01075.x","article-title":"Severity of liver disease does not predict osteopenia or low bone mineral density in primary sclerosing cholangitis","volume":"25","author":"Campbell","year":"2005","journal-title":"Liver Int."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1053\/j.gastro.2010.10.014","article-title":"Bone disease in patients with primary sclerosing cholangitis","volume":"140","author":"Angulo","year":"2011","journal-title":"Gastroenterology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/S0140-6736(18)32112-3","article-title":"Osteoporosis","volume":"393","author":"Compston","year":"2019","journal-title":"Lancet"},{"key":"ref_21","first-page":"92","article-title":"Osteoporosis: A review of treatment options","volume":"43","author":"Tu","year":"2018","journal-title":"Pharm. Ther."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1595","DOI":"10.1210\/jc.2019-00221","article-title":"Pharmacological management of osteoporosis in postmenopausal women: An endocrine society* clinical practice guideline","volume":"104","author":"Eastell","year":"2019","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.jocd.2019.01.004","article-title":"Bone health in patients with liver diseases","volume":"23","author":"Danford","year":"2020","journal-title":"J. Clin. Densitom."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"n71","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 statement: An updated guideline for reporting systematic reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"ref_25","unstructured":"Wells, G., Shea, B., O\u2019Connell, D., Peterson, J., Welch, V., Losos, M., and Tugwel, P. (2022, January 21). The Newcastle Ottawa Scale (NOS) for Assessing the Quality of Nonrandomized Studies in Meta-Analyses; 2011. Available online: http:\/\/www.ohri.ca\/programs\/clinical_epidemiology\/oxford.asp."},{"key":"ref_26","first-page":"1","article-title":"Closing the quality gap: Revisiting the state of the science (vol. 3: Quality improvement interventions to address health disparities)","volume":"208.3","author":"McPheeters","year":"2012","journal-title":"Evid. Rep. Technol. Assess"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v036.i03","article-title":"Conducting Meta-Analyses in R with the Metafor Package","volume":"36","author":"Viechtbauer","year":"2010","journal-title":"J. Stat. Softw."},{"key":"ref_28","first-page":"1","article-title":"Biological variation of laboratory analytes based on the 1999-2002 National Health and Nutrition Examination Survey","volume":"21","author":"Lacher","year":"2010","journal-title":"Natl. Health Stat. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1016\/S0168-8278(98)80253-5","article-title":"Bone disease in patients with primary sclerosing cholangitis: Prevalence, severity and prediction of progression","volume":"29","author":"Angulo","year":"1998","journal-title":"J. Hepatol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1390","DOI":"10.1002\/lt.20874","article-title":"Bone mineral density before and after OLT: Long-term follow-up and predictive factors","volume":"12","author":"Guichelaar","year":"2006","journal-title":"Liver. Transplant."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1002\/hep.1840140209","article-title":"The metabolic bone disease of primary sclerosing cholangitis","volume":"14","author":"Hay","year":"1991","journal-title":"Hepatology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1007\/s11604-016-0573-z","article-title":"Diffusion-weighted MRI for detection of hepatic osteodystrophy in primary sclerosing cholangitis: A comparison study with dual-energy X-ray absorptiometry","volume":"34","author":"Keller","year":"2016","journal-title":"Jpn. J. Radiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1016\/j.jhep.2018.12.035","article-title":"Th17 cell frequency is associated with low bone mass in primary sclerosing cholangitis","volume":"70","author":"Schmidt","year":"2019","journal-title":"J. Hepatol."},{"key":"ref_34","first-page":"e25539","article-title":"The impact of fragility fractures on health-related quality of life in patients with primary sclerosing cholangitis","volume":"15","author":"Kucharski","year":"2015","journal-title":"Hepat. Mon."},{"key":"ref_35","unstructured":"(2022, January 21). The National Institutes of Health (NIH) Consensus Development Program: Osteoporosis Prevention, Diagnosis, and Therapy, Available online: https:\/\/consensus.nih.gov\/2000\/2000osteoporosis111html.htm."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3516","DOI":"10.3748\/wjg.15.3516","article-title":"Bone mineral density and disorders of mineral metabolism in chronic liver disease","volume":"15","author":"George","year":"2009","journal-title":"World J. Gastroenterol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1002\/hep.23294","article-title":"American Association for the Study of Liver Diseases. Diagnosis and management of primary sclerosing cholangitis","volume":"51","author":"Chapman","year":"2010","journal-title":"Hepatology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2581","DOI":"10.1172\/JCI117959","article-title":"Role of hyperbilirubinemia in the impairment of osteoblast proliferation associated with cholestatic jaundice","volume":"95","author":"Janes","year":"1995","journal-title":"J. Clin. Investig."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s10354-008-0594-z","article-title":"Cholestasis and metabolic bone disease\u2014A clinical review","volume":"158","author":"Gasser","year":"2008","journal-title":"Wien. Med. Wochenschr."},{"key":"ref_40","first-page":"185","article-title":"Hepatic osteodystrophy","volume":"11","author":"Gatta","year":"2014","journal-title":"Clin. Cases Miner. Bone Metab."},{"key":"ref_41","first-page":"305","article-title":"Osteocalcin and bone alkaline phosphatase in the serum of women with liver disease","volume":"21","author":"Steinberg","year":"1991","journal-title":"Ann. Clin. Lab. Sci."},{"key":"ref_42","first-page":"1462","article-title":"Bone disease in liver transplant recipients: Incidence, timing, and risk factors","volume":"23","author":"Porayko","year":"1991","journal-title":"Transplant. Proc."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1002\/hep.1840140215","article-title":"Rates of vertebral bone loss before and after liver transplantation in women with primary biliary cirrhosis","volume":"14","author":"Eastell","year":"1991","journal-title":"Hepatology"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1867","DOI":"10.1111\/liv.13110","article-title":"Alkaline phosphatase at diagnosis of primary sclerosing cholangitis and 1 year later: Evaluation of prognostic value","volume":"36","author":"Wang","year":"2016","journal-title":"Liver Int."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1356","DOI":"10.1136\/gutjnl-2018-317993","article-title":"British Society of Gastroenterology and UK-PSC guidelines for the diagnosis and management of primary sclerosing cholangitis","volume":"68","author":"Chapman","year":"2019","journal-title":"Gut"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"s1","DOI":"10.1136\/gutjnl-2019-318484","article-title":"British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults","volume":"68","author":"Lamb","year":"2019","journal-title":"Gut"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/13\/3807\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:41:22Z","timestamp":1760139682000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/13\/3807"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,6,30]]},"references-count":46,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["jcm11133807"],"URL":"https:\/\/doi.org\/10.3390\/jcm11133807","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,6,30]]}}}