Pharmacokinetics and pharmacodynamics of pegylated interferon for the treatment of hepatitis B

References

• Chang TT, Gish RG, de Man R, et al. A comparison of entecavir and lamivudine for HBeAg-positive chronic hepatitis B. N Engl J Med. 2006 Mar 9;354(10):1001–1010.
   Google Scholar
• Sorrell MF, Belongia EA, Costa J, et al. National Institutes of Health consensus development conference statement: management of hepatitis B. Hepatology. 2009 May;49(5 Suppl):S4–S12.
   Google Scholar
• Iloeje UH, Yang HI, Su J, et al. Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology. 2006 Mar;130(3):678–686.
   Google Scholar
• Chen CJ, Yang HI, Su J, et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA. 2006 Jan 4;295(1):65–73.
   Google Scholar
• Chen CF, Lee WC, Yang HI, et al. Changes in serum levels of HBV DNA and alanine aminotransferase determine risk for hepatocellular carcinoma. Gastroenterology. 2011 Oct;141(4):1240–8, 1248 e1–2.
   Google Scholar
• Yang HI, Sherman M, Su J, et al. Nomograms for risk of hepatocellular carcinoma in patients with chronic hepatitis B virus infection. J Clin Oncol. 2010 May 10;28(14):2437–2444.
   Google Scholar
• Allweiss L, Dandri M. The role of cccDNA in HBV maintenance. Viruses. 2017;9(6).
   Google Scholar
• Ghany MG. Current treatment guidelines of chronic hepatitis B: the role of nucleos(t)ide analogues and peginterferon. Best Pract Res Clin Gastroenterol. 2017 Jun;31(3):299–309.
   Google Scholar
• Marcellin P, Gane E, Buti M, et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet. 2013 Feb 9;381(9865):468–475.
   Google Scholar
• Chon YE, Park JY, Myoung SM, et al. Improvement of liver fibrosis after long-term antiviral therapy assessed by fibroscan in chronic hepatitis B patients with advanced fibrosis. Am J Gastroenterol. 2017 Jun;112(6):882–891.
   Google Scholar
• Wong GL, Chan HL, Mak CW, et al. Entecavir treatment reduces hepatic events and deaths in chronic hepatitis B patients with liver cirrhosis. Hepatology. 2013 Nov;58(5):1537–1547.
   Google Scholar
• Wu CY, Lin JT, Ho HJ, et al. Association of nucleos(t)ide analogue therapy with reduced risk of hepatocellular carcinoma in patients with chronic hepatitis B: a nationwide cohort study. Gastroenterology. 2014 Jul;147(1):143–151 e5.
   Google Scholar
• Hosaka T, Suzuki F, Kobayashi M, et al. Long-term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology. 2013 Jul;58(1):98–107.
   Google Scholar
• Sarin SK, Kumar M, Lau GK, et al. Asian-pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int. 2016 Jan;10(1):1–98.
   Google Scholar
• European Association for the Study of the Liver. Electronic address eee, European Association for the Study of the L. EASL 2017 clinical practice guidelines on the management of hepatitis B virus infection. J Hepatol. 2017 Aug;67(2):370–398.
   Google Scholar
• Terrault NA, Lok ASF, McMahon BJ, et al. Update on prevention, diagnosis, and treatment of chronic hepatitis B: AASLD 2018 hepatitis B guidance. Hepatology. 2018 Apr;67(4):1560–1599.
   Google Scholar
• Buster EH, Schalm SW, Janssen HL. Peginterferon for the treatment of chronic hepatitis B in the era of nucleos(t)ide analogues. Best Pract Res Clin Gastroenterol. 2008;22(6):1093–1108.
   Google Scholar
• Durantel D, Zoulim F. New antiviral targets for innovative treatment concepts for hepatitis B virus and hepatitis delta virus. J Hepatol. 2016 Apr;64(1 Suppl):S117–S131.
   Google Scholar
• Perrillo R. Benefits and risks of interferon therapy for hepatitis B. Hepatology. 2009 May;49(5 Suppl):S103–11.
   Google Scholar
• Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol. 2008 Jul;8(7):559–568.
   Google Scholar
• Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev. 2001 Oct;14(4):778–809, table of contents.
   Google Scholar
• Harris JM, Martin NE, Modi M. Pegylation: a novel process for modifying pharmacokinetics. Clin Pharmacokinet. 2001;40(7):539–551.
   Google Scholar
• Matthews SJ, McCoy C. Peginterferon alfa-2a: a review of approved and investigational uses. Clin Ther. 2004 Jul;26(7):991–1025.
   Google Scholar
• Cooksley WG, Piratvisuth T, Lee SD, et al. Peginterferon alpha-2a (40 kDa): an advance in the treatment of hepatitis B e antigen-positive chronic hepatitis B. J Viral Hepat. 2003 Jul;10(4):298–305.
   Google Scholar
• Ingle H, Peterson ST, Baldridge MT. Distinct effects of type I and III interferons on enteric viruses. Viruses. 2018 Jan 20;10(1).
   Google Scholar
• Lee S, Baldridge MT. Interferon-Lambda: a potent regulator of intestinal viral infections. Front Immunol. 2017;8:749.
   Google Scholar
• Isaacs A, Lindenmann J. Virus interference. I. The interferon. By A. Isaacs and J. Lindenmann, 1957. J Interfer Res. 1987 Oct;7(5):429–438.
   Google Scholar
• Wheelock EF. Interferon-like virus-inhibitor induced in human leukocytes by phytohemagglutinin. Science. 1965 Jul 16;149(3681):310–311.
   Google Scholar
• Vilcek J. Fifty years of interferon research: aiming at a moving target. Immunity. 2006 Sep;25(3):343–348.
   Google Scholar
• Wieland SF, Guidotti LG, Chisari FV. Intrahepatic induction of alpha/beta interferon eliminates viral RNA-containing capsids in hepatitis B virus transgenic mice. J Virol. 2000 May;74(9):4165–4173.
   Google Scholar
• Li J, Lin S, Chen Q, et al. Inhibition of hepatitis B virus replication by MyD88 involves accelerated degradation of pregenomic RNA and nuclear retention of pre-S/S RNAs. J Virol. 2010 Jul;84(13):6387–6399.
   Google Scholar
• Xu C, Guo H, Pan XB, et al. Interferons accelerate decay of replication-competent nucleocapsids of hepatitis B virus. J Virol. 2010 Sep;84(18):9332–9340.
   Google Scholar
• Belloni L, Allweiss L, Guerrieri F, et al. IFN-alpha inhibits HBV transcription and replication in cell culture and in humanized mice by targeting the epigenetic regulation of the nuclear cccDNA minichromosome. J Clin Invest. 2012 Feb;122(2):529–537.
   Google Scholar
• Lucifora J, Xia Y, Reisinger F, et al. Specific and nonhepatotoxic degradation of nuclear hepatitis B virus cccDNA. Science. 2014 Mar 14;343(6176):1221–1228.
   Google Scholar
• Bruno R, Sacchi P, Cima S, et al. Comparison of peginterferon pharmacokinetic and pharmacodynamic profiles. J Viral Hepat. 2012 Jan;19(Suppl 1):33–36.
   Google Scholar
• Reddy KR. Development and pharmacokinetics and pharmacodynamics of pegylated interferon alfa-2a (40 kD). Semin Liver Dis. 2004;24(Suppl 2):33–38.
   Google Scholar
• Ahn SB, Jun DW, Kim SG, et al. Efficacy and safety of pegylated interferon base treatment in patients with chronic hepatitis C on dialysis. Eur J Intern Med. 2015 May;26(4):292–296.
   Google Scholar
• Brennan BJ, Xu ZX, Grippo JF. Evaluation of the absolute bioavailability of pegylated interferon alfa-2a after subcutaneous administration to healthy male volunteers: an open-label, randomized, parallel-group study. Clin Ther. 2012 Sep;34(9):1883–1891.
   Google Scholar
• Costa MB, Picon PD, Sander GB, et al. Pharmacokinetics comparison of two pegylated interferon alfa formulations in healthy volunteers. BMC Pharmacol Toxicol. 2018 Jan 4;19(1):1.
   Google Scholar
• Woo ASJ, Kwok R, Ahmed T. Alpha-interferon treatment in hepatitis B. Ann Transl Med. 2017 Apr;5(7):159.
   Google Scholar
• Youngster S, Wang YS, Grace M, et al. Structure, biology, and therapeutic implications of pegylated interferon alpha-2b. Curr Pharm Des. 2002;8(24):2139–2157.
   Google Scholar
• Foster GR. Review article: pegylated interferons: chemical and clinical differences. Aliment Pharmacol Ther. 2004 Oct 15;20(8):825–830.
   Google Scholar
• Bruno R, Sacchi P, Ciappina V, et al. Viral dynamics and pharmacokinetics of peginterferon alpha-2a and peginterferon alpha-2b in naive patients with chronic hepatitis c: a randomized, controlled study. Antivir Ther. 2004 Aug;9(4):491–497.
   Google Scholar
• Formann E, Jessner W, Bennett L, et al. Twice-weekly administration of peginterferon-alpha-2b improves viral kinetics in patients with chronic hepatitis C genotype 1. J Viral Hepat. 2003 Jul;10(4):271–276.
   Google Scholar
• Brennan BJ, Xu ZX, Grippo JF. Effect of peginterferon alfa-2a (40KD) on cytochrome P450 isoenzyme activity. Br J Clin Pharmacol. 2013 Feb;75(2):497–506.
   Google Scholar
• Jonkman JH, Nicholson KG, Farrow PR, et al. Effects of alpha-interferon on theophylline pharmacokinetics and metabolism. Br J Clin Pharmacol. 1989 Jun;27(6):795–802.
   Google Scholar
• Marcellin P, Wursthorn K, Wedemeyer H, et al. Telbivudine plus pegylated interferon alfa-2a in a randomized study in chronic hepatitis B is associated with an unexpected high rate of peripheral neuropathy. J Hepatol. 2015 Jan;62(1):41–47.
   Google Scholar
• Berk SI, Litwin AH, Arnsten JH, et al. Effects of pegylated interferon alfa-2b on the pharmacokinetic and pharmacodynamic properties of methadone: a prospective, nonrandomized, crossover study in patients coinfected with hepatitis C and HIV receiving methadone maintenance treatment. Clin Ther. 2007 Jan;29(1):131–138.
   Google Scholar
• Baron S, Tyring SK, Fleischmann WR, Jr., et al. The interferons. Mechanisms of action and clinical applications. JAMA. 1991 Sep 11;266(10):1375–1383.
   Google Scholar
• Tan G, Song H, Xu F, et al. When Hepatitis B Virus Meets Interferons. Front Microbiol. 2018;9:1611.
   Google Scholar
• Garcia-Garcia I, Gonzalez-Delgado CA, Valenzuela-Silva CM, et al. Pharmacokinetic and pharmacodynamic comparison of two “pegylated” interferon alpha-2 formulations in healthy male volunteers: a randomized, crossover, double-blind study. BMC Pharmacol. 2010 Nov;23(10):15.
   Google Scholar
• Dhalluin C, Ross A, Huber W, et al. Structural, kinetic, and thermodynamic analysis of the binding of the 40 kDa PEG-interferon-alpha2a and its individual positional isomers to the extracellular domain of the receptor IFNAR2. Bioconjug Chem. 2005 May-Jun;16(3):518–527.
   Google Scholar
• Silva M, Poo J, Wagner F, et al. A randomised trial to compare the pharmacokinetic, pharmacodynamic, and antiviral effects of peginterferon alfa-2b and peginterferon alfa-2a in patients with chronic hepatitis C (COMPARE). J Hepatol. 2006 Aug;45(2):204–213.
   Google Scholar
• Bruno R, Sacchi P, Scagnolari C, et al. Pharmacodynamics of peginterferon alpha-2a and peginterferon alpha-2b in interferon-naive patients with chronic hepatitis C: a randomized, controlled study. Aliment Pharmacol Ther. 2007 Aug 1;26(3):369–376.
   Google Scholar
• Howell CD, Dowling TC, Paul M, et al. Peginterferon pharmacokinetics in African American and Caucasian American patients with hepatitis C virus genotype 1 infection. Clin Gastroenterol Hepatol. 2008 May;6(5):575–583.
   Google Scholar
• Lau GK, Piratvisuth T, Luo KX, et al. Peginterferon Alfa-2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N Engl J Med. 2005 Jun 30;352(26):2682–2695.
   Google Scholar
• Marcellin P, Lau GK, Bonino F, et al. Peginterferon alfa-2a alone, lamivudine alone, and the two in combination in patients with HBeAg-negative chronic hepatitis B. N Engl J Med. 2004 Sep 16;351(12):1206–1217.
   Google Scholar
• Buster EH, Flink HJ, Cakaloglu Y, et al. Sustained HBeAg and HBsAg loss after long-term follow-up of HBeAg-positive patients treated with peginterferon alpha-2b. Gastroenterology. 2008 Aug;135(2):459–467.
   Google Scholar
• Buster EH, Flink HJ, Simsek H, et al. Early HBeAg loss during peginterferon alpha-2b therapy predicts HBsAg loss: results of a long-term follow-up study in chronic hepatitis B patients. Am J Gastroenterol. 2009 Oct;104(10):2449–2457.
   Google Scholar
• Sonneveld MJ, Rijckborst V, Boucher CA, et al. Prediction of sustained response to peginterferon alfa-2b for hepatitis B e antigen-positive chronic hepatitis B using on-treatment hepatitis B surface antigen decline. Hepatology. 2010 Oct;52(4):1251–1257.
   Google Scholar
• Chan HL, Leung NW, Hui AY, et al. A randomized, controlled trial of combination therapy for chronic hepatitis B: comparing pegylated interferon-alpha2b and lamivudine with lamivudine alone. Ann Intern Med. 2005 Feb 15;142(4):240–250.
   Google Scholar
• Wong VW, Wong GL, Yan KK, et al. Durability of peginterferon alfa-2b treatment at 5 years in patients with hepatitis B e antigen-positive chronic hepatitis B. Hepatology. 2010 Jun;51(6):1945–1953.
   Google Scholar
• Sun J, Ding H, Chen G, et al. Sustained serological and complete responses in HBeAg-positive patients treated with Peginterferon alfa-2b: a 6-year long-term follow-up of a multicenter, randomized, controlled trial in China. BMC Gastroenterol. 2019 May 2;19(1):65.
   Google Scholar
• Marcellin P, Bonino F, Lau GK, et al. Sustained response of hepatitis B e antigen-negative patients 3 years after treatment with peginterferon alpha-2a. Gastroenterology. 2009 Jun;136(7):2169–2179e1–4.
   Google Scholar
• Marcellin P, Ahn SH, Ma X, et al. Combination of Tenofovir Disoproxil Fumarate and Peginterferon alpha-2a increases loss of hepatitis B surface antigen in patients with chronic hepatitis B. Gastroenterology. 2016 Jan;150(1):134–144 e10.
   Google Scholar
• Lutgehetmann M, Volzt T, Quaas A, et al. Sequential combination therapy leads to biochemical and histological improvement despite low ongoing intrahepatic hepatitis B virus replication. Antivir Ther. 2008;13(1):57–66.
   Google Scholar
• Ning Q, Han M, Sun Y, et al. Switching from entecavir to PegIFN alfa-2a in patients with HBeAg-positive chronic hepatitis B: a randomised open-label trial (OSST trial). J Hepatol. 2014 Oct;61(4):777–784.
   Google Scholar
• Tamaki N, Kurosaki M, Kusakabe A, et al. Hepatitis B surface antigen reduction by switching from long-term nucleoside/nucleotide analogue administration to pegylated interferon. J Viral Hepat. 2017 Aug;24(8):672–678.
   Google Scholar
• Ouzan D, Penaranda G, Joly H, et al. Add-on peg-interferon leads to loss of HBsAg in patients with HBeAg-negative chronic hepatitis and HBV DNA fully suppressed by long-term nucleotide analogs. J Clin Virol. 2013 Dec;58(4):713–717.
   Google Scholar
• Yan L, Zhu C, Li J, et al. Entecavir add-on or switch-to pegylated interferon improves HBsAg clearance in HBe antigen negative chronic hepatitis B patients. Infect Drug Resist. 2018;11:2001–2009.
   Google Scholar
• He LT, Ye XG, Zhou XY. Effect of switching from treatment with nucleos(t)ide analogs to pegylated interferon alpha-2a on virological and serological responses in chronic hepatitis B patients. World J Gastroenterol. 2016 Dec 14;22(46):10210–10218.
   Google Scholar
• Li GJ, Yu YQ, Chen SL, et al. Sequential combination therapy with pegylated interferon leads to loss of hepatitis B surface antigen and hepatitis B e antigen (HBeAg) seroconversion in HBeAg-positive chronic hepatitis B patients receiving long-term entecavir treatment. Antimicrob Agents Chemother. 2015 Jul;59(7):4121–4128.
   Google Scholar
• Allweiss L, Volz T, Lutgehetmann M, et al. Immune cell responses are not required to induce substantial hepatitis B virus antigen decline during pegylated interferon-alpha administration. J Hepatol. 2014 Mar;60(3):500–507.
   Google Scholar
• Wursthorn K, Lutgehetmann M, Dandri M, et al. Peginterferon alpha-2b plus adefovir induce strong cccDNA decline and HBsAg reduction in patients with chronic hepatitis B. Hepatology. 2006 Sep;44(3):675–684.
   Google Scholar
• Hagiwara S, Kudo M, Osaki Y, et al. Impact of peginterferon alpha-2b and entecavir hydrate combination therapy on persistent viral suppression in patients with chronic hepatitis B. J Med Virol. 2013 Jun;85(6):987–995.
   Google Scholar
• Krebs K, Bottinger N, Huang LR, et al. T cells expressing a chimeric antigen receptor that binds hepatitis B virus envelope proteins control virus replication in mice. Gastroenterology. 2013 Aug;145(2):456–465.
   Google Scholar
• Cradick TJ, Keck K, Bradshaw S, et al. Zinc-finger nucleases as a novel therapeutic strategy for targeting hepatitis B virus DNAs. Mol Ther. 2010 May;18(5):947–954.
   Google Scholar
• Chen J, Zhang W, Lin J, et al. An efficient antiviral strategy for targeting hepatitis B virus genome using transcription activator-like effector nucleases. Mol Ther. 2014 Feb;22(2):303–311.
   Google Scholar
• Mali P, Esvelt KM, Church GM. Cas9 as a versatile tool for engineering biology. Nat Methods. 2013;Oct;10(10):957–963.
   Google Scholar
• Ahn SH, Marcellin P, Ma X, et al. Hepatitis B surface antigen loss with Tenofovir Disoproxil Fumarate Plus Peginterferon Alfa-2a: week 120 analysis. Dig Dis Sci. 2018 Dec;63(12):3487–3497.
   Google Scholar
• Lok AS, Zoulim F, Dusheiko G, et al. Hepatitis B cure: from discovery to regulatory approval. J Hepatol. 2017 Oct;67(4):847–861.
   Google Scholar
• Niu C, Li L, Daffis S, et al. Toll-like receptor 7 agonist GS-9620 induces prolonged inhibition of HBV via a type I interferon-dependent mechanism. J Hepatol. 2018 May;68(5):922–931.
   Google Scholar
• Boni C, Vecchi A, Rossi M, et al. TLR7 agonist increases responses of hepatitis B virus-specific T cells and natural killer cells in patients with chronic hepatitis B treated with nucleos(T)Ide analogues. Gastroenterology. 2018 May;154(6):1764–1777 e7.
   Google Scholar
• Agarwal K, Ahn SH, Elkhashab M, et al. Safety and efficacy of vesatolimod (GS-9620) in patients with chronic hepatitis B who are not currently on antiviral treatment. J Viral Hepat. 2018 Nov;25(11):1331–1340.
   Google Scholar
• Janssen HLA, Brunetto MR, Kim YJ, et al. Safety, efficacy and pharmacodynamics of vesatolimod (GS-9620) in virally suppressed patients with chronic hepatitis B. J Hepatol. 2018 Mar;68(3):431–440.
   Google Scholar
• Gane EJ, Lim YS, Gordon SC, et al. The oral toll-like receptor-7 agonist GS-9620 in patients with chronic hepatitis B virus infection. J Hepatol. 2015 Aug;63(2):320–328.
   Google Scholar
• Tsuge M, Uchida T, Hiraga N, et al. Development of a novel site-specific pegylated interferon beta for antiviral therapy of chronic hepatitis B virus. Antimicrob Agents Chemother. 2017 Jun;61(6).
   Google Scholar