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Evidence-Based Recommendations on the Management of Extrahepatic Manifestations of Chronic Hepatitis C Virus Infection

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Evidence-Based Recommendations on the Management of Extrahepatic Manifestations of Chronic Hepatitis C Virus Infection Review Evidence-based recommendations on the management of extrahepatic manifestations of chronic hepatitis C virus infection ⇑ Manuel Ramos-Casals1,2,3, , Anna Linda Zignego4, Clodoveo Ferri5, Pilar Brito-Zerón1,2,6, Soledad Retamozo1,7, Milvia Casato8, Peter Lamprecht9, Alessandra Mangia10, David Saadoun11,12,13,14, Athanasios G. Tzioufas15, Zobair M. Younossi16, Patrice Cacoub11,12,13,14, on behalf of the International Study Group of Extrahepatic Manifestations related to HCV (ISG-EHCV)à Keywords: Hepatitis C virus; Ext- Introduction rahepatic manifestations; DAAs; Rituximab. The hepatitis C virus (HCV), a linear, single- (eradication \50% for HCV genotype 1), often Received 10 November 2016; stranded RNA virus identified in 1989, is a required several months of therapy and had high received in revised form 5 February hepatotropic virus that causes liver cirrhosis and rates of intolerance [10]. Direct-acting antiviral 2017; accepted 6 February 2017 hepatocellular cancer and is a global health prob- (DAA) therapies have recently emerged as a strik- lem. It is recognized as one of the hepatic viruses ing therapeutic approach for HCV infection, with Key point most often associated with the development of a short treatment duration, minimal side effects extrahepatic manifestations (EHMs), which can be and efficacy approaching 100% [11–14]. These The objective of this international consensus is classified according to the principal underlying new drugs are providing the opportunity to effec- to provide therapeutic etiopathogenic process (autoimmune, inflamma- tively cure chronic HCV infection and reduce the recommendations for HCV tory, metabolic or neoplastic) [1]. HCV infected burden caused by both the hepatic and extrahep- patients with extrahepatic patients with extrahepatic involvement require a atic complications of HCV, thereby offering hope manifestations. multidisciplinary approach and a complex thera- for a dramatic change in patient outcomes. The peutic management. objective of this international multidisciplinary 1 Laboratory of Autoimmune In the 1990s, various authors described the consensus is to provide the first set of recommen- Diseases Josep Font, CELLEX- IDIBAPS, Barcelona, Spain; association between HCV infection with organ dations on a homogeneous therapeutic approach 2Department of Autoimmune damage beyond the liver and a heterogeneous to HCV infected patients with extrahepatic involve- Diseases, ICMiD, Hospital Clínic, group of extrahepatic conditions including pul- ment in the new DAA era. Barcelona, Spain; monary fibrosis, cutaneous vasculitis, glomeru- 3Department of Medicine, Univer- Review sity of Barcelona, Barcelona, Spain; lonephritis, Mooren ulcer, porphyria cutanea tarda 4Interdepartmental Center MASVE, and lichen planus, among others [2–4]. However, Department of Experimental and it is currently accepted that there is a weak associ- Methods Clinical Medicine, University of ation with some of these features [1,5], and that Florence, Florence, Italy; cryoglobulinemic vasculitis (CV) is the key extra- In 2015, the convenor (PC) and co-convenors (MC, 5Chair and Rheumatology Unit, Medical School, University of hepatic disease related to chronic HCV infection. CF, PL, AM, MRC, DS, AT, ZY, ALZ) constituted the Modena and Reggio Emilia, Azienda There is growing interest in the association with Steering Committee of the International Study Ospedaliero-Universitaria, Policlin- both systemic and organ-specific autoimmune dis- Group of Extrahepatic Manifestations related to ico di Modena, Modena, Italy; eases and with the development of neoplastic HCV (ISG-EHCV). International experts known for 6Autoimmune Diseases Unit, haematologic processes due to the specific lym- Department of Medicine, Hospital their experience in managing and treating HCV CIMA- Sanitas, Barcelona, Spain; photropism of HCV [1,6,7]. infected patients and their long, active history of 7Rheumatology Department, Currently, there are no international recom- clinical/basic research in this field were invited to Hospital Privado Universitario de mendations on the therapeutic management of join the multidisciplinary Advisory Working Group, Córdoba, INSTITUTO DE INVESTI- HCV infected patients with EHMs. The first thera- including rheumatologists, internists, hepatologists, GACIONES EN CIENCIAS DE LA SALUD (INICSA), National Scientific peutic approaches were based on immunosup- nephrologists and haematologists. To find potential and Technical Research Council, pressive therapies mirroring the regimens used topics of interest related to the therapeutic manage- CONICET - CORDOBA - Argentina; in non-HCV vasculitides [8]. The introduction of ment of EHM, a core group (MRC, ALZ, CF and PC) 8 Department of Clinical the first antiviral therapies combination (inter- created a list of potential proposals (no limit were Immunology, Sapienza University feron [IFN] alpha and ribavirin [RBV]) clearly placed on proposals) (Table S1), which were catego- of Rome, Italy; 9Department of Rheumatology & improved survival rates[9]. However, this thera- rized, refined (overlapping questions were elimi- Vasculitis Center, University of peutic approach had limited virological efficacy nated) and grouped in to three categories: A) Lübeck, Germany; Journal of Hepatology 2017 vol. 66 j 1282–1299 JOURNAL OF HEPATOLOGY Antiviral therapeutic approach; B) Pre-treatment rounds finally carried out. The level of scientific evaluation; and C) Non-antiviral therapeutic evidence was classified on a 5-point scale and the Key point approach. The specific search terms for the system- strength of evidence on a 3-point scale [21] (Tables The current therapeutic atic literature review (SLR) for each proposal were S3 and S4). armamentarium against also discussed. The SLR was carried out by MRC, HCV has been recently PBZ and SR searching PubMed (July 20, 2016) using expanded with an explosion the following as key terms; ‘‘Hepatitis C virus”, Summary of evidence of new molecules (DAAs) ‘‘extrahepatic” and ‘‘therapy”, and as secondary with high virological efficacy. terms those proposed for each specific statement, The current armamentarium against HCV has been with no research restrictions. Other databases, such expanded in the last 5 years with an explosion of as EMBASE and Cochrane Library were also new molecules able to directly target non-structural Key point checked. Studies were considered as eligible when proteins that play a key role in HCV replication B cell depletion with (i) the study population included adults with HCV (Fig. 1). These agents have been called DAAs [22] rituximab is the established chronic infection presenting EHMs; (ii) the inter- and target some of the main molecular components biologic approach to cryo- vention consisted of therapy with specific drugs; of HCV, including NS3/4A protease (first and second globulinaemic vasculitis (iii) studies were randomized controlled trials, generation protease inhibitors), NS5B polymerase (CV) employed to date. prospective cohort, retrospective cohort, case-con- (nucleoside and non-nucleoside analogs) and NS5A trol studies and case series; isolated case reports protein. In spring 2011, the US Food and Drug were accepted only for DAA regimens; reviews, Administration (FDA) approved the first generation experimental animal studies, in vitro studies and of NS3/4A protease inhibitors (boceprevir and duplicate publications were excluded; and (iv) telaprevir) as treatments for chronic HCV infection. studies contained sufficient and clear information NS3/4A protease inhibitors (PIs: telaprevir, bocepre- about the effect of the drugs evaluated (antiviral vir, simeprevir, paritaprevir, voxilaprevir, asunapre- and non-antiviral) on the extrahepatic manifesta- vir, grazoprevir, glecaprevir) block the catalytic site 10Liver Unit, IRCCS ‘‘Casa Sollievo tions presented by the patients, either classified of the protease, resulting in the failure of polypro- della Sofferenza”, San Giovanni as improvement vs. no improvement, or as com- tein cleaving and processing. NS5B polymerase inhi- Rotondo, Italy; 11Sorbonne Universités, UPMC plete response, partial response or no response. In bitors include nucleoside analogs (sofosbuvir) that Université Paris 06, UMR 7211, and addition, the current evidence-based guidelines act as chain terminators within the polymerase cat- Inflammation-Immunopathology- for the therapeutic management of unselected alytic site and non-nucleoside inhibitors (dasabuvir, Biotherapy Department (DHU i2B), HCV infected populations were also specifically beclabavir) bind to different allosteric sites causing F-75005 Paris, France; 12INSERM, UMR_S 959, F-75013 evaluated, including the UK 2014 [15], Latin Amer- conformational changes that render the polymerase Paris, France; ican Recommendations [16], INASL Recommenda- ineffective. Finally, NS5A inhibitors (daclatasvir, 13CNRS, FRE3632, F-75005 Paris, tions 2015[17], EASL 2016 [18] and the AASLD/ ledipasvir, ombitasvir, velpatasvir, elbasvir, pibren- France; IDSA 2015 [19]. tasvir) have been shown to be potent antivirals, 14AP-HP, Groupe Hospitalier Based on the SLR results, a core group (MRC, although the exact mechanism by which they inter- Pitié-Salpêtrière, Department of Internal Medicine and Clinical ALZ, CF and PC) developed initial statements and act with the NS5A protein and inhibit HCV replica- Immunology, F-75013 Paris, France; a support group (PBZ, SR) prepared and reviewed tion remains unclear [22]. Table 1 summarizes the 15Department of Pathophysiology, the scientific evidence to support
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