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1 GASTROENTEROLOGY 2012;142: Will Interferon-Free Regimens Prevail? Christoph Welsch Stefan Zeuzem Department of Internal Medicine I, J. W. Goethe University Hospital, Frankfurt/Main, Germany Many promising small molecule inhibitors directed against hepatitis C virus (HCV) proteins (directacting antiviral [DAA] agents) and compounds targeting host cell factors (host-targeting agents [HTAs]) are currently in the drug development and clinical trial pipeline, whereas contraindications and adverse effects limit the clinical applicability of peginterferon (Peg-IFN)-based therapies. The increasing number of alternative treatment options is driving the investigation of interferon-sparing regimens and paving the way for the question on the future place for interferon in HCV therapy. The recent approval of 2 DAAs by the US Food and Drug Administration and European Medicines Agency has opened a new era in the treatment of chronic HCV infection (CHC). The new standard of care is a triple therapy, combining the previous standard, 1 Peg-IFN- plus ribavirin (RBV), with a ketoamide protease inhibitor. The new standard of care is licensed for patients infected with genotype 1 HCV, the most prevalent genotype in Europe and North America. Ketoamide compounds, boceprevir (Victrelis, Merck & Co, Whitehouse Station, NJ) and telaprevir (Incivek, Vertex Pharmaceuticals, Cambridge, MA), are designed to mimic the natural NS3/4A protease substrate in genotype 1 HCV. Their addition to Peg-IFN/RBV significantly improves the sustained virologic response (SVR) rate. 2 4 Strategies in current clinical trials focus on the evaluation of different DAA combinations with or without RBV, because it soon became apparent that DAA monotherapy may not suffice to eliminate the virus. The availability of numerous drugs belonging to different classes actually stimulates those multiple DAA/HTA combination trials aiming for an ultimate goal: Peg-IFN free, all-oral HCV therapy (Figure 1). Unlike Peg-IFN/RBV, the selection of drug-resistant virus variants during treatment with DAAs is a major concern. The highly replicative nature of HCV infection, with approximately new virions produced each day in the typical infected individual, 5 coupled with the lack of proofreading activity in the RNA-dependent RNA polymerase, NS5B, results in the generation of every possible viral variant every day. 6 Thus, each patient is infected with a viral quasispecies cloud composed of genetically distinct but closely related viral genomes. Mathematical models suggest that every possible drug-resistant viral variant is likely to preexist at a low frequency in the replicating viral quasispecies population of the typical HCV-infected patient. 6 It is well established that resistance-associated amino acid variants (RAVs) are present at readily detectable frequencies in a minority of patients before the initiation of DAA-containing therapy. In the absence of concomitant Peg-IFN/RBV therapy, those drug-resistant viral variants are rapidly selected and may emerge at frequencies as high as 5% to 20% in the quasispecies of patients as early as the second day of treatment. 7 Unless suppressed by concomitant Peg-IFN/RBV, these preexisting resistant variants are likely to cause treatment failure. Therefore, combinations of non cross-resistant drugs and compounds with high antiviral efficacy and a high barrier to resistance are of major importance to avoid the emergence of RAVs and treatment failure. Some pharmacologic prerequisites are important to combine multiple DAAs, that is, at least additive antiviral efficacy for every DAA, as well as careful ascertainment of possible drug-drug interactions and overlapping safety issues. The INFORM-1 trial provided a proof of principle that Peg-IFN free DAA combination therapy in treatment- and treatment-experienced patients with genotype 1 CHC can effectively suppress HCV replication. 8 Abbreviations used in this paper: CHC, chronic hepatitis C virus infection; DAA, direct-acting antiviral; HTA, host-targeting agent; Peg- IFN, peginterferon; RAV, resistance-associated amino acid variant; RBV, ribavirin; RVR, rapid virologic response; SVR, sustained virologic response by the AGA Institute /$36.00 doi: /j.gastro
2 1352 WELSCH AND ZEUZEM GASTROENTEROLOGY Vol. 142, No. 6 Figure 1. Development stage for clinical studies with DAAs/ HTAs in chronic hepatitis C. Green boxes indicate planned and ongoing studies with Peg- IFN/RBV backbone, and blue boxes indicate IFN-free trials. Combining the macrocyclic NS3/4A protease inhibitor danoprevir with the nucleoside analogue NS5B polymerase inhibitor mericitabine (R7128), strongest antiviral activity was observed in treatment- patients at highest dose levels, and similar responses were also achieved in previous null responders. Other trials assessed the combination of an NS3/4A protease inhibitor with a non-nucleoside polymerase inhibitor. The SOUND-C1 trial showed potent antiviral activity in treatment- patients with genotype 1 HCV, combining the protease inhibitor BI with the non-nucleoside polymerase inhibitor BI and RBV. Higher response rates were observed in genotype 1b compared with genotype 1a, with rapid virologic response (RVR) rates for dual DAA plus RBV from 73% to 100% depending on the DAA dosing. 9 The SOUND-C2 trial confirmed the potent antiviral activity of this combination therapy; however, the RBV-sparing arm showed substantial but lower response rates than other arms of the trial. 10 In another study, patients were randomized for 4-week dual, triple, or quadruple therapy, combining the protease inhibitor GS-9256 and the non-nucleoside polymerase inhibitor GS-9190 with or without RBV or Peg- IFN/RBV. The range for RVR was from 100% in quadruple to 38% in triple and only 7% in dual therapy, combining only the 2 DAAs. 11 The very low response rate in the latter group was related to the frequent occurrence of RAVs, which highlights the extraordinarily important role of Peg-IFN and RBV to prevent the emergence of resistance and virologic breakthrough in DAA-containing regimens. The ZENITH trial assessed antiviral activity of the protease inhibitor telaprevir and the non-nucleoside polymerase inhibitor VX-222 in a dual regimen, as well as with RBV as triple or with Peg-IFN/RBV as quadruple combination therapy in treatment- patients with genotype 1 HCV. The quadruple therapy was associated with high antiviral activity, comparable to SVR rates in Peg-IFN/ RBV plus telaprevir, and without viral breakthrough on treatment. Furthermore, 38% to 50% of the patients were able to undergo only 12 weeks of therapy with 82% to 93% achieving SVR In a different approach, genotype 1 HCV infected, treatment-experienced null responders were randomized to receive an all oral combination of an NS5A and protease inhibitor, BMS and BMS , respectively, or a combination of the 2 DAAs with Peg-IFN/RBV for 24 weeks. 13 The DAA-alone group showed a viral breakthrough rate of overall 54.5%, with only 2 of 9 genotype 1a HCV-infected patients achieving SVR, whereas 2 of 2 genotype 1b HCV infected patients achieved SVR. This is further confirmed by a Japanese study, showing SVR12 in 90% of genotype 1b infected previous null responders. 14 The quadruple therapy with the Peg-IFN/RBV backbone was highly effective, with all patients achieving SVR after treatment completion. 15 The genetic barrier to resistance is different between genotypes 1a and 1b HCV, with often only one nucleotide change needed in genotype 1a and 2 changes required in genotype 1b for development of RAV. 7 In contrast to that, nucleoside analogues against the highly conserved active site of NS5B have an equal antiviral activity against different subtypes and a high barrier to resistance. 7 The QUANTUM trial 16 was planned as the first interferon-free, all-nucleotide study, combining PSI-7977 and PSI-938 with or without RBV for 12 or 24 weeks in patients with CHC in all genotypes. However, PSI-938 was dropped from the QUANTUM trial due to adverse events. The broad genotype coverage using nucleotide NS5B inhibitors is supported by data reported from
3 May 2012 HCV AND THE METABOLIC SYNDROME 1353 the NUCLEAR and PROTON studies in genotype 1 and interferon-free arms of the ELECTRON trial in patients infected with HCV genotype 2 or 3. The key lesson to learn from all data reported in previous trials containing DAAs is as follows. High antiviral efficacy and high barrier to resistance are indispensable requirements for all oral Peg-IFN free regimens to avoid early treatment failure. Naturally occurring polymorphisms in DAA target structures may be of clinical importance, because some variants may provide a priori for escape from DAAs, and second-site compensatory mutations that enhance the fitness of resistant viruses emerging on therapy are likely to occur. 17 We expect complex patterns of RAVs with varying and yet unknown escape mechanisms from DAAs in future antiviral treatment. The lead-in concept with Peg-IFN/RBV specifically designated to suppress such types of RAVs before starting on a direct antiviral. However, the majority of studies have shown no effect in reducing breakthrough or relapse rates, as shown in REALIZE, 18 Silen-C1, 19 and Silen-C2. 20 A major hurdle on the way to an all-oral HCV therapy is the genotype-dependent antiviral activity of DAAs (with the exception of nucleoside polymerase inhibitors), most of them targeting HCV genotype 1, with implications for all HCV non genotype 1 DAA combination trials. A way to circumvent that problem is inhibitors targeting host cell structures relevant for replication of HCV in hepatocytes. Among the most advanced and promising HTAs for a Peg-IFN free DAA combination regimen is the cyclophilin A binding molecule alisporivir, previously known as DEB025/Debio 025, which possesses a novel mechanism of action with a broad genotype coverage from 1 to 4 and potent anti-hcv activity. The selection of resistant HCV genotype 1b replicons against alisporivir was reportedly difficult, with an average of 20 weeks compared with less than 2 weeks in HCV NS3/4A protease or non-nucleoside polymerase inhibitors. 21 A recent phase 2 clinical trial showed the superiority of once-daily alisporivir plus Peg- IFN/RBV in achieving SVR in genotype 1 HCV infected patients with 76% SVR in triple therapy compared with 55% in the Peg-IFN/RBV control arm, and a treatment duration of only 24 weeks was needed for SVR in patients with RVR. 22 Interestingly, one case of SVR in a genotype 3 HCV infected patient was reported after alisporivir monotherapy for 29 days. 23 The genetic barrier to resistance in vitro was shown to be much higher than for protease or non-nucleoside polymerase inhibitors, which is corroborated in vivo by the low overall breakthrough rate of only 4.7%. 22 Another promising HTA is miravirsen (SPC3649), an oligonucleotide mir-122 targeting drug, Table 1. Summary on IFN-Sparing Regimens and Their Major Outcomes Regimen Trial Patient population Compounds Major study outcome INFORM-1 8 experienced SOUND-C1 9 SOUND-C2 10 Zeuzem et al 11 ZENITH 12 Lok et al, 13 Chayama et al, 14 and Lok et al 15 NUCLEAR, 16 PROTON, 16 ELECTRON, 16 and QUANTUM 16 Flisiak et al 22 Mono Janssen et al 24 experienced (previous null responders) 6 PI (danoprevir) Nuc (mericitabine) PI (BI ) Non-Nuc (BI ) PI (BI ) Non-Nuc (BI ) PI (GS-9256) Non-Nuc (GS-9190) PI (Telaprevir) Non-Nuc (VX-222) PI (BMS ) NS5A (BMS ) Nuc (PSI-7977) Nuc (PSI-938) Cyclophilin A targeting (alisporivir, DEB025) mir-122 targeting (miravirsen, SPC3649) Proof of principle for IFN-free therapy Dose-dependent response rates Dose-dependent response rates Lower response rates in RBV-sparing arm Important role of Peg-IFN/RBV to prevent resistance Emergence of RAVs with low response in the dual regimen 100% response in the quadruple regimen High antiviral activity in quadruple No viral breakthrough Viral breakthrough in dual DAA Higher response in HCV b Highly effective quadruple regimen First all-nuc study High SVR rates in GT2,3 Broad genotype coverage High barrier to resistance High response for triple regimen Broad genotype coverage from 1 to 4 High barrier to resistance Proof-of-concept study Dose-dependent, prolonged reduction in HCV RNA levels No evidence of RAVs GT, genotype; Non-nuc, non-nucleos(t)ide polymerase inhibitor; Nuc, nucleos(t)ide analogue; PI, protease inhibitor.
4 1354 WELSCH AND ZEUZEM GASTROENTEROLOGY Vol. 142, No. 6 which is a liver-specific microrna that HCV requires for RNA replication. The drug specifically recognizes mir- 122, which is subsequently sequestered and unavailable for HCV. A proof-of-concept study in treatment- genotype 1 HCV infected patients, receiving miravirsen for 29 days as a once-weekly subcutaneous injection without Peg-IFN/RBV, showed dose-dependent, prolonged reductions in HCV RNA levels that continued to decrease after the end of treatment with a mean decrease in HCV RNA level from baseline to week 10 of 2.71 log 10. Miravirsen seems to provide an extraordinary high barrier to resistance, with no evidence of RAVs in any studies. 24 Mostly treatment- patients with CHC have been enrolled in previous DAA/HTA trials (Table 1); however, additional interferon-free combination therapies have been announced and will be available for hard-to-treat patient populations (eg, previous null responders). In summary, an all-oral HCV therapy is an ambitious goal for future treatment of patients with CHC, with recent data providing good evidence that this goal is achievable and that Peg-IFN has only a bridging function and is not an ultimate solution. If there is any need for interferon in future treatment of CHC, the EMERGE study showed that treatment with Peg-IFN- resulted in superior viral response in HCV genotypes 1 to 4 and improved safety and tolerability compared with Peg-IFN-. 25 Despite the many promising data on the potency of DAAs and HTAs in all-oral HCV therapy, some obstacles might delay the success story of interferon-free regimens. First of all, most DAAs are restricted for genotype 1 HCV, but other genotypes are highly prevalent in many parts of the world, with some next-generation drugs, notably cyclophilin, NS5A, NS5B, and novel NS3/4A protease inhibitors, showing broader genotype coverage. Probably most important, naturally existing variants are of substantial relevance to the success of DAA-containing regimens but may be of limited clinical significance at present because they are likely to be suppressed by Peg-IFN/RBV in current standard of care regimens. They can be expected to be of substantial importance to the outcome of future interferon-sparing, all-oral DAA combination therapies. Whether the detection of baseline RAVs is a way to predict treatment failure in interferon-free regimens and if there is a quantitative threshold on the frequency of RAVs in the quasispecies population needed to predict treatment failure needs further investigation. The lead-in concept with Peg-IFN/RBV to avoid or reduce the selection of RAVs is highly questionable. Not least, many practical issues need to be improved for future-generation antivirals, in particular drug-drug interactions and overlapping safety issues, which restrict their applicability at present and conversely foster the use of interferon for some time. However, its expiration date seems to be foreseeable. References 1. Fried MW, Shiffman ML, Reddy KR, et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002;347: Hezode C, Forestier N, Dusheiko G, et al. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med 2009;360: Kwo PY, Lawitz EJ, McCone J, et al. Efficacy of boceprevir, an NS3 protease inhibitor, in combination with peginterferon alfa-2b and ribavirin in treatment-naive patients with genotype 1 hepatitis C infection (SPRINT-1): an open-label, randomised, multicentre phase 2 trial. Lancet 2010;376: McHutchison JG, Everson GT, Gordon SC, et al. Telaprevir with peginterferon and ribavirin for chronic HCV genotype 1 infection. N Engl J Med 2009;360: Neumann AU, Lam NP, Dahari H, et al. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 1998;282: Rong L, Dahari H, Ribeiro RM, et al. Rapid emergence of protease inhibitor resistance in hepatitis C virus. Sci Transl Med 2010;2: 30ra Sarrazin C, Zeuzem S. Resistance to direct antiviral agents in patients with hepatitis C virus infection. Gastroenterology 2010; 138: Gane EJ, Roberts SK, Stedman CA, et al. Oral combination therapy with a nucleoside polymerase inhibitor (RG7128) and danoprevir for chronic hepatitis C genotype 1 infection (INFORM-1): a randomized, double-blind, placebo-controlled, dose-escalation trial. Lancet 2010;376: Zeuzem S, Asselah T, Angus P, et al. Efficacy of the protease inhibitor BI , polymerase inhibitor BI , and ribavirin in patients with chronic HCV infection. Gastroenterology 2011; 141: Zeuzem S, Soriano V, Asselah T, et al. Virologic response to an interferon-free regimen of BI and BI , with and without ribavirin, in treatment-naive patients with chronic genotype-1 HCV infection: week 12 interim results of the SOUND-C2 study. Presented at: 62nd Annual Meeting of the American Association of the Study of Liver Diseases; November 4 8, 2011; San Francisco, CA. LB Zeuzem S, Buggisch P, Agarwal K, et al., triple, and quadruple combination treatment with a protease inhibitor (GS-9256) and a polymerase inhibitor (GS-9190) alone and in combination with ribavirin (RBV) or PegIFN/RBV for up to 28 days in treatment, genotype 1 HCV subjects. Presented at: 61st Annual Meeting of the American Association of the Study of Liver Diseases; October 30 to November 2, 2010; Boston, MA. LB Nelson DR, Gane EJ, Jacobson IM, et al. VX-222/telaprevir in combination with peginterferon-alfa-2a and ribavirin in treatmentnaive genotype 1 HCV patients treated for 12 weeks: ZENITH study, SVR12 interim analysis. Presented at: 62nd Annual Meeting of the American Association of the Study of Liver Diseases; November 4 8, 2011; San Francisco, CA. LB Lok A, Gardiner D, Lawitz E, et al. Combination therapy with BMS and BMS alone or with pegylated interferon and ribavirin (pegifn/rbv) results in undetectable HCV RNA through 12 weeks of therapy in HCV genotype 1 null responders. Presented at: 61st Annual Meeting of the American Association of the Study of Liver Diseases; October 30 to November 2, 2010; Boston, MA. 14. Chayama K, Takahashi S, Kawakami Y, et al. oral combination therapy with the NS5A inhibitor BMS and the NS3 protease inhibitor BMS achieved 90% sustained virologic response (SVR12) in HCV genotype 1b-infected null responders. Presented at: 62nd Annual Meeting of the American Association of the Study of Liver Diseases; November 4 8, 2011; San Francisco, CA. LB Lok A, Gardiner D, Lawitz E, et al. therapy with BMS , BMS and PEG-IFN/RBV for 24 weeks results in 100% SVR12 in HCV genotype 1 null responders. Presented at: 2011 Annual Meeting of the European Association for the Study of the Liver; March 30 to April 3, 2011; Berlin, Germany.
5 May 2012 HCV AND THE METABOLIC SYNDROME Pharmasset initiates QUANTUM, a phase 2b interferon-free trial of PSI-7977 and PSI-938 for all HCV genotypes. Princeton, NJ: Pharmasset, Shimakami T, Welsch C, Yamane D, et al. Protease inhibitorresistant hepatitis C virus mutants with reduced fitness from impaired production of infectious virus. Gastroenterology 2011; 140: Zeuzem S, Andreone P, Pol S, et al. Telaprevir for retreatment of HCV infection. N Engl J Med 2011;364: Sulkowski MS, Ceasu E, Asselah T, et al. Silen-C1: Sustained virologic response (SVR) and safety of BI combined with peginterferon alfa-2a and ribavirin (P/R) in treatment- patients with chronic genotype 1 HCV infection. Presented at: 2011 Annual Meeting of the European Association for the Study of the Liver; March 30 to April 3, 2011; Berlin, Germany. 20. Sulkowski MS, Bourliere M, Bronowicki JP, et al. Silen-C2: Sustained virologic response (SVR) and safety of BI combined with peginterferon alfa-2a and ribavirin (P/R) in chronic HCV genotype-1 patients with non-response to P/R. Presented at: 2011 Annual Meeting of the European Association for the Study of the Liver; March 30 to April 3, 2011; Berlin, Germany. 21. Coelmont L, Hanoulle X, Chatterji U, et al. DEBO25 (Alispovir) inhibits hepatitis C virus replication by preventing a cyclophilin A induced cis-trans isomerisation in domain II of NS5A. PLoS One 2010;5:e Flisiak R, Pawlotsky JM, Crabbé R, et al. Once daily alisporivir (DEBO25) plus PegIFNalfa2A/ribavirin results in superior sustained virologic response (SVR24) in chronic hepatitis C genotype 1 treatment patients. Presented at: 2011 Annual Meeting of the European Association for the Study of the Liver; March 30 to April 3, 2011; Berlin, Germany. 23. Patel H, Heathcote EJ. Sustained virological response with 29 days of Debio 025 monotherapy in hepatitis C virus genotype 3. Gut 2011;60: Janssen HL, Reesink HW, Zeuzem S, et al. A randomized, doubleblind, placebo (PLB) controlled safety and antiviral proof of concept study of miravirsen (MIR), an oligonucleotide targeting mir- 122, in treatment naive patients with genotype 1 () chronic HCV infection. Presented at: 62nd Annual Meeting of the American Association of the Study of Liver Diseases; November 4 8, 2011; San Francisco, CA. LB Zeuzem S, Arora S, Bacon BR, et al. Pegylated interferon-lambda (pegifn-[lambda]) shows superior viral response with improved safety and tolerability versus pegifn-[alpha]-2a in HCV patients (G1/2/3/4): EMERGE phase IIb through week 12. Presented at: 2011 Annual Meeting of the European Association for the Study of the Liver; March 30 to April 3, 2011; Berlin, Germany. Received October 18, Accepted December 19, Reprint requests Address requests for reprints to: Christoph Welsch, MD, Department of Internal Medicine I, J. W. Goethe University Hospital, Theodor-Stern-Kai 7, Frankfurt/Main, Germany. christophwelsch@gmx.net; fax: 49 (0) Conflicts of interest: The authors disclose the following: SZ has served as a consultant for Abbott, Achillion, AstraZeneca, BMS, Boehringer, Gilead, Idenix, Janssen, Merck, Novartis, Roche, Santaris, and Vertex. CW discloses no conflicts.
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