Review article: safety of new biologic agents for inflammatory bowel disease in the liver.
Journal
European journal of gastroenterology & hepatology
ISSN: 1473-5687
Titre abrégé: Eur J Gastroenterol Hepatol
Pays: England
ID NLM: 9000874
Informations de publication
Date de publication:
01 05 2021
01 05 2021
Historique:
pubmed:
21
1
2021
medline:
10
8
2021
entrez:
20
1
2021
Statut:
ppublish
Résumé
New biologic agents (vedolizumab, ustekinumab and tofacitinib) represent an effective treatment for inflammatory bowel diseases and have been recently approved. However, with a rapidly evolving complement of advanced targeted therapies, new concerns about their potentially undesirable effects on liver function emerge. In particular, little is known about safety data in patients with hepatitis B virus, hepatitis C virus chronic infections, cirrhosis and in transplanted patients who are accumulating. In addition, these new agents have also been associated with drug-induced liver injury. Limited data on the efficacy of vedolizumab in patients with primary sclerosing cholangitis are also available. This article reviews available data about hepatic safety concerns in patients receiving vedolizumab, ustekinumab and tofacitinib with and without preexistent hepatic diseases.
Identifiants
pubmed: 33470695
doi: 10.1097/MEG.0000000000002076
pii: 00042737-202105000-00004
doi:
Substances chimiques
Biological Factors
0
Ustekinumab
FU77B4U5Z0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
623-630Commentaires et corrections
Type : CommentIn
Informations de copyright
Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.
Références
Miehsler W, Novacek G, Wenzl H, Vogelsang H, Knoflach P, Kaser A, et al.; Austrian Society of Gastroenterology and Hepatology. A decade of infliximab: the Austrian evidence based consensus on the safe use of infliximab in inflammatory bowel disease. J Crohns Colitis. 2010; 4:221–256.
Ford AC, Khan KJ, Sandborn WJ, Kane SV, Moayyedi P. Once-daily dosing vs. conventional dosing schedule of mesalamine and relapse of quiescent ulcerative colitis: systematic review and meta-analysis. Am J Gastroenterol. 2011; 106:2070–7; quiz 2078.
Yanai H, Hanauer SB. Assessing response and loss of response to biological therapies in IBD. Am J Gastroenterol. 2011; 106:685–698.
Yanai H, Lichtenstein L, Assa A, Mazor Y, Weiss B, Levine A, et al. Levels of drug and antidrug antibodies are associated with outcome of interventions after loss of response to infliximab or adalimumab. Clin Gastroenterol Hepatol. 2015; 13:522–530.e2.
Danese S, Vuitton L, Peyrin-Biroulet L. Biologic agents for IBD: practical insights. Nat Rev Gastroenterol Hepatol. 2015; 12:537–545.
Papa A, Mocci G, Bonizzi M, Felice C, Andrisani G, De Vitis I, et al. Use of infliximab in particular clinical settings: management based on current evidence. Am J Gastroenterol. 2009; 104:1575–1586.
Rossi RE, Parisi I, Despott EJ, Burroughs AK, O’Beirne J, Conte D, et al. Anti-tumour necrosis factor agent and liver injury: literature review, recommendations for management. World J Gastroenterol. 2014; 20:17352–17359.
Feagan BG, Rutgeerts P, Sands BE, Hanauer S, Colombel JF, Sandborn WJ, et al.; GEMINI 1 Study Group. Vedolizumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2013; 369:699–710.
Sandborn WJ, Feagan BG, Rutgeerts P, Hanauer S, Colombel JF, Sands BE, et al.; GEMINI 2 Study Group. Vedolizumab as induction and maintenance therapy for Crohn’s disease. N Engl J Med. 2013; 369:711–721.
European Medicines Agency. Entyvio - Vedolizumab. Agencia Europea de Medicamentos; 2014. doi: 10.1158/0008-5472.SABCS12-S5-3
Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ. Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet. 2015; 386:1546–1555.
Naghavi M, Wang H, Lozano R, Davis A, Liang X, Zhou M, et al. Global, regional, and national age-sex specific all-cause and cause-specific mortality for 240 causes of death, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015; 385:117–171.
Biancone L, Pavia M, Del Vecchio Blanco G, D’Incà R, Castiglione F, De Nigris F, et al.; Italian Group for the Study of the Colon and Rectum (GISC). Hepatitis B and C virus infection in Crohn’s disease. Inflamm Bowel Dis. 2001; 7:287–294.
Papa A, Felice C, Marzo M, Andrisani G, Armuzzi A, Covino M, et al. Prevalence and natural history of hepatitis B and C infections in a large population of IBD patients treated with anti-tumor necrosis factor-α agents. J Crohns Colitis. 2013; 7:113–119.
Lampertico P, Agarwal K, Berg T, Buti M, Janssen HLA, Papatheodoridis G, et al. EASL 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection. J Hepatol. 2017; 67:370–398.
Lanini S, Easterbrook PJ, Zumla A, Ippolito G. Hepatitis C: global epidemiology and strategies for control. Clin Microbiol Infect. 2016; 22:833–838.
Blach S, Zeuzem S, Manns M, Altraif I, Duberg AS, Muljono DH, et al. Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study. Lancet Gastroenterol Hepatol. 2017; 2:161–176.
Lee J, Conniff J, Kraus C, Schrager S. A brief clinical update on hepatitis C—the essentials. Wis Med J. 2015; 114:263–269.
Pawlotsky JM, Negro F, Aghemo A, Berenguer M, Dalgard O, Dusheiko G, et al. EASL recommendations on treatment of hepatitis C 2018. J Hepatol. 2018; 69:461–511.
EASL. European Association for the Study of the Liver (EASL) 2017 Clinical Practice Guidelines on the management of hepatitis B virus infection. J Hepatol. 2017; 67:370–398.
Marzano A, Angelucci E, Astegiano M, Baratelli C, Biancone L, Bironzo P, et al. AISF position paper on HCV in immunocompromised patients. Dig Liver Dis. 2019; 51:10–23.
Ng SC, Hilmi IN, Blake A, Bhayat F, Adsul S, Khan QR, Wu DC. Low frequency of opportunistic infections in patients receiving vedolizumab in clinical trials and post-marketing setting. Inflamm Bowel Dis. 2018; 24:2431–2441.
Rojo E, Chaparro M, García-Buey L. Efficacy and safety of glecaprevir/pibrentasvir in a patient With HCV-induced porphyria cutanea tarda receiving vedolizumab for Crohn’s disease. J Crohn’s Colitis. 2019; 14:567–568.
Degasperi E, Caprioli F, El Sherif O, Back D, Colombo M, Aghemo A. Challenges in treating patients with inflammatory bowel disease and concurrent viral hepatitis infection. Expert Rev Gastroenterol Hepatol. 2016; 10:1373–1383.
Colombel JF, Loftus EV Jr, Siegel CA, Lewis JD, Smyth M, Sankoh S, Abhyankar B. Efficacy of vedolizumab with concomitant corticosteroid or immunomodulator use in patients with ulcerative colitis from GEMINI 1. Gastroenterology. 2015; 9:S296–S297.
Naveau S, Chollet-Martin S, Dharancy S, Mathurin P, Jouet P, Piquet MA, et al.; Foie-Alcool group of the Association Française pour l’Etude du Foie. A double-blind randomized controlled trial of infliximab associated with prednisolone in acute alcoholic hepatitis. Hepatology. 2004; 39:1390–1397.
Kapila N, Flocco G, Shen B, Modaresi Esfeh J. The use of vedolizumab in patients with concomitant cirrhosis and Crohn’s disease. Cureus. 2018; 10:e3080.
Fishman JA. Infection in solid-organ transplant recipients. N Engl J Med. 2007; 357:2601–2614.
Chapman R, Fevery J, Kalloo A, Nagorney DM, Boberg KM, Shneider B, Gores GJ; American Association for the Study of Liver Diseases. Diagnosis and management of primary sclerosing cholangitis. Hepatology. 2010; 51:660–678.
Van Meeteren MJW, Hayee B, Inderson A, Van der Meulen AE, Altwegg R, Van Hoek B, et al. Safety of anti-TNF treatment in liver transplant recipients: a systematic review and metaanalysis. J Crohn’s Colitis. 2017; 11:1146–1151.
Colombel JF, Sands BE, Rutgeerts P, Sandborn W, Danese S, D’Haens G, et al. The safety of vedolizumab for ulcerative colitis and Crohn’s disease. Gut. 2016; 66:839–851.
Spadaccini M, Aghemo A, Caprioli F, Lleo A, Invernizzi F, Danese S, Donato MF. Safety of vedolizumab in liver transplant recipients: a systematic review. United European Gastroenterol J. 2019; 7:875–880.
Hillan KJ, Hagler KE, MacSween RN, Ryan AM, Renz ME, Chiu HH, et al. Expression of the mucosal vascular addressin, MAdCAM-1, in inflammatory liver disease. Liver. 1999; 19:509–518.
Eksteen B, Grant AJ, Miles A, Curbishley SM, Lalor PF, Hübscher SG, et al. Hepatic endothelial CCL25 mediates the recruitment of CCR9+ gut-homing lymphocytes to the liver in primary sclerosing cholangitis. J Exp Med. 2004; 200:1511–1517.
Christensen B, Micic D, Gibson PR, Yarur A, Bellaguarda E, Corsello P, et al. Vedolizumab in patients with concurrent primary sclerosing cholangitis and inflammatory bowel disease does not improve liver biochemistry but is safe and effective for the bowel disease. Aliment Pharmacol Ther. 2018; 47:753–762.
Tse CS, Loftus EV, Raffals LE, Gossard AA, Lightner AL. Effects of vedolizumab, adalimumab and infliximab on biliary inflammation in individuals with primary sclerosing cholangitis and inflammatory bowel disease. Aliment Pharmacol Ther. 2018; 48:190–195.
Caron B, Peyrin-Biroulet L, Pariente B, Bouhnik Y, Seksik P, Bouguen G, et al. Vedolizumab therapy is ineffective for primary sclerosing cholangitis in Patients with inflammatory bowel disease: a GETAID multicentre cohort study. J Crohns Colitis. 2019; 13:1239–1247.
EMA and EMEA. Stelara (ustekinumab). EMA/636854/2016. 2016. https://www.medisoc.it/wp-content/uploads/Ustekinumab-Stelara_EPAR.pdf .
Ustekinumab (Stelara) for psoriasis. Med Lett Drugs Ther. 2010; 52:7–8.
Feagan BG, Sandborn WJ, Gasink C, Jacobstein D, Lang Y, Friedman JR, et al.; UNITI–IM-UNITI Study Group. Ustekinumab as induction and maintenance therapy for Crohn’s disease. N Engl J Med. 2016; 375:1946–1960.
Piaserico S, Messina F, Russo FP. Managing psoriasis in patients with HBV or HCV infection: practical considerations. Am J Clin Dermatol. 2019; 20:829–845.
Löhr HF, Pingel S, Böcher WO, Bernhard H, Herzog-Hauff S, Rose-John S, Galle PR. Reduced virus specific T helper cell induction by autologous dendritic cells in patients with chronic hepatitis B - restoration by exogenous interleukin-12. Clin Exp Immunol. 2002; 130:107–114.
Rossol S, Marinos G, Carucci P, Singer MV, Williams R, Naoumov NV. Interleukin-12 induction of Th1 cytokines is important for viral clearance in chronic hepatitis B. J Clin Invest. 1997; 99:3025–3033.
Wang Q, Zhou J, Zhang B, Tian Z, Tang J, Zheng Y, et al. Hepatitis B virus induces IL-23 production in antigen presenting cells and causes liver damage via the IL-23/IL-17 axis. Plos Pathog. 2013; 9:e1003410.
Bao S, Zheng J, Li N, Huang C, Chen M, Cheng Q, et al. Role of interleukin-23 in monocyte-derived dendritic cells of HBV-related acute-on-chronic liver failure and its correlation with the severity of liver damage. Clin Res Hepatol Gastroenterol. 2017; 41:147–155.
Navarro R, Vilarrasa E, Herranz P, Puig L, Bordas X, Carrascosa JM, et al. Safety and effectiveness of ustekinumab and antitumour necrosis factor therapy in patients with psoriasis and chronic viral hepatitis B or C: a retrospective, multicentre study in a clinical setting. Br J Dermatol. 2013; 168:609–616.
Chiu HY, Chen CH, Wu MS, Cheng YP, Tsai TF. The safety profile of ustekinumab in the treatment of patients with psoriasis and concurrent hepatitis B or C. Br J Dermatol. 2013; 169:1295–1303.
Ting SW, Chen YC, Huang YH. Risk of hepatitis B reactivation in patients with psoriasis on ustekinumab. Clin Drug Investig. 2018; 38:873–880.
Koutsianas C, Thomas K, Vassilopoulos D. Prevention of HBV reactivation in patients treated with biologic agents. Expert Rev Clin Pharmacol. 2016; 9:579–589.
Cooper S, Erickson AL, Adams EJ, Kansopon J, Weiner AJ, Chien DY, et al. Analysis of a successful immune response against hepatitis C virus. Immunity. 1999; 10:439–449.
Lechner F, Wong DK, Dunbar PR, Chapman R, Chung RT, Dohrenwend P, et al. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med. 2000; 191:1499–1512.
Abuchar A, Vitiello M, Kerdel FA. Psoriasis treated with ustekinumab in a patient with hepatitis C. Int J Dermatol. 2013; 52:381–382.
Llamas-Velasco M, Concha-Garzón MJ, García-Diez A, Daudén E. Liver injury in psoriasis patients receiving ustekinumab: a retrospective study of 44 patients treated in the clinical practice setting. Actas Dermosifiliogr. 2015; 106:470–476.
Martínez-Montiel M, Piedracoba-Cadahia P, Gómez-Gómez C, Gonzalo J. Ustekinumab is effective and safe in the treatment of Crohn’s disease refractory to anti-TNFα in an orthotopic liver transplant patient. J Crohns Colitis. 2015; 9:816–817.
Peverelle M, Asadi K, De Cruz P. Ustekinumab is a safe and effective biologic agent for Crohn’s disease in a liver transplant patient. J Crohn’s Colitis. 2020; 14:1498–1499
Abraham C, Dulai PS, Vermeire S, Sandborn WJ. Lessons learned from trials targeting cytokine pathways in patients with inflammatory bowel diseases. Gastroenterology. 2017; 152:374–388.e4.
Sandborn WJ, Su C, Sands BE, D’Haens GR, Vermeire S, Schreiber S, et al.; OCTAVE Induction 1, OCTAVE Induction 2, and OCTAVE Sustain Investigators. Tofacitinib as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2017; 376:1723–1736.
Boor PPC, de Ruiter PE, Asmawidjaja PS, Lubberts E, van der Laan LJW, Kwekkeboom J. JAK-inhibitor tofacitinib suppresses interferon alfa production by plasmacytoid dendritic cells and inhibits arthrogenic and antiviral effects of interferon alfa. Transl Res. 2017; 188:67–79.
Chen YM, Huang WN, Wu Y-D, Lin CT, Chen YH, Chen DY, et al. Reactivation of hepatitis B virus infection in patients with rheumatoid arthritis receiving tofacitinib: a real-world study. Ann Rheum Dis. 2018; 77:780–782
Chen YM, Huang WN, Liao TL, Chen JP, Yang SS, Chen HH, et al. Comparisons of hepatitis C viral replication in patients with rheumatoid arthritis receiving tocilizumab, abatacept and tofacitinib therapy. Ann Rheum Dis. 2019; 78:849–850.
Singh JA, Saag KG, Bridges SL Jr, Akl EA, Bannuru RR, Sullivan MC, et al. 2015 American College of Rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Rheumatol. 2016; 68:1–26.
Migita K, Izumi Y, Jiuchi Y, Kozuru H, Kawahara C, Izumi M, et al. Effects of Janus kinase inhibitor tofacitinib on circulating serum amyloid A and interleukin-6 during treatment for rheumatoid arthritis. Clin Exp Immunol. 2014; 175:208–214.
Tanaka Y, Takeuchi T, Yamanaka H, Nakamura H, Toyoizumi S, Zwillich S. Efficacy and safety of tofacitinib as monotherapy in Japanese patients with active rheumatoid arthritis: a 12-week, randomized, phase 2 study. Mod Rheumatol. 2015; 25:514–521.
Panés J, Sandborn WJ, Schreiber S, Sands BE, Vermeire S, D’Haens G, et al. Tofacitinib for induction and maintenance therapy of Crohn’s disease: results of two phase IIb randomised placebo-controlled trials. Gut. 2017; 66:1049–1059.
Chalasani N, Bonkovsky HL, Fontana R, Lee W, Stolz A, Talwalkar J, et al.; United States Drug Induced Liver Injury Network. Features and outcomes of 899 patients with drug-induced liver injury: the DILIN prospective study. Gastroenterology. 2015; 148:1340–52.e7.
Meunier L, Clerc C, Meszaros M. Use of Tofacitinib for ulcerative colitis in a liver transplant patient. J Crohn’s Colitis. 2020;jjaa032. doi: 10.1093/ecco-jcc/jjaa032. [Epub ahead of print]
doi: 10.1093/ecco-jcc/jjaa032
Rahier JF, Magro F, Abreu C, Armuzzi A, Ben-Horin S, Chowers Y, et al.; European Crohn’s and Colitis Organisation (ECCO). Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis. 2014; 8:443–468.
Lledó JL, Fernández C, Gutiérrez ML, Ocaña S. Management of occult hepatitis B virus infection: an update for the clinician. World J Gastroenterol. 2011; 17:1563–1568.
Loras C, Gisbert JP, Mínguez M, Merino O, Bujanda L, Saro C, et al.; REPENTINA study; GETECCU (Grupo Español de Enfermedades de Crohn y Colitis Ulcerosa) Group. Liver dysfunction related to hepatitis B and C in patients with inflammatory bowel disease treated with immunosuppressive therapy. Gut. 2010; 59:1340–1346.
Liu CJ, Chen PJ, Chen DS, Kao JH. Hepatitis B virus reactivation in patients receiving cancer chemotherapy: natural history, pathogenesis, and management. Hepatol Int. 2013; 7:316–326.
Loras C, Gisbert JP, Saro MC, Piqueras M, Sánchez-Montes C, Barrio J, et al.; REPENTINA study, GETECCU group (Grupo Español de trabajo de Enfermedades de Crohn y Colitis Ulcerosa). Impact of surveillance of hepatitis b and hepatitis c in patients with inflammatory bowel disease under anti-TNF therapies: multicenter prospective observational study (REPENTINA 3). J Crohns Colitis. 2014; 8:1529–1538.
Bruix J, Sherman M. AASLD practice guideline management of hepatocellular carcinoma: an update. Hepatology. 2010; 53:1020–1022.
Pontisso P, Bellati G, Brunetto M, Chemello L, Colloredo G, Di Stefano R, et al. Hepatitis C virus RNA profiles in chronically infected individuals: do they relate to disease activity? Hepatology. 1999; 29:585–589.
Imperatore N, Castiglione F, Rispo A, Sessa A, Caporaso N, Morisco F. Timing strategies of direct-acting antivirals and biologics administration in HCV-infected subjects with inflammatory bowel diseases. Front Pharmacol. 2017; 8:867.
Stine JG, Chalasani N. Chronic liver injury induced by drugs: a systematic review. Liver Int. 2015; 35:2343–2353.