Long-term outcomes of pediatric-onset primary sclerosing cholangitis: A single-center experience in Japan.

autoimmune hepatitis autoimmune sclerosing cholangitis inflammatory bowel disease liver transplantation overlap syndrome

Journal

Hepatology research : the official journal of the Japan Society of Hepatology
ISSN: 1386-6346
Titre abrégé: Hepatol Res
Pays: Netherlands
ID NLM: 9711801

Informations de publication

Date de publication:
Dec 2019
Historique:
received: 15 03 2019
revised: 27 07 2019
accepted: 05 08 2019
pubmed: 14 8 2019
medline: 14 8 2019
entrez: 14 8 2019
Statut: ppublish

Résumé

Primary sclerosing cholangitis (PSC) is very rare in Japan. Although a large-scale cohort study of 781 pediatric-onset PSC patients in Europe and North America showed that the 5-year survival with native liver was 88%, the long-term outcomes of pediatric-onset PSC in Japan are unknown. Here, we evaluated the clinical outcomes of pediatric-onset PSC in Japan. We carried out a retrospective cohort study with a medical records review of pediatric PSC patients diagnosed between 1986 and 2017 at a single center. The PSC diagnoses were based on cholangiography, liver histology, and biochemical findings. The patients' survival was analyzed using the Kaplan-Meier method. Prognostic factors were determined by univariate and multivariate analyses using the Cox proportional hazards regression model. We identified 39 pediatric-onset PSC patients (22 boys, 17 girls). The median age at diagnosis was 9 years (interquartile range 6.0-13.5 years). The median follow-up period was 5.5 years (interquartile range 3.4-8.7 years). The phenotypes of PSC-autoimmune hepatitis, PSC-inflammatory bowel disease, and small-duct PSC were diagnosed in 13 (33.3%), 36 out of 38 (94.8%), and three (7.7%) patients, respectively. The 5-year liver transplantation-free survival of the whole cohort was 93.5%. Nine patients underwent liver transplantation, and four of these nine cases resulted in death. Both the univariate and multivariate analyses showed that the phenotype of "PSC-autoimmune hepatitis overlap" was an independent poor prognostic factor. The overall survival of pediatric-onset PSC in Japan was comparable to those in Western countries. The phenotype of PSC-autoimmune hepatitis was identified as a prognostic factor associated with a poorer long-term outcome.

Identifiants

pubmed: 31408920
doi: 10.1111/hepr.13421
doi:

Types de publication

Journal Article

Langues

eng

Pagination

1386-1397

Informations de copyright

© 2019 The Japan Society of Hepatology.

Références

Hirschfield GM, Karlsen TH, Lindor KD, Adams DH. Primary sclerosing cholangitis. Lancet 2013; 382: 1587-1599.
Chapman R, Fevery J, Kalloo A et al. Diagnosis and management of primary sclerosing cholangitis. Hepatology 2010; 51: 660-678.
Lindor KD, Kowdley KV, Harrison ME. American College of G. ACG Clinical Guideline: Primary Sclerosing Cholangitis. Am J Gastroenterol 2015; 110: 646-659.
Deneau M, Jensen MK, Holmen J, Williams MS, Book LS, Guthery SL. Primary sclerosing cholangitis, autoimmune hepatitis, and overlap in Utah children: Epidemiology and natural history. Hepatology 2013; 58: 1392-1400.
Weismuller TJ, Trivedi PJ, Bergquist A et al. Patient age, sex, and inflammatory bowel disease phenotype associate with course of primary sclerosing cholangitis. Gastroenterology 2017; 152: 1975-1984.
Loftus EV Jr, Harewood GC, Loftus CG et al. PSC-IBD: A unique form of inflammatory bowel disease associated with primary sclerosing cholangitis. Gut 2005; 54: 91-96.
Nakazawa T, Naitoh I, Hayashi K et al. Inflammatory bowel disease of primary sclerosing cholangitis: A distinct entity? World J Gastroenterol 2014; 28(20): 3245-3254.
Jorgensen KK, Grzyb K, Lundin KE et al. Inflammatory bowel disease in patients with primary sclerosing cholangitis: Clinical characterization in liver transplanted and nontransplanted patients. Inflamm Bowel Dis 2012; 18: 536-545.
Fevery J, Van Steenbergen W, Van Pelt J et al. Patients with large-duct primary sclerosing cholangitis and Crohn's disease have a better outcome than those with ulcerative colitis, or without IBD. Aliment Pharmacol Ther 2016; 43: 612-620.
Ricciuto A, Fish J, Carman N et al. Symptoms do not correlate with findings from colonoscopy in children with inflammatory bowel disease and primary sclerosing cholangitis. Clin Gastroenterol Hepatol 2018; 16: 1098-1105.
Gregorio GV, Portmann B, Karani J et al. Autoimmune hepatitis/sclerosing cholangitis overlap syndrome in childhood: A 16-year prospective study. Hepatology 2001; 33: 544-553.
Feldstein AE, Perrault J, El-Youssif M, Lindor KD, Freese DK, Angulo P. Primary sclerosing cholangitis in children: A long-term follow-up study. Hepatology 2003; 38: 210-217.
Miloh T, Arnon R, Shneider B, Suchy F, Kerkar N. A retrospective single-center review of primary sclerosing cholangitis in children. Clin Gastroenterol Hepatol 2009; 7: 239-245.
Tenca A, Farkkila M, Arola J, Jaakkola T, Penagini R, Kolho KL. Clinical course and prognosis of pediatric-onset primary sclerosing cholangitis. United European Gastroenterol J 2016; 4: 562-569.
Rodrigues AT, Liu PM, Fagundes ED et al. Clinical characteristics and prognosis in children and adolescents with autoimmune hepatitis and overlap syndrome. J Pediatr Gastroenterol Nutr 2016; 63: 76-81.
Valentino PL, Wiggins S, Harney S, Raza R, Lee CK, Jonas MM. The natural history of primary sclerosing cholangitis in children: A large single-center longitudinal cohort study. J Pediatr Gastroenterol Nutr 2016; 63: 603-609.
Deneau MR, El-Matary W, Valentino PL et al. The natural history of primary sclerosing cholangitis in 781 children: A multicenter, international collaboration. Hepatology 2017; 66: 518-527.
Karlsen TH, Boberg KM. Update on primary sclerosing cholangitis. J Hepatol 2013; 59: 571-582.
Boonstra K, Beuers U, Ponsioen CY. Epidemiology of primary sclerosing cholangitis and primary biliary cirrhosis: A systematic review. J Hepatol 2012; 56: 1181-1188.
Lee WS, Lum SH, Lim CB et al. Characteristics and outcome of autoimmune liver disease in Asian children. Hepatol Int 2015; 9: 292-302.
Yoon J, Oh SH, Kim HJ et al. Primary sclerosing cholangitis with inflammatory bowel disease in Korean children. Pediatr Gastroenterol Hepatol Nutr 2015; 18: 268-275.
Umetsu S, Inui A, Sogo T, Komatsu H, Fujisawa T. Usefulness of serum Wisteria floribunda agglutinin-positive Mac-2 binding protein in children with primary sclerosing cholangitis. Hepatol Res 2018; 48: 355-363.
Tanaka A, Tazuma S, Okazaki K, Tsubouchi H, Inui K, Takikawa H. Nationwide survey for primary sclerosing cholangitis and IgG4-related sclerosing cholangitis in Japan. J Hepatobiliary Pancreat Sci 2014; 21: 43-50.
Takikawa H, Manabe T. Primary sclerosing cholangitis in Japan--Analysis of 192 cases. J Gastroenterol 1997; 32: 134-137.
Takikawa H, Takamori Y, Tanaka A, Kurihara H, Nakanuma Y. Analysis of 388 cases of primary sclerosing cholangitis in Japan; Presence of a subgroup without pancreatic involvement in older patients. Hepatol Res 2004; 29: 153-159.
Eaton JE, Talwalkar JA, Lazaridis KN, Gores GJ, Lindor KD. Pathogenesis of primary sclerosing cholangitis and advances in diagnosis and management. Gastroenterology 2013; 145: 521-536.
Kaplan GG, Laupland KB, Butzner D, Urbanski SJ, Lee SS. The burden of large and small duct primary sclerosing cholangitis in adults and children: A population-based analysis. Am J Gastroenterol 2007; 102: 1042-1049.
Czaja AJ. The overlap syndromes of autoimmune hepatitis. Dig Dis Sci 2013; 58: 326-343.
Czaja AJ, Carpenter HA. Autoimmune hepatitis overlap syndromes and liver pathology. Gastroenterol Clin North Am 2017; 46: 345-364.
Wai CT, Greenson JK, Fontana RJ et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology 2003; 38: 518-526.
Kim WR, Therneau TM, Wiesner RH et al. A revised natural history model for primary sclerosing cholangitis. Mayo Clin Proc 2000 Jul; 75: 688-694.
Ludwig J, Batts KP. Practical liver biopsy interpretation: Diagnostic algorithms, 2nd edn. ASCP Press, 1998.
Levine A, Koletzko S, Turner D et al. ESPGHAN revised porto criteria for the diagnosis of inflammatory bowel disease in children and adolescents. J Pediatr Gastroenterol Nutr 2014; 58: 795-806.
Lindor KD, Kowdley KV, Luketic VA et al. High-dose ursodeoxycholic acid for the treatment of primary sclerosing cholangitis. Hepatology 2009; 50: 808-814.
Imam MH, Sinakos E, Gossard AA et al. High-dose ursodeoxycholic acid increases risk of adverse outcomes in patients with early stage primary sclerosing cholangitis. Aliment Pharmacol Ther 2011; 34: 1185-1192.
Triantos CK, Koukias NM, Nikolopoulou VN, Burroughs AK. Meta-analysis: Ursodeoxycholic acid for primary sclerosing cholangitis. Aliment Pharmacol Ther 2011; 34: 901-910.
Sogo T, Fujisawa T, Inui A et al. Intravenous methylprednisolone pulse therapy for children with autoimmune hepatitis. Hepatol Res 2006; 34: 187-192.
Tanaka A, Takamori Y, Toda G, Ohnishi S, Takikawa H. Outcome and prognostic factors of 391 Japanese patients with primary sclerosing cholangitis. Liver Int 2008; 28: 983-989.
de Ledinghen V, Le Bail B, Rebouissoux L et al. Liver stiffness measurement in children using FibroScan: Feasibility study and comparison with Fibrotest, aspartate transaminase to platelets ratio index, and liver biopsy. J Pediatr Gastroenterol Nutr 2007; 45: 443-450.
Lindstrom L, Hultcrantz R, Boberg KM, Friis-Liby I, Bergquist A. Association between reduced levels of alkaline phosphatase and survival times of patients with primary sclerosing cholangitis. Clin Gastroenterol Hepatol 2013; 11: 841-846.
Rupp C, Rossler A, Halibasic E et al. Reduction in alkaline phosphatase is associated with longer survival in primary sclerosing cholangitis, independent of dominant stenosis. Aliment Pharmacol Ther 2014; 40: 1292-1301.
Ponsioen CY, Chapman RW, Chazouilleres O et al. Surrogate endpoints for clinical trials in primary sclerosing cholangitis: Review and results from an International PSC Study Group consensus process. Hepatology 2016; 63: 1357-1367.
Floreani A, Rizzotto ER, Ferrara F et al. Clinical course and outcome of autoimmune hepatitis/primary sclerosing cholangitis overlap syndrome. Am J Gastroenterol 2005; 100: 1516-1522.
Al-Chalabi T, Portmann BC, Bernal W, McFarlane IG, Heneghan MA. Autoimmune hepatitis overlap syndromes: An evaluation of treatment response, long-term outcome and survival. Aliment Pharmacol Ther 2008; 28: 209-220.
Tanaka A, Takikawa H. Geoepidemiology of primary sclerosing cholangitis: A critical review. J Autoimmun 2013; 46: 35-40.
Zolfino T, Heneghan MA, Norris S, Harrison PM, Portmann BC, McFarlane IG. Characteristics of autoimmune hepatitis in patients who are not of European Caucasoid ethnic origin. Gut 2002; 50: 713-717.
Miyagawa-Hayashino A, Egawa H, Yoshizawa A et al. Frequent overlap of active hepatitis in recurrent primary sclerosing cholangitis after living-donor liver transplantation relates to its rapidly progressive course. Hum Pathol 2011; 42: 1329-1336.
Karlsen TH, Folseraas T, Thorburn D, Vesterhus M. Primary sclerosing cholangitis - A comprehensive review. J Hepatol 2017; 67: 1298-1323.
Sabino J, Vieira-Silva S, Machiels K et al. Primary sclerosing cholangitis is characterised by intestinal dysbiosis independent from IBD. Gut 2016; 65: 1681-1689.
Iwasawa K, Suda W, Tsunoda T et al. Characterisation of the faecal microbiota in Japanese patients with paediatric-onset primary sclerosing cholangitis. Gut 2017; 66: 1344-1346.
Boberg KM, Chapman RW, Hirschfield GM et al. Overlap syndromes: The International Autoimmune Hepatitis Group (IAIHG) position statement on a controversial issue. J Hepatol 2011; 54: 374-385.
Gatselis NK, Zachou K, Papamichalis P et al. Comparison of simplified score with the revised original score for the diagnosis of autoimmune hepatitis: A new or a complementary diagnostic score? Dig Liver Dis 2010; 42: 807-812.
Hiejima E, Komatsu H, Sogo T, Inui A, Fujisawa T. Utility of simplified criteria for the diagnosis of autoimmune hepatitis in children. J Pediatr Gastroenterol Nutr 2011; 52: 470-473.
Mieli-Vergani G, Vergani D, Baumann U et al. Diagnosis and management of pediatric autoimmune liver disease: ESPGHAN Hepatology Committee Position Statement. J Pediatr Gastroenterol Nutr 2018; 66: 345-360.
Sogo T, Takahashi A, Inui A, Fujisawa T, Ohira H, Takikawa H. Clinical features of pediatric autoimmune hepatitis in Japan: A nationwide survey. Hepatol Res 2018; 48: 286-294.

Auteurs

Shuichiro Umetsu (S)

Department of Pediatric Hepatology and Gastroenterology, Saiseikai Yokohama-shi Tobu Hospital, Yokohama, Japan.
Department of Hepatology and Gastroenterology for Growth and Health, Toho University Graduate School of Medicine, Tokyo, Japan.

Kenji Notohara (K)

Department of Anatomic Pathology, Kurashiki Central Hospital, Kurashiki, Japan.

Takahiro Nakazawa (T)

Department of Gastroenterology, Japanese Red Cross Nagoya Daini Hospital, Nagoya, Japan.

Tomoyuki Tsunoda (T)

Department of Pediatric Hepatology and Gastroenterology, Saiseikai Yokohama-shi Tobu Hospital, Yokohama, Japan.

Tsuyoshi Sogo (T)

Department of Pediatric Hepatology and Gastroenterology, Saiseikai Yokohama-shi Tobu Hospital, Yokohama, Japan.

Haruki Komatsu (H)

Department of Pediatrics, Toho University Sakura Hospital, Sakura, Japan.

Atsushi Tanaka (A)

Department of Medicine, Teikyo University School of Medicine, Tokyo, Japan.

Susumu Tazuma (S)

Department of General Medicine, Hiroshima University Graduate School of Medical Science, Programs of Applied Medicine, Clinical Pharmacotherapy, Hiroshima, Japan.

Hajime Takikawa (H)

Department of Medicine, Teikyo University School of Medicine, Tokyo, Japan.

Ayano Inui (A)

Department of Pediatric Hepatology and Gastroenterology, Saiseikai Yokohama-shi Tobu Hospital, Yokohama, Japan.
Department of Hepatology and Gastroenterology for Growth and Health, Toho University Graduate School of Medicine, Tokyo, Japan.

Tomoo Fujisawa (T)

Department of Pediatric Hepatology and Gastroenterology, Saiseikai Yokohama-shi Tobu Hospital, Yokohama, Japan.

Classifications MeSH