Treatment of HCV-related Liver Disease in the Dialysis Population: A Novel Challenge for Clinical Nephrologists

Choo Q.L. , Kuo G. , Weiner A.J. , Overby L.R. , Bradley D.W. , Houghton M. . Isolation of a cDNA clone derived from a blood-borne non-A non-B viral hepatitis genome. Science 1989; 244: 359–61.

Kuo G. , Choo Q.L. , Alter H.J. . An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 1989; 244: 362–4.

Alter M.J. , Kruszon-Moran D. , Nainan O.V. . The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med 1999; 341: 556–62.

Schafer D.F. , Sorrell M.F. . Conquering hepatitis C, step by step (Editorial). N Engl J Med 2000; 343: 1723–4.

Hoofnagle J.H. , Mullen K.D. , Jones D.B. . Treatment of chronic non-A, non-B hepatitis with recombinant human alpha interferon. N Engl J Med 1986; 315: 1575–8.

Ellis M.E. , Alfurayh O. , Halim M.A. . Chronic non-A, non-B hepatitis complicated by end stage renal failure treated with recombinant interpheron alpha. J Hepatol 1993; 18: 210–6.

Fernandez J.L. , Rendo P. , Del Pino N. , Viola L. , the Nephrologists's Group for the study of HCV infection. A double-blind controlled trial of recombinant interferon alfa-2b in haemodialysis patients with chronic hepatitis C virus infection and abnormal aminotransferase levels. J Viral Hepatitis 1997; 4: 113–9.

Campistol J.M. , Esforzado N. , Martinez J. . Efficacy and tolerance of interferon alfa2b in the treatment of chronic hepatitis C virus in haemodialysis patients. Pre- and post-renal transplantation assessment. Nephrol Dial Transplant 1999; 14: 2074–9.

Koenig P. , Vogel W. , Umlauft F. . Interferon treatment for chronic hepatitis C virus infection in uremic patients. Kidney Int 1994; 45: 1507–9.

Pol S. , Thiers V. , Carnot F. , Zins B. , Romeo R. , Berthelot P. , Brechot C. . Efficacy and tolerance of alfa-2b interferon therapy on HCV infection of hemodialyzed patients. Kidney Int 1995; 47: 1412–8.

Duarte R. , Huraib S. , Said R. . Interpheron-alpha facilitates renal transplantation in hemodialysis patients with chronic viral hepatitis. Am J Kidney Dis 1995; 25: 40–5.

Okuda K. , Hayashi H. , Yokoseki K. , Kondo T. , Kashima T. , Irie Y. . Interferon treatment for chronic hepatitis C in hemodialysis patients: suggestions based on a small series. J Gastroenterol Hepatol 1995; 10: 616–20.

Raptopoulou-Gigi M. , Spaia S. , Garifallos A. . Interferon alfa2b treatment of chronic hepatitis C in haemodialysis patients. Nephrol Dial Transplant 1995; 10: 1834–7.

Simsek H. . Interferon-alpha treatment of haemodialysis patients with chronic viral hepatitis and its impact on kidney transplantation (Letter). Nephrol Dial Transplant 1996; 11: 912–3.

Chan T.M. , Wu P.C. , Lau J.Y.N. , Lok A.S.F. , Lai C.L. , Cheng I.K.P. . Interferon treatment for hepatitis C virus infection in patients on haemodialysis. Nephrol Dial Transplant 1997; 12: 1414–9.

Izopet J. , Rostaing L. , Moussion F. . High rate of hepatitis C virus clearance in hemodialysis patients after interferontherapy. J Infect Dis 1997; 176: 1614–7.

Huraib S. , Tanimu D. , Romeh S.A. . Interferon-alpha in chronic hepatitis C infection in dialysis patients. Am J Kidney Dis 1999; 34: 55–60.

Espinosa M. , Rodriguez M. , Martin-Malo A. . Interferon therapy in hemodialysis patients with chronic hepatitis C virus infection induces a high rate of long-term sustained virological and biochemical response. Clin Nephrol 2001; 55: 220–6.

Tokars J.I. , Miller E.R. , Alter M.J. , Arduino M.J. . National surveillance of dialysis-associated diseases in the United States, 1997. Semin Dial 2000; 13: 75–85.

Salama G. , Rostaing L. , Sandres K. , Izopet J. . Hepatitis C virus infection in French hemodialysis units: a multicenter study. J Med Virol 2000; 61: 44–51.

Limido A. , Conte F. , Malberti F. , Spotti D. , Marcelli D. , Locatelli F. . Prevention of hepatitis B (HBV) and C (HCV) in Lombardy: data from Regional Dialysis and Transplant Registry (RLDT). ERA-EDTA Abstracts 2000; 150.

Schneeberger P.M. , Keur I. , van der VIet W. . Hepatitis C virus infections in dialysis centers in the Netherlands: a national survey by serological and molecular methods. J Clin Microbiol 1998; 36: 1711–5.

AI-Ghamdi S.M.G. , AI-Harbi A.S. . Hepatitis C virus sero-status in hemodialysis patients returning from holiday: another risk factor for HCV transmission. Saudi J Kidney Transplant 2001; 12: 14–20.

Hassan A.A. , Khalil R. . Hepatitis C in dialysis patients in Egypt: Relationship to dialysis duration, blood transfusion, and liver disease. Saudi J Kidney Dis Transplant 2000; 11: 72–5.

Sayner A.A. , Zeytinoglu A. , Ozkahya M. . HCV infection in haemodialysis and CAPD patients (Letter). Nephrol Dial Transplant 1998; 14: 256–7.

Covic A. , lancu L. , Apetrei M. . Hepatitis C virus infection in haemodialysis patients from Moldavia. Nephrol Dial Transplant 1999; 14: 40–5.

Todorov V. , Boneva R. , Ilieva P. , Doichinova T. , Donchev M. . High prevalence of hepatitis C virus infection in one dialysis center in Bulgaria (Letter). Nephron 1998; 79: 222–3.

Djordjevic V. , Stojanovic K. , Stojanovic M. , Stefanovic V. . Prevention of nosocomial transmission of hepatitis C infection in a hemodialysis unit. A prospective study. Int J Artif Organs 2000; 23: 181–8.

Hoofnagle H.J. , Lau D. . Chronic viral hepatitis- benefits of current therapies (Editorial). N Engl J Med 1996; 334: 1470–1.

Perrillo R P. , Schiff E.R. , Davis G.L. . A randomized controlled trial of interferon alfa-2b alone and after prednisone withdrawal for the treatment of chronic hepatitis B. N Engl J Med 1989; 323: 295–301.

Davis G.L. , Balart L.A. , Schiff E.R. . Treatment of chronic hepatitis C with recombinant interferon alfa. A multicenter randomized, controlled trial. N Engl J Med 1989; 321: 1501–6.

Di Bisceglie A.M. , Martin P. , Kassianides C. . Recombinant interferon alfa therapy for chronic hepatitis C. A randomized, double-blind, placebo-controlled trial. N Engl J Med 1989 321: 1506–10.

lsaacs A. , Lindenmann J. . Virus interference, I. The interferon. Proc R Soc London (Biol) 1957; 147: 258–67.

Gresser I. , Bourali C. . Antitumor effects of interferon preparations in mice. J Natl Cancer Inst 1970; 45: 365.

Kimmel P.L. , Abraham A.A. , Phillips T.M. . Membranoproliferative glomerulonephritis in a patient treated with interferon-alfa for human immunodeficiency virus infection. Am J Kidney Dis 1994; 24: 858–63.

Badid C. , McGregor B. , Faivre J.M. . Renal thrombotic microangiopathy induced by interferon-alfa. Nephrol Dial Transplant 2001; 16: 846–8.

Jadoul M. , Piessevaux H. , Ferrant A. , Cosyns J.P. , van Ypersele de Strihou C. Renal thrombotic microangiopathy in patients with chronic myelogenous leukaemia treated with interferon alfa-2b. Nephrol Dial Transplant 1995; 10: 111–3.

Lindsay K. . Therapy of chronic hepatitis C: Overview. Hepatology 1997; 26: 71S–7S.

Desmet V.J. , Gerber M. , Hoofnagle J.H. , Manns M. , Scheuer P.J. . Classification of chronic hepatitis: Diagnosis, grading and staging. Hepatology 1994; 19: 1513–20.

Marcellin P. , Boyer N. , Gervais A. . Long-term histologic improvement and loss of detectable intrahepatic HCV RNA in patients with chronic hepatitis C and sustained response to interferon alfa therapy. Ann Intern Med 1997; 127: 875–81.

Lau D.T.Y. , Klemer D.E. , Ghany M.G. , Park Y. , Schmid P. , Hoofnagle J.H. . 10-year follow-up after interferon-alfa therapy for chronic hepatitis C. Hepatology 1998; 28: 1121–7.

Chemello L. , Cavalletto L. , Casarin C. . Persistent hepatitis C viremia predicts late relapse after sustained response to interferon-alfa in chronic hepatitis C. Ann Intern Med 1996; 124: 1058–60.

Pawlotsky J.M. . Hepatitis C virus resistance to antiviral therapy (Editorial). Hepatology 2000; 32: 889–96.

Rostaing L. , Modesto A. , Baron E. . Acute renal failure in kidney transplant patients treated with interferon alpha 2b for chronic hepatitis C. Nephron 1996; 74: 512–6.

Magnone M. , Magnone J.M. , Holley J.L. . Interferon-alpha induces acute renal allograft rejection. Transplantation 1995; 59: 1068–70.

Lam N.P. , Neumann A.U. , Gretch D.R. , Wiley T.E. , Perelson A.S. , Layden T.J. . Dose-dependent acute clearance of hepatitis C virus genotype 1 virus with interferon alfa. Hepatology 1997; 26: 226–31.

Poynard T. , Leroy V. , Cohard M. . Metaanalysis of interferon randomized trials in the treatment of viral hepatitis C: effects of dose and duration. Hepatology 1996; 24: 778–89.

Poynard T. , Marcellin P. , Lee S.S. . Randomised trial of interferon alfa2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alfa2b placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. Lancet 1998; 352: 1426–32.

Rajender Reddy K. , Hoofnagle J. , Tong M. . Racial differences in responders to therapy with interferon in chronic hepatitis C. Hepatology 1999; 30: 787–93.

Lam N P. , Pitrak D. , Speralakis R. , Lau A.H. , Wiley T.E. , Layden T.J. . Effect of obesity on pharmacokinetics and biologic effect of interferon-alpha in hepatitis C. Dig Dis Sd 1997; 42: 178–85.

Schiff E.R. . The alcoholic patient with hepatitis C virus infection. Am J Med 1999; 107: 95S–99S.

Degos F. . Hepatitis C and alcohol. J Hepatol 1999; 31(suppl. 1): 113–8.

Mizokami M. , Onto E. , Gibo Y. . Genotype, serum level of hepatitis C virus RNA and liver histology as predictors of response to interferon-alfa therapy in Japanese patients with chronic hepatitis C. Liver 1996; 16: 23–7.

National Institutes of Health Consensus Development Conference Panel Statement. Management of hepatitis C. Hepatology 1997; 26(suppl. 1): 122S–127S.

EASL International Consensus Conference on Hepatitis C. Consensus Statement. J Hepatol 1999; 30: 956–61.

Silverman A.L. , Piquette D.L. , Filipiak C.L. , Neill J.S. , Bayati N. , Gordon S.C. . Alfa-interferon treatment of HCV RNA positive patients with normal or near-normal ALT levels. Am J Gastroenterol 1997; 92: 1793–5.

Van Thiel D.H. , Caraceni P. , Molloy P.J. , Hassanein T. , Gurakar A. , Friedlander L. . Chronic hepatitis C in patients with normal or near normal alanine aminotransferase levels: the role of interpheron alpha 2b therapy. J Hepatol 1995; 23: 503–8.

Gordon S.C. , Fang J.W.S. , Silverman A.L. , McHutchison J.G. , Albrecht J.K. . The significance of baseline serum alanine aminotransferase on pretreatment disease characteristics and response to antiviral therapy in chronic hepatitis C. Hepatology 2000; 32: 400–4.

Yamada G. , Takatani M. , Kishi F. . Efficacy of interferon alfa therapy in chronic hepatitis C patients depends primarily on hepatitis C virus RNA level. Hepatology 1995; 22: 1351–4.

Martinot-Peignoux M. , Marcellin P. , Pouteau M. . Pretreatment serum hepatitis C virus RNA levels and hepatitis C virus genotype are the main and independent prognostic factors of sustained response to interferon alfa therapy in chronic hepatitis C. Hepatology 1995; 22: 1050–60.

Yuki N. , Hayashi N. , Kasahara A. . Pretreatment viral load and response to prolonged interferon-alfa course for chronic hepatitis C. J Hepatol 1995; 22: 457–63.

Hagiwara H. , Hayashi N. , Mita E. . Quantitative analysis of hepatitis C virus RNA in serum during interferon alfa therapy. Gastroenterology 1993; 104: 877–83.

Toyoda H. , Nakano S. , Kumada T. . Comparison of serum hepatitis C virus RNA concentration by branched DNA probe assay with competitive reverse transcription polymerase chain reaction as a predictor of response to interferon-alfa therapy in chronic hepatitis C patients. J Med Virol 1996; 48: 354–9.

Shiratori Y. , Kato N. , Yokosuka O. . Predictors of the efficacy of interferon therapy in chronic hepatitis C virus infection. Gastroenterology 1997; 113: 558–66.

Nousbaum J.B. , Pol 5 , Nalpas B. , Landais P. , Berthelot P. , Brechot C. , and the Collaborative Study Group. Hepatitis C virus type lb (II) infection in France and Italy. Ann Intern Med 1995; 122: 161–8.

Pawlotsky J.M. , Pellerin M. , Bouvier M. . Genetic complexity of the hypervariable region 1 (HVR1) of hepatitis C virus (HCV): Influence on the characteristics of the infection and responses to interferon alfa therapy in patients with chronic hepatitis C. J Med Virol 1998; 54: 256–64.

McHutchison J.G. , Poynard T. , Pianko S. . The impact of interferon plus ribavirin on response to therapy in black patients with chronic hepatitis C. Gastroenterology 2000; 119: 1317–23.

Toyoda H. , Kumada T. , Nakano S. . Quasispecies nature of hepatitis C virus and response to alpha interferon: significance as a predictor of direct response to interferon. J Hepatol 1997; 26: 6–13.

Hoofnagle J.H. . Therapy of viral hepatitis (Editorial). Digestion 1998; 59: 563–78.

Piperno A. , Sampietro M. , D'Alba R. . Iron stones, response to alpha interferon therapy and effects of iron depletion in chronic hepatitis C. Liver 1996; 16: 248–54.

Hirsch M.S. , Tolkoff-Rubin N.E. , Kelly A.P. , Rubin R.H. . Pharmacokinetics of human and recombinant leukocyte interferon in patients with chronic renal failure who are undergoing hemodialysis. J Infect Dis 1983; 148: 335.

Rostaing L. , Chatelut E. , Payen J.L. . Pharmacokinetics of alfa IFN-2b in chronic hepatitis C virus undergoing chronic hemodialysis or with normal renal function: clinical implications. J Am Soc Nephrol 1998; 9: 2344–8.

Uchihara M. , Izumi N. , Sakai Y. . Interferon therapy for chronic hepatitis C in hemodialysis patients: increased serum levels of interferon. Nephron 1998; 80: 51–6.

Bino T. , Madar Z. , Gertler A. , Rosenberg H. . The kidney is the major site of interferon degradation. J Interferon Res 1982; 2: 301–8.

Graziani G. , Badalamenti S. , Sampietro M. . Produzione endogena di interferone durante emodialisi in pazienti HCV positivi (Abstract). Gion It Nefrol 1998; 15(suppl. 10): 191.

Ozylkan E. , Simsek H. , Uzunalimoglu B. , Telatar H. . Interferon treatment of chronic active hepatitis C in patients with end-stage chronic renal failure. Nephron 1995; 71: 156–9.

Farrell G.C. . Therapy of hepatitis C: interferon alfa-n1 trials. Hepatology 1997; 26(suppl. 1): 96–100.

Carithers R.L. , Emerson S.S. . Therapy of hepatitis C: meta-analysis of interferon alfa-2b trials. Hepatology 1997; 26(suppl. 1): 83–8.

McHutchison J.G. , Gordon S.C. , Schiff E. . Interferon alfa 2-b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N Engl J Med 1998; 339: 1485–92.

Poynard T. , Marcellin P. , Lee SS . Randomised trial of interferon alfa2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alfa2b plus placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. Lancet 1998; 352: 1426–32.

Davis G.L. , Esteban-Mur R. , Rustgi V. . Interferon alfa-2b alone or in combination with ribavirin for the treatment of relapse of chronic hepatitis C. N Engl J Med 1998; 339: 1493–9.

Patterson J.L. , Fernandez-Larsson R. . Molecular mechanisms of action of ribavirin. Rev Infect Dis 1990; 12: 1139–46.

Wills R.J. . Clinical pharmacokinetics of interferons. Olin Pharmacokinet 1990; 19: 390–9.

Abuchowski A. , McCoy J.R. , Palczuk N.C. , Van Es T. , Davis F.F. . Effect of covalent attachment of polyethylene glycol on immunogenicity and circulating life of bovine liver catalase. J Biol Chem 1977; 252: 3582–6.

Katre N.V. . Immunogenicity of recombinant 11–2 modified by covalent attachment of polyethylene glycol. J Immunol 1990; 144: 209–13.

He X.H. , Shaw P.C. , Tam S.C. . Reducing the immunogenicity and improving the in vivo activity of tricosanthin by site-directed pegylation. Life Sci 1999; 65: 355–68.

Wang Q.C. , Pai L.H. , Debinski W. , Fitzgerald J. , Pastan I. . Polyethylene glycol-modified chimeric toxin composed of transforming growth factor alfa and Pseudomonas exotoxin. Cancer Res 1993; 53: 4588–94.

Berardi M.R. , Walters K.M. , Monge A. , Batra V. . Toxicokinetics of PEG1 2000-interferon (IFN) alfa-2b given by subcutaneous (SC) injection to cynomolgus monkeys for one month (Abstract). Fundam Appl Toxicol 1996; 30: 36.

Talpaz M. , Cortes J. , O'Brien S. . Phase I study of polyethylene glycol (PEG) interferon alpha-2b (Intron A) in CML patients (Abstract). Blood 1998; 92: 251.

Zeuzem S. , Feinman S.V. , Rasenack J. . Peginterferon alfa-2a in patients with chronic hepatitis C. N Engl J Med 2000; 343: 1666–72.

Heathcote E.J. , Shiffman M.L. , Cooksley G.E. . Peginterferon alfa-2a in patients with chronic hepatitis C and cirrhosis. N Engl J Med 2000; 343: 1673–80.

Glue P. , Rouzier-Panis R. , Raffanel C. . A dose-ranging study of pegylated interferon alfa-2b and ribavirin in chronic hepatitis C. N Engl J Med 2000; 32: 647–53.

Nicholson K.G. , Wiselka M.J. . Amantadine for influenza A. Br Med J 1991; 302: 425–6.

Schalm S.W. , Brouwer J.T. , Bekkering F.C. , van Rossum T.G. . New treatment strategies in non-responder patients with chronic hepatitis C. J Hepatol 1999; 31(suppl. 1): 184–8.

Barbaro G. , Di Lorenzo G. , Soldini M. . Interferon alfa-2b and ribavirin in combination for chronic hepatitis C patients not responding to interferon alone: an Italian, multicenter, randomized, controlled, clinical study. Am J Gastroenterol 1998; 93: 2445–51.

Gish R.G. . Standards of treatment in chronic hepatitis C. Semin Liver Dis 1999; 19: 35–47.

Brillanti S. , Levantesi F. , Masi L. , Foli M. , Bolondi L. . Triple antiviral therapy as a new option for patients with interferon nonresponsive chronic hepatitis C. Hepatology 2000; 32: 630–4.