Metabolism of Direct-acting Antiviral Agents (DAAs) in Hepatitis C Therapy: A Review of the Literature

Author(s): Ivana Mikolasevic*, Tajana F. Kanizaj, Dorotea Bozic, Petra Puz, Sanja S. Shapeski, Zeljko Puljiz, Delfa Radic-Kristo, Milos Lalovac, Maja Mijic, Bozena Delija, Toni Juric, Ivan Bogadi, Lucija Virovic-Jukic

Journal Name: Current Drug Metabolism

Volume 22 , Issue 2 , 2021


Become EABM
Become Reviewer
Call for Editor

Abstract:

Background: Hepatitis C virus (HCV) infection is still one of the leading causes of chronic liver disease, with chronically infected making up approximately 1% of the global population. Of those infected, 70% (55-85%) will develop chronic HCV infection. Chronic HCV infection causes substantial morbidity and mortality, with complications including cirrhosis, end-stage liver disease, hepatocellular carcinoma, and eventually death.

Objective: Therapeutic options for chronic HCV infection have evolved dramatically since 2014, with a translation from pegylated interferon and ribavirin (associated with suboptimal cure and high treatment-related toxicity) to oral direct-acting antiviral treatment. There are four classes of direct-acting antivirals which differ by their mechanism of action and therapeutic target. They are all pointed to proteins that form the cytoplasmic viral replication complex. Multiple studies have demonstrated that direct-acting antiviral therapy is extremely well tolerated, highly efficacious, with few side effects.

Methods: We performed an indexed MEDLINE search with keywords regarding specific direct-acting antiviral regimes and their pharmacokinetics, drug-drug interactions, and metabolism in specific settings of pregnancy, lactation, liver cirrhosis, liver transplantation and HCC risk, kidney failure and kidney transplantation.

Results: We present a comprehensive overview of specific direct-acting antiviral metabolism and drug-drug interaction issues in different settings.

Conclusion: Despite its complex pharmacokinetics and the possibility of drug-drug interactions, direct-acting antivirals are highly efficacious in providing viral clearance, which is an obvious advantage compared to possible interactions or side effects. They should be administered cautiously in patients with other comorbidities, and with tight control of immunosuppressive therapy.

Keywords: Hepatitis C, direct-acting antivirals, drug-drug interactions, hepatocellular carcinoma, cirrhosis, liver transplantation.

[1]
World Health Organization. Global Hepatitis report. 2017. Available at: https://www.who.int/hepatitis/publications/global-hepatitis-report2017/en
[2]
Shepard, C.W.; Finelli, L.; Alter, M.J. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis., 2005, 5(9), 558-567.
[http://dx.doi.org/10.1016/S1473-3099(05)70216-4] [PMID: 16122679]
[3]
European Association for the Study of the Liver. EASL Recommendations on Treatment of Hepatitis C 2018. J. Hepatol., 2018, 69(2), 461-511.
[http://dx.doi.org/10.1016/j.jhep.2018.03.026] [PMID: 29650333]
[4]
Garfein, R.S.; Vlahov, D.; Galai, N.; Doherty, M.C.; Nelson, K.E. Viral infections in short-term injection drug users: the prevalence of the hepatitis C, hepatitis B, human immunodeficiency, and human T-lymphotropic viruses. Am. J. Public Health, 1996, 86(5), 655-661.
[http://dx.doi.org/10.2105/AJPH.86.5.655] [PMID: 8629715]
[5]
Patrick, D.M.; Buxton, J.A.; Bigham, M.; Mathias, R.G. Public health and hepatitis C. Can. J. Public Health, 2000, 91(Suppl. 1), S18-S21, S19-S23.
[PMID: 11059125]
[6]
Jonas, M.M. Children with hepatitis C. Hepatology, 2002, 36(5)(Suppl. 1), S173-S178.
[PMID: 12407591]
[7]
Mele, A.; Corona, R.; Tosti, M.E.; Palumbo, F.; Moiraghi, A.; Novaco, F.; Galanti, C.; Bernacchia, R.; Ferraro, P. Beauty treatments and risk of parenterally transmitted hepatitis: results from the hepatitis surveillance system in Italy. Scand. J. Infect. Dis., 1995, 27(5), 441-444.
[http://dx.doi.org/10.3109/00365549509047042] [PMID: 8588131]
[8]
Mansell, C.J.; Locarnini, S.A. Epidemiology of hepatitis C in the East. Semin. Liver Dis., 1995, 15(1), 15-32.
[http://dx.doi.org/10.1055/s-2007-1007260] [PMID: 7597442]
[9]
Farci, P.; Alter, H.J.; Govindarajan, S.; Wong, D.C.; Engle, R.; Lesniewski, R.R.; Mushahwar, I.K.; Desai, S.M.; Miller, R.H.; Ogata, N. Lack of protective immunity against reinfection with hepatitis C virus. Science, 1992, 258(5079), 135-140.
[http://dx.doi.org/10.1126/science.1279801] [PMID: 1279801]
[10]
Yuki, N.; Hayashi, N.; Ohkawa, K.; Hagiwara, H.; Oshita, M.; Katayama, K.; Sasaki, Y.; Kasahara, A.; Fusamoto, H.; Kamada, T. The significance of immunoglobulin M antibody response to hepatitis C virus core protein in patients with chronic hepatitis C. Hepatology, 1995, 22(2), 402-406.
[PMID: 7543432]
[11]
Wedemeyer, H.; Hepatitis, C. Sleisenger and Fordtran’s gastrointestinal and liver disease 10th ed. Feldman, M.; Friedman, L.; Brandt, L., Ed; Saunders: Philadelphia, , 2016; pp. 1332-1352.
[12]
Poordad, F.; Dieterich, D. Treating hepatitis C: current standard of care and emerging direct-acting antiviral agents. J. Viral Hepat., 2012, 19(7), 449-464.
[http://dx.doi.org/10.1111/j.1365-2893.2012.01617.x] [PMID: 22676357]
[13]
Zeuzem, S.; Dusheiko, G.M.; Salupere, R.; Mangia, A.; Flisiak, R.; Hyland, R.H.; Illeperuma, A.; Svarovskaia, E.; Brainard, D.M.; Symonds, W.T.; Subramanian, G.M.; McHutchison, J.G.; Weiland, O.; Reesink, H.W.; Ferenci, P.; Hézode, C.; Esteban, R. VALENCE Investigators. SOF and ribavirin in HCV genotypes 2 and 3. N. Engl. J. Med., 2014, 370, 1993-2001.
[http://dx.doi.org/10.1056/NEJMoa1316145] [PMID: 24795201]
[14]
Kowdley, K.V.; Gordon, S.C.; Reddy, K.R.; Rossaro, L.; Bernstein, D.E.; Lawitz, E.; Shiffman, M.L.; Schiff, E.; Ghalib, R.; Ryan, M.; Rustgi, V.; Chojkier, M.; Herring, R.; Di Bisceglie, A.M.; Pockros, P.J.; Subramanian, G.M.; An, D.; Svarovskaia, E.; Hyland, R.H.; Pang, P.S.; Symonds, W.T.; McHutchison, J.G.; Muir, A.J.; Pound, D.; Fried, M.W. ION-3 Investigators. LDV and SOF for 8 or 12 weeks for chronic HCV without cirrhosis. N. Engl. J. Med., 2014, 370, 1879-1888.
[http://dx.doi.org/10.1056/NEJMoa1402355] [PMID: 24720702]
[15]
Nelson, D.R.; Cooper, J.N.; Lalezari, J.P.; Lawitz, E.; Pockros, P.J.; Gitlin, N.; Freilich, B.F.; Younes, Z.H.; Harlan, W.; Ghalib, R.; Oguchi, G.; Thuluvath, P.J.; Ortiz-Lasanta, G.; Rabinovitz, M.; Bernstein, D.; Bennett, M.; Hawkins, T.; Ravendhran, N.; Sheikh, A.M.; Varunok, P.; Kowdley, K.V.; Hennicken, D.; McPhee, F.; Rana, K.; Hughes, E.A. ALLY-3 Study Team. All-oral 12-week treatment with daclatasvir plus sofosbuvir in patients with hepatitis C virus genotype 3 infection: ALLY-3 phase III study. Hepatology, 2015, 61(4), 1127-1135.
[http://dx.doi.org/10.1002/hep.27726] [PMID: 25614962]
[16]
Younossi, Z.M.; Stepanova, M.; Henry, L.; Nader, F.; Hunt, S. An in-depth analysis of patient-reported outcomes in patients with chronic hepatitis C treated with different anti-viral regimens. Am. J. Gastroenterol., 2016, 111(6), 808-816.
[http://dx.doi.org/10.1038/ajg.2016.99] [PMID: 27021197]
[17]
Lerat, H.; Hollinger, F.B. Hepatitis C virus (HCV) occult infection or occult HCV RNA detection? J. Infect. Dis., 2004, 189(1), 3-6.
[http://dx.doi.org/10.1086/380203] [PMID: 14702146]
[18]
Pham, T.N.; King, D.; Macparland, S.A.; McGrath, J.S.; Reddy, S.B.; Bursey, F.R.; Michalak, T.I. Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection. Gastroenterology, 2008, 134(3), 812-822.
[http://dx.doi.org/10.1053/j.gastro.2007.12.011] [PMID: 18243182]
[19]
Dubuisson, J. Hepatitis C virus proteins. World J. Gastroenterol., 2007, 13(17), 2406-2415.
[http://dx.doi.org/10.3748/wjg.v13.i17.2406] [PMID: 17552023]
[20]
Powdrill, M.H.; Tchesnokov, E.P.; Kozak, R.A.; Russell, R.S.; Martin, R.; Svarovskaia, E.S.; Mo, H.; Kouyos, R.D.; Götte, M. Contribution of a mutational bias in hepatitis C virus replication to the genetic barrier in the development of drug resistance. Proc. Natl. Acad. Sci. USA, 2011, 108(51), 20509-20513.
[http://dx.doi.org/10.1073/pnas.1105797108] [PMID: 22135458]
[21]
Smolders, E.J.; Ter Horst, P.J.G.; Wolters, S.; Burger, D.M. Cardiovascular risk management and hepatitis C: combining drugs. Clin. Pharmacokinet., 2019, 58(5), 565-592.
[http://dx.doi.org/10.1007/s40262-018-0710-1] [PMID: 30259390]
[22]
University of Liverpool. HEP drug interactions. Available at: https://www.hep-druginteractions.org/checker
[23]
Talavera Pons, S.; Boyer, A.; Lamblin, G.; Chennell, P.; Châtenet, F-T.; Nicolas, C.; Sautou, V.; Abergel, A. Managing drug-drug interactions with new direct-acting antiviral agents in chronic hepatitis C. Br. J. Clin. Pharmacol., 2017, 83(2), 269-293.
[http://dx.doi.org/10.1111/bcp.13095] [PMID: 27530469]
[24]
Smolders, E.J.; Jansen, A.M.E.; Ter Horst, P.G.J.; Rockstroh, J.; Back, D.J.; Burger, D.M. Viral hepatitis C therapy: pharmacokinetic and pharmacodynamic considerations: a 2019 update. Clin. Pharmacokinet., 2019, 58(10), 1237-1263.
[http://dx.doi.org/10.1007/s40262-019-00774-0] [PMID: 31114957]
[25]
Néant, N.; Solas, C. Drug-drug interactions potential of direct-acting antivirals for the treatment of chronic hepatitis C virus infection. Int. J. Antimicrob. Agents, 2020, 56(1), 105571. [Online early access].
[http://dx.doi.org/10.1016/j.ijantimicag.2018.10.014] [PMID: 30394302]
[26]
Höner Zu Siederdissen, C.; Maasoumy, B.; Marra, F.; Deterding, K.; Port, K.; Manns, M.P.; Cornberg, M.; Back, D.; Wedemeyer, H. Drug-drug interactions with novel all oral interferon-free antiviral agents in a large real- world cohort. Clin. Infect. Dis., 2016, 62(5), 561-567.
[http://dx.doi.org/10.1093/cid/civ973] [PMID: 26611779]
[27]
Kondili, L.A.; Gaeta, G.B.; Ieluzzi, D.; Zignego, A.L.; Monti, M.; Gori, A.; Soria, A.; Raimondo, G.; Filomia, R.; Di Leo, A.; Iannone, A.; Massari, M.; Corsini, R.; Gulminetti, R.; Gatti Comini, A.; Toniutto, P.; Dissegna, D.; Russo, F.P.; Zanetto, A.; Rumi, M.G.; Brancaccio, G.; Danieli, E.; Brunetto, M.R.; Weimer, L.E.; Quaranta, M.G.; Vella, S.; Puoti, M. Real-life data on potential drug-drug interactions in patients with chronic hepatitis C viral infection undergoing antiviral therapy with interferon-free DAAs in the PITER Cohort Study. PLoS One, 2017, 12(2), e0172159. [Online].
[http://dx.doi.org/10.1371/journal.pone.0172159] [PMID: 28245248]
[28]
Langness, J.A.; Nguyen, M.; Wieland, A.; Everson, G.T.; Kiser, J.J. Optimizing hepatitis C virus treatment through pharmacist interventions: Identification and management of drug-drug interactions. World J. Gastroenterol., 2017, 23(9), 1618-1626.
[http://dx.doi.org/10.3748/wjg.v23.i9.1618] [PMID: 28321163]
[29]
Ottman, A.A.; Townsend, M.L.; Hashem, M.G.; DiMondi, V.P.; Britt, R.B. Incidence of drug interactions identified by clinical pharmacists in veterans initiating treatment for chronic hepatitis C infection. Ann. Pharmacother., 2018, 52(8), 763-768.
[http://dx.doi.org/10.1177/1060028018766507] [PMID: 29577765]
[30]
Vermehren, J.; Peiffer, K.H.; Welsch, C.; Grammatikos, G.; Welker, M.W.; Weiler, N.; Zeuzem, S.; Welzel, T.M.; Sarrazin, C. The efficacy and safety of direct acting antiviral treatment and clinical significance of drug-drug interactions in elderly patients with chronic hepatitis C virus infection. Aliment. Pharmacol. Ther., 2016, 44(8), 856-865.
[http://dx.doi.org/10.1111/apt.13769] [PMID: 27549000]
[31]
Keast, S.L.; Holderread, B.; Cothran, T.; Skrepnek, G.H.; Hepatitis, C. Hepatitis C direct-acting antiviral treatment selection, treatment failure, and use of drug-drug interactions in a state medicaid program. J. Manag. Care Spec. Pharm., 2019, 25(11), 1261-1267.
[http://dx.doi.org/10.18553/jmcp.2019.25.11.1261] [PMID: 31663456]
[32]
Garrison, K.L.; German, P.; Mogalian, E.; Mathias, A. The drug-drug interaction potential of antiviral agents for the treatment of chronic hepatitis C infection. Drug Metab. Dispos., 2018, 46(8), 1212-1225.
[http://dx.doi.org/10.1124/dmd.117.079038] [PMID: 29695614]
[33]
Yu, G.; Zheng, Y.; Yu, Y.; Li, G.F.; Derendorf, H. Gastric-acid-mediated drug-drug interactions with direct-acting antiviral medications for hepatitis C virus infection: clinical relevance and mitigation strategies. Drug Discov. Today, 2019, 24(3), 845-857.
[http://dx.doi.org/10.1016/j.drudis.2019.01.003] [PMID: 30648608]
[34]
Ing Lorenzini, K.; Girardin, F. Direct-acting antiviral interactions with opioids, alcohol or illicit drugs of abuse in HCV-infected patients. Liver Int., 2020, 40(1), 32-44.
[http://dx.doi.org/10.1111/liv.14283] [PMID: 31654604]
[35]
Christensen, S.; Buggisch, P.; Mauss, S.; Böker, K.H.; Müller, T.; Klinker, H.; Zimmermann, T.; Serfert, Y.; Weber, B.; Reimer, J.; Wedemeyer, H. Alcohol and cannabis consumption does not diminish cure rates in a real- world cohort of chronic hepatitis C virus infected patients on opioid substitution therapy-data from the German Hepatitis C-Registry [DHC-R]. Subst. Abuse., 2019, 28, 13.
[36]
Kosloski, M.P.; Zhao, W.; Asatryan, A.; Kort, J.; Geoffroy, P.; Liu, W. No clinically relevant drug-drug interactions between methadone or buprenorphine-naloxone and antiviral combination GLE and PIB. Antimicrob. Agents Chemother., 2017, 61, e00958-17.
[37]
Grebely, J.; Dore, G.J.; Alami, N.N.; Conway, B.; Dillon, J.F.; Gschwantler, M.; Felizarta, F.; Hézode, C.; Tomasiewicz, K.; Fredrick, L.M.; Dumas, E.O. Safety and efficacy of GLE/PIB in patients with chronic hepatitis C genotypes 1-6 receiving opioid substitution therapy. Int. J. Drug Policy, 2019, 66, 73-79.
[http://dx.doi.org/10.1016/j.drugpo.2019.01.011] [PMID: 30735896]
[38]
Tsui, J.I.; Williams, E.C.; Green, P.K.; Berry, K.; Su, F.; Ioannou, G.N. Alcohol use and hepatitis C virus treatment outcomes among patients receiving direct antiviral agents. Drug Alcohol Depend., 2016, 169, 101-109.
[http://dx.doi.org/10.1016/j.drugalcdep.2016.10.021] [PMID: 27810652]
[39]
Yeoh, S.W. Iatrogenic cushing syndrome from interaction between ritonavir and oral budesonide during direct acting antiviral hepatitis C therapy. J. Clin. Exp. Hepatol., 2016, 6(3), 246-249.
[http://dx.doi.org/10.1016/j.jceh.2016.05.006] [PMID: 27746623]
[40]
Hofstraat, S.H.I.; Falla, A.M.; Duffell, E.F.; Hahné, S.J.M.; Amato-Gauci, A.J.; Veldhuijzen, I.K.; Tavoschi, L. Current prevalence of chronic hepatitis B and C virus infection in the general population, blood donors and pregnant women in the EU/EEA: a systematic review. Epidemiol. Infect., 2017, 145(14), 2873-2885.
[http://dx.doi.org/10.1017/S0950268817001947] [PMID: 28891457]
[41]
Benova, L.; Mohamoud, Y.A.; Calvert, C.; Abu-Raddad, L.J. Vertical transmission of hepatitis C virus: systematic review and meta-analysis. Clin. Infect. Dis., 2014, 59(6), 765-773.
[http://dx.doi.org/10.1093/cid/ciu447] [PMID: 24928290]
[42]
Spera, A.M.; Eldin, T.K.; Tosone, G.; Orlando, R. Antiviral therapy for hepatitis C: Has anything changed for pregnant/lactating women? World J. Hepatol., 2016, 8(12), 557-565.
[http://dx.doi.org/10.4254/wjh.v8.i12.557] [PMID: 27134703]
[43]
Feghali, M.; Venkataramanan, R.; Caritis, S. Pharmacokinetics of drugs in pregnancy. Semin. Perinatol., 2015, 39(7), 512-519.
[http://dx.doi.org/10.1053/j.semperi.2015.08.003] [PMID: 26452316]
[44]
Freriksen, J.J.M.; van Seyen, M.; Judd, A.; Gibb, D.M.; Collins, I.J.; Greupink, R.; Russel, F.G.M.; Drenth, J.P.H.; Colbers, A.; Burger, D.M. Review article: direct-acting antivirals for the treatment of HCV during pregnancy and lactation - implications for maternal dosing, foetal exposure, and safety for mother and child. Aliment. Pharmacol. Ther., 2019, 50(7), 738-750.
[http://dx.doi.org/10.1111/apt.15476] [PMID: 31448450]
[45]
Schalkwijk, S.; Greupink, R.; Burger, D. Free dug concentrations in pregnancy: Bound to measure unbound? Br. J. Clin. Pharmacol., 2017, 83(12), 2595-2598.
[http://dx.doi.org/10.1111/bcp.13432] [PMID: 28983934]
[46]
Newton, E.R.; Hale, T.W. Drugs in breast milk. Clin. Obstet. Gynecol., 2015, 58(4), 868-884.
[http://dx.doi.org/10.1097/GRF.0000000000000142] [PMID: 26457856]
[47]
Belli, L.S.; Duvoux, C.; Berenguer, M.; Berg, T.; Coilly, A.; Colle, I.; Fagiuoli, S.; Khoo, S.; Pageaux, G.P.; Puoti, M.; Samuel, D.; Strazzabosco, M. ELITA consensus statements on the use of DAAs in liver transplant candidates and recipients. J. Hepatol., 2017, 67(3), 585-602.
[http://dx.doi.org/10.1016/j.jhep.2017.03.006] [PMID: 28323126]
[48]
AASLD/IDSA. HCV guidance: recommendations for testing, managing, and treating hepatitis C. 2019, Available at: https://www.hcvguidelines.org/sites/default/files/full-guidance-pdf/200206_HCVGuidance_November_06_2019_a.pdf
[49]
Manns, M.; Samuel, D.; Gane, E.J.; Mutimer, D.; McCaughan, G.; Buti, M.; Prieto, M.; Calleja, J.L.; Peck-Radosavljevic, M.; Müllhaupt, B.; Agarwal, K.; Angus, P.; Yoshida, E.M.; Colombo, M.; Rizzetto, M.; Dvory- Sobol, H.; Denning, J.; Arterburn, S.; Pang, P.S.; Brainard, D.; McHutchison, J.G.; Dufour, J.F.; Van Vlierberghe, H.; van Hoek, B.; Forns, X. SOLAR-2 investigators. Ledipasvir and sofosbuvir plus ribavirin in patients with genotype 1 or 4 hepatitis C virus infection and advanced liver disease: a multicentre, open-label, randomised, phase 2 trial. Lancet Infect. Dis., 2016, 16(6), 685-697.
[PMID: 26907736]
[50]
Jacobson, I.M.; Poordad, F.; Firpi-Morell, R.; Everson, G.T. Efficacy and safety of GZR and EBR in hepatitis C genotype 1-infected patients with Child-Pugh class B cirrhosis (C-SALT part A). J. Hepatol., 2015, 62(Suppl. 2), S193-S194.
[51]
Belli, L.S.; Berenguer, M.; Cortesi, P.A.; Strazzabosco, M.; Rockenschaub, S.R.; Martini, S.; Morelli, C.; Donato, F.; Volpes, R.; Pageaux, G.P.; Coilly, A.; Fagiuoli, S.; Amaddeo, G.; Perricone, G.; Vinaixa, C.; Berlakovich, G.; Facchetti, R.; Polak, W.; Muiesan, P.; Duvoux, C. European Liver and Intestine Association (ELITA). Delisting of liver transplant candidates with chronic hepatitis C after viral eradication: A European study. J. Hepatol., 2016, 65(3), 524-531.
[PMID: 27212241]
[52]
Charlton, M.; Everson, G.T.; Flamm, S.L.; Kumar, P.; Landis, C.; Brown, R.S.; Fried, M.W.; Terrault, N.A.; O’Leary, J.G.; Vargas, H.E.; Kuo, A.; Schiff, E.; Sulkowski, M.S.; Gilroy, R.; Watt, K.D.; Brown, K.; Kwo, P.; Pungpapong, S.; Korenblat, K.M.; Muir, A.J.; Teperman, L.; Fontana, R.J.; Denning, J.; Arterburn, S.; Dvory-Sobol, H.; Brandt-Sarif, T.; Pang, P.S.; McHutchison, J.G.; Reddy, K.R.; Afdhal, N. SOLAR-1 Investigators. LDV and SOF plus ribavirin for treatment of HCV infection in patients with advanced liver disease. Gastroenterology, 2015, 149, 649-659.
[PMID: 25985734]
[53]
Chhatwal, J.; Samur, S.; Kues, B.; Ayer, T.; Roberts, M.S.; Kanwal, F.; Hur, C.; Donnell, D.M.; Chung, R.T. Optimal timing of hepatitis C treatment for patients on the liver transplant waiting list. Hepatology, 2017, 65(3), 777-788.
[PMID: 27906468]
[54]
Fabrizi, F.; Verdesca, S.; Messa, P.; Martin, P. Hepatitis C virus infection increases the risk of developing chronic kidney disease: a systematic review and meta-analysis. Dig. Dis. Sci., 2015, 60(12), 3801-3813.
[http://dx.doi.org/10.1007/s10620-015-3801-y] [PMID: 26195311]
[55]
Jadoul, M.; Bieber, B.A.; Martin, P.; Akiba, T.; Nwankwo, C.; Arduino, J.M.; Goodkin, D.A.; Pisoni, R.L. Prevalence, incidence, and risk factors for hepatitis C virus infection in hemodialysis patients. Kidney Int., 2019, 95(4), 939-947.
[http://dx.doi.org/10.1016/j.kint.2018.11.038] [PMID: 30904068]
[56]
Söderholm, J.; Millbourn, C.; Büsch, K.; Kövamees, J.; Schvarcz, R.; Lindahl, K.; Bruchfeld, A. Higher risk of renal disease in chronic hepatitis C patients: Antiviral therapy survival benefit in patients on hemodialysis. J. Hepatol., 2018, 68(5), 904-911.
[http://dx.doi.org/10.1016/j.jhep.2017.12.003] [PMID: 29233630]
[57]
van der Meer, A.J.; Veldt, B.J.; Feld, J.J.; Wedemeyer, H.; Dufour, J.F.; Lammert, F.; Duarte-Rojo, A.; Manns, M.P.; Zeuzem, S.; Hofmann, W.P.; de Knegt, R.J.; Hansen, B.E.; Janssen, H.L. The number needed to treat to prevent mortality and cirrhosis-related complications among patients with cirrhosis and HCV genotype 1 infection. J. Viral Hepat., 2014, 21(8), 568-577.
[http://dx.doi.org/10.1111/jvh.12185] [PMID: 24118177]
[58]
Saxena, V1.; Khungar, V.; Verna, EC.; Levitsky, J.; Brown, RS Jr.; Hassan, MA.; Sulkowski, MS.; O’Leary, JG.; Koraishy, F.; Galati, JS.; Kuo, AA.; Vainorius, M.; Akushevich, L.; Nelson, DR.; Fried, MW.; Terrault, N.; Reddy, KR. Safety and efficacy of current direct-acting antiviral regimens in kidney and liver transplant recipients with hepatitis C: Results from the HCV-TARGET study. Hepatology, 2017, 66, 1090-1101.
[59]
Cohen-Bucay, A.; Francis, J.M.; Gordon, C.E. Timing of hepatitis C virus infection treatment in kidney transplant candidates. Hemodial. Int., 2018, 22(Suppl. 1), S61-S70.
[http://dx.doi.org/10.1111/hdi.12643] [PMID: 29694723]
[60]
Reig, M.; Mariño, Z.; Perelló, C.; Iñarrairaegui, M.; Ribeiro, A.; Lens, S.; Díaz, A.; Vilana, R.; Darnell, A.; Varela, M.; Sangro, B.; Calleja, J.L.; Forns, X.; Bruix, J. Unexpected high rate of early tumor recurrence in patients with HCV-related HCC undergoing interferon-free therapy. J. Hepatol., 2016, 65(4), 719-726.
[http://dx.doi.org/10.1016/j.jhep.2016.04.008] [PMID: 27084592]
[61]
Conti, F.; Buonfiglioli, F.; Scuteri, A.; Crespi, C.; Bolondi, L.; Caraceni, P.; Foschi, F.G.; Lenzi, M.; Mazzella, G.; Verucchi, G.; Andreone, P.; Brillanti, S. Early occurrence and recurrence of hepatocellular carcinoma in HCV-related cirrhosis treated with direct-acting antivirals. J. Hepatol., 2016, 65(4), 727-733.
[http://dx.doi.org/10.1016/j.jhep.2016.06.015] [PMID: 27349488]
[62]
Butt, A.S.; Sharif, F.; Abid, S. Impact of direct acting antivirals on occurrence and recurrence of hepatocellular carcinoma: biologically plausible or an epiphenomenon? World J. Hepatol., 2018, 10(2), 267-276.
[http://dx.doi.org/10.4254/wjh.v10.i2.267] [PMID: 29527262]
[63]
Faillaci, F.; Marzi, L.; Critelli, R.; Milosa, F.; Schepis, F.; Turola, E.; Andreani, S.; Vandelli, G.; Bernabucci, V.; Lei, B.; D’Ambrosio, F.; Bristot, L.; Cavalletto, L.; Chemello, L.; Sighinolfi, P.; Manni, P.; Maiorana, A.; Caporali, C.; Bianchini, M.; Marsico, M.; Turco, L.; de Maria, N.; Del Buono, M.; Todesca, P.; di Lena, L.; Romagnoli, D.; Magistri, P.; di Benedetto, F.; Bruno, S.; Taliani, G.; Giannelli, G.; Martinez-Chantar, M.L.; Villa, E. Liver angiopoietin is a key predictor of de novo or recurrent hepatocellular cancer after hepatitis C virus direct-acting antivirals. Hepatology, 2018, 68(3), 1010-1024.
[http://dx.doi.org/10.1002/hep.29911] [PMID: 29604220]
[64]
Debes, J.D.; van Tilborg, M.; Groothuismink, Z.M.A.; Hansen, B.E.; Schulze Zur Wiesch, J.; von Felden, J.; de Knegt, R.J.; Boonstra, A. Levels of cytokines in serum associate with development of hepatocellular carcinoma in patients with HCV infection treated with direct-acting antivirals. Gastroenterology, 2018, 154(3), 515-517.e3.
[http://dx.doi.org/10.1053/j.gastro.2017.10.035] [PMID: 29102620]
[65]
Rutledge, S.M.; Zheng, H.; Li, D.K.; Chung, R.T. No evidence for higher rates of hepatocellular carcinoma after direct-acting antiviral treatment: a meta-analysis. Hepatoma Res., 2019, 5, 31.
[http://dx.doi.org/10.20517/2394-5079.2019.19]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 22
ISSUE: 2
Year: 2021
Published on: 14 December, 2020
Page: [89 - 98]
Pages: 10
DOI: 10.2174/1389200221999201214224126
Price: $65

Article Metrics

PDF: 46
HTML: 1