Semin Liver Dis 2012; 32(03): 245-255
DOI: 10.1055/s-0032-1323630
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Liver Transplantation in Delta Virus Infection

Bruno Roche
1   Assistance Publique-Hopitaux de Paris, Hopital Paul Brousse, Centre Hepato-Biliaire, Villejuif, France
2   INSERM, U785, Villejuif, France
3   Univ Paris-Sud, UMR-S785 Villejuif, France
,
Didier Samuel
1   Assistance Publique-Hopitaux de Paris, Hopital Paul Brousse, Centre Hepato-Biliaire, Villejuif, France
2   INSERM, U785, Villejuif, France
3   Univ Paris-Sud, UMR-S785 Villejuif, France
› Author Affiliations
Further Information

Publication History

Publication Date:
29 August 2012 (online)

Abstract

Liver transplantation is the only therapy for patients with end-stage liver disease, hepatocellular carcinoma, or fulminant hepatitis due to hepatitis D virus (HDV) and hepatitis B virus (HBV) coinfection or superinfection. Patients chronically coinfected with HDV are less at risk of HBV recurrence and have a better survival rate than patients infected with HBV alone. Patients coinfected with HDV generally do not require pretransplant antiviral therapy. Rates of recurrent HBV-HDV infection are lower than 5% using low-dose intramuscular (IM) HBIg and antiviral prophylaxis in combination. Few studies have evaluated the possibility of using shorter-term HBIg (12–24 months) then switching to antiviral therapy. Although HBV replication can be controlled by potent HBV-polymerase inhibitors, reappearance of HBsAg and/or the persistence of HBV DNA in serum, liver, or peripheral blood mononuclear cells might have deleterious consequences in the setting of HBV-HDV coinfection as they may provide the biologic substrate to the reactivation of HDV. No effective antiviral drug is available for the treatment of graft infection with HDV.

 
  • References

  • 1 Rizzetto M. Hepatitis D: thirty years after. J Hepatol 2009; 50 (5) 1043-1050
  • 2 Hughes SA, Wedemeyer H, Harrison PM. Hepatitis delta virus. Lancet 2011; 378 (9785) 73-85
  • 3 Samuel D, Muller R, Alexander G , et al. Liver transplantation in European patients with the hepatitis B surface antigen. N Engl J Med 1993; 329 (25) 1842-1847
  • 4 Grellier L, Mutimer D, Ahmed M , et al. Lamivudine prophylaxis against reinfection in liver transplantation for hepatitis B cirrhosis. Lancet 1996; 348 (9036) 1212-1215
  • 5 Markowitz JS, Martin P, Conrad AJ , et al. Prophylaxis against hepatitis B recurrence following liver transplantation using combination lamivudine and hepatitis B immune globulin. Hepatology 1998; 28 (2) 585-589
  • 6 Fattovich G, Bortolotti F, Donato F. Natural history of chronic hepatitis B: special emphasis on disease progression and prognostic factors. J Hepatol 2008; 48 (2) 335-352
  • 7 Fattovich G, Giustina G, Christensen E , et al. Influence of hepatitis delta virus infection on morbidity and mortality in compensated cirrhosis type B. The European Concerted Action on Viral Hepatitis (Eurohep). Gut 2000; 46 (3) 420-426
  • 8 European Liver Transplant Registry. Homepage. Available at: http://www.eltr.org . Accessed February 29, 2012.
  • 9 Ottobrelli A, Marzano A, Smedile A , et al. Patterns of hepatitis delta virus reinfection and disease in liver transplantation. Gastroenterology 1991; 101 (6) 1649-1655
  • 10 Reynès M, Zignego L, Samuel D , et al. Graft hepatitis delta virus reinfection after orthotopic liver transplantation in HDV cirrhosis. Transplant Proc 1989; 21 (1 Pt 2) 2424-2425
  • 11 Rizzetto M, Macagno S, Chiaberge E , et al. Liver transplantation in hepatitis delta virus disease. Lancet 1987; 2 (8557) 469-471
  • 12 Samuel D, Zignego AL, Reynes M , et al. Long-term clinical and virological outcome after liver transplantation for cirrhosis caused by chronic delta hepatitis. Hepatology 1995; 21 (2) 333-339
  • 13 Steinmüller T, Seehofer D, Rayes N , et al. Increasing applicability of liver transplantation for patients with hepatitis B-related liver disease. Hepatology 2002; 35 (6) 1528-1535
  • 14 Kim WR, Poterucha JJ, Kremers WK, Ishitani MB, Dickson ER. Outcome of liver transplantation for hepatitis B in the United States. Liver Transpl 2004; 10 (8) 968-974
  • 15 David E, Rahier J, Pucci A , et al. Recurrence of hepatitis D (delta) in liver transplants: histopathological aspects. Gastroenterology 1993; 104 (4) 1122-1128
  • 16 Smedile A, Casey JL, Cote PJ , et al. Hepatitis D viremia following orthotopic liver transplantation involves a typical HDV virion with a hepatitis B surface antigen envelope. Hepatology 1998; 27 (6) 1723-1729
  • 17 Mederacke I, Filmann N, Yurdaydin C , et al. Rapid early HDV RNA decline in the peripheral blood but prolonged intrahepatic hepatitis delta antigen persistence after liver transplantation. J Hepatol 2012; 56 (1) 115-122
  • 18 Faria LC, Gigou M, Roque-Afonso AM , et al. Hepatocellular carcinoma is associated with an increased risk of hepatitis B virus recurrence after liver transplantation. Gastroenterology 2008; 134 (7) 1890-1899 , quiz 2155
  • 19 Gane EJ, Angus PW, Strasser S , et al; Australasian Liver Transplant Study Group. Lamivudine plus low-dose hepatitis B immunoglobulin to prevent recurrent hepatitis B following liver transplantation. Gastroenterology 2007; 132 (3) 931-937
  • 20 Degertekin B, Han SH, Keeffe EB , et al; NIH HBV-OLT Study Group. Impact of virologic breakthrough and HBIG regimen on hepatitis B recurrence after liver transplantation. Am J Transplant 2010; 10 (8) 1823-1833
  • 21 Jiang L, Yan L, Li B , et al. Prophylaxis against hepatitis B recurrence posttransplantation using lamivudine and individualized low-dose hepatitis B immunoglobulin. Am J Transplant 2010; 10 (8) 1861-1869
  • 22 Zheng S, Chen Y, Liang T , et al. Prevention of hepatitis B recurrence after liver transplantation using lamivudine or lamivudine combined with hepatitis B immunoglobulin prophylaxis. Liver Transpl 2006; 12 (2) 253-258
  • 23 Chun J, Kim W, Kim BG , et al. High viremia, prolonged lamivudine therapy and recurrent hepatocellular carcinoma predict posttransplant hepatitis B recurrence. Am J Transplant 2010; 10 (7) 1649-1659
  • 24 Coffin CS, Stock PG, Dove LM , et al. Virologic and clinical outcomes of hepatitis B virus infection in HIV-HBV coinfected transplant recipients. Am J Transplant 2010; 10 (5) 1268-1275
  • 25 Marzano A, Gaia S, Ghisetti V , et al. Viral load at the time of liver transplantation and risk of hepatitis B virus recurrence. Liver Transpl 2005; 11 (4) 402-409
  • 26 Caccamo L, Agnelli F, Reggiani P , et al. Role of lamivudine in the posttransplant prophylaxis of chronic hepatitis B virus and hepatitis delta virus coinfection. Transplantation 2007; 83 (10) 1341-1344
  • 27 Marzano A, Salizzoni M, Debernardi-Venon W , et al. Prevention of hepatitis B virus recurrence after liver transplantation in cirrhotic patients treated with lamivudine and passive immunoprophylaxis. J Hepatol 2001; 34 (6) 903-910
  • 28 Perrillo RP, Wright T, Rakela J , et al; Lamivudine North American Transplant Group. A multicenter United States-Canadian trial to assess lamivudine monotherapy before and after liver transplantation for chronic hepatitis B. Hepatology 2001; 33 (2) 424-432
  • 29 Lo CM, Cheung ST, Lai CL , et al. Liver transplantation in Asian patients with chronic hepatitis B using lamivudine prophylaxis. Ann Surg 2001; 233 (2) 276-281
  • 30 Malkan G, Cattral MS, Humar A , et al. Lamivudine for hepatitis B in liver transplantation: a single-center experience. Transplantation 2000; 69 (7) 1403-1407
  • 31 Mutimer D, Dusheiko G, Barrett C , et al. Lamivudine without HBIg for prevention of graft reinfection by hepatitis B: long-term follow-up. Transplantation 2000; 70 (5) 809-815
  • 32 Yoshida H, Kato T, Levi DM , et al. Lamivudine monoprophylaxis for liver transplant recipients with non-replicating hepatitis B virus infection. Clin Transplant 2007; 21 (2) 166-171
  • 33 Schiff E, Lai CL, Hadziyannis S , et al; Adefovir Dipivoxil Study 45 International Investigators Group. Adefovir dipivoxil for wait-listed and post-liver transplantation patients with lamivudine-resistant hepatitis B: final long-term results. Liver Transpl 2007; 13 (3) 349-360
  • 34 Fung J, Cheung C, Chan SC , et al. Entecavir monotherapy is effective in suppressing hepatitis B virus after liver transplantation. Gastroenterology 2011; 141 (4) 1212-1219
  • 35 Dickson RC, Terrault NA, Ishitani M , et al. Protective antibody levels and dose requirements for IV 5% Nabi hepatitis B immune globulin combined with lamivudine in liver transplantation for hepatitis B-induced end stage liver disease. Liver Transpl 2006; 12 (1) 124-133
  • 36 Buti M, Mas A, Prieto M , et al. A randomized study comparing lamivudine monotherapy after a short course of hepatitis B immune globulin (HBIg) and lamivudine with long-term lamivudine plus HBIg in the prevention of hepatitis B virus recurrence after liver transplantation. J Hepatol 2003; 38 (6) 811-817
  • 37 Wong SN, Chu CJ, Wai CT , et al. Low risk of hepatitis B virus recurrence after withdrawal of long-term hepatitis B immunoglobulin in patients receiving maintenance nucleos(t)ide analogue therapy. Liver Transpl 2007; 13 (3) 374-381
  • 38 Han SH, Ofman J, Holt C , et al. An efficacy and cost-effectiveness analysis of combination hepatitis B immune globulin and lamivudine to prevent recurrent hepatitis B after orthotopic liver transplantation compared with hepatitis B immune globulin monotherapy. Liver Transpl 2000; 6 (6) 741-748
  • 39 Rosenau J, Bahr MJ, Tillmann HL, Trautwein C, Klempnauer J, Manns MP ; Böker KHW. Lamivudine and low-dose hepatitis B immune globulin for prophylaxis of hepatitis B reinfection after liver transplantation possible role of mutations in the YMDD motif prior to transplantation as a risk factor for reinfection. J Hepatol 2001; 34 (6) 895-902
  • 40 Neff GW, O'brien CB, Nery J , et al. Outcomes in liver transplant recipients with hepatitis B virus: resistance and recurrence patterns from a large transplant center over the last decade. Liver Transpl 2004; 10 (11) 1372-1378
  • 41 Anselmo DM, Ghobrial RM, Jung LC , et al. New era of liver transplantation for hepatitis B: a 17-year single-center experience. Ann Surg 2002; 235 (5) 611-619 , discussion 619–620
  • 42 Xi ZF, Xia Q, Zhang JJ , et al. The role of entecavir in preventing hepatitis B recurrence after liver transplantation. J Dig Dis 2009; 10 (4) 321-327
  • 43 Yi NJ, Suh KS, Cho JY , et al. Recurrence of hepatitis B is associated with cumulative corticosteroid dose and chemotherapy against hepatocellular carcinoma recurrence after liver transplantation. Liver Transpl 2007; 13 (3) 451-458
  • 44 Hooman N, Rifai K, Hadem J , et al. Antibody to hepatitis B surface antigen trough levels and half-lives do not differ after intravenous and intramuscular hepatitis B immunoglobulin administration after liver transplantation. Liver Transpl 2008; 14 (4) 435-442
  • 45 Yahyazadeh A, Beckebaum S, Cicinnati V , et al. Efficacy and safety of subcutaneous human HBV-immunoglobulin (Zutectra) in liver transplantation: an open, prospective, single-arm phase III study. Transpl Int 2011; 24 (5) 441-450
  • 46 Cholongitas E, Goulis J, Akriviadis E, Papatheodoridis GV. Hepatitis B immunoglobulin and/or nucleos(t)ide analogues for prophylaxis against hepatitis b virus recurrence after liver transplantation: a systematic review. Liver Transpl 2011; 17 (10) 1176-1190
  • 47 Rao W, Wu X, Xiu D. Lamivudine or lamivudine combined with hepatitis B immunoglobulin in prophylaxis of hepatitis B recurrence after liver transplantation: a meta-analysis. Transpl Int 2009; 22 (4) 387-394
  • 48 Katz LH, Paul M, Guy DG, Tur-Kaspa R. Prevention of recurrent hepatitis B virus infection after liver transplantation: hepatitis B immunoglobulin, antiviral drugs, or both? Systematic review and meta-analysis. Transpl Infect Dis 2010; 12 (4) 292-308
  • 49 Loomba R, Rowley AK, Wesley R , et al. Hepatitis B immunoglobulin and lamivudine improve hepatitis B-related outcomes after liver transplantation: meta-analysis. Clin Gastroenterol Hepatol 2008; 6 (6) 696-700
  • 50 Sánchez-Fueyo A, Rimola A, Grande L , et al. Hepatitis B immunoglobulin discontinuation followed by hepatitis B virus vaccination: a new strategy in the prophylaxis of hepatitis B virus recurrence after liver transplantation. Hepatology 2000; 31 (2) 496-501
  • 51 Angelico M, Di Paolo D, Trinito MO , et al. Failure of a reinforced triple course of hepatitis B vaccination in patients transplanted for HBV-related cirrhosis. Hepatology 2002; 35 (1) 176-181
  • 52 Bienzle U, Günther M, Neuhaus R , et al. Immunization with an adjuvant hepatitis B vaccine after liver transplantation for hepatitis B-related disease. Hepatology 2003; 38 (4) 811-819
  • 53 Albeniz Arbizu E, Barcena Marugan R, Oton Nieto E , et al. Prophylaxis of recurrent hepatitis B virus by vaccination after liver transplant: preliminary results. Transplant Proc 2003; 35 (5) 1848-1849
  • 54 Lo CM, Liu CL, Chan SC, Lau GK, Fan ST. Failure of hepatitis B vaccination in patients receiving lamivudine prophylaxis after liver transplantation for chronic hepatitis B. J Hepatol 2005; 43 (2) 283-287
  • 55 Rosenau J, Hooman N, Hadem J , et al. Failure of hepatitis B vaccination with conventional HBsAg vaccine in patients with continuous HBIG prophylaxis after liver transplantation. Liver Transpl 2007; 13 (3) 367-373
  • 56 Dodson SF, de Vera ME, Bonham CA, Geller DA, Rakela J, Fung JJ. Lamivudine after hepatitis B immune globulin is effective in preventing hepatitis B recurrence after liver transplantation. Liver Transpl 2000; 6 (4) 434-439
  • 57 Naoumov NV, Lopes AR, Burra P , et al. Randomized trial of lamivudine versus hepatitis B immunoglobulin for long-term prophylaxis of hepatitis B recurrence after liver transplantation. J Hepatol 2001; 34 (6) 888-894
  • 58 Angus PW, Patterson SJ, Strasser SI, McCaughan GW, Gane E. A randomized study of adefovir dipivoxil in place of HBIG in combination with lamivudine as post-liver transplantation hepatitis B prophylaxis. Hepatology 2008; 48 (5) 1460-1466
  • 59 Saab S, Desai S, Tsaoi D , et al. Posttransplantation hepatitis B prophylaxis with combination oral nucleoside and nucleotide analog therapy. Am J Transplant 2011; 11 (3) 511-517
  • 60 Lenci I, Tisone G, Di Paolo D , et al. Safety of complete and sustained prophylaxis withdrawal in patients liver-transplanted for HBV-related cirrhosis at low risk of HBV recurrence. J Hepatol 2011; 55 (3) 587-593
  • 61 Roche B, Feray C, Gigou M , et al. HBV DNA persistence 10 years after liver transplantation despite successful anti-HBS passive immunoprophylaxis. Hepatology 2003; 38 (1) 86-95
  • 62 Hussain M, Soldevila-Pico C, Emre S, Luketic V, Lok AS ; NIH HBV-OLT Study Group. Presence of intrahepatic (total and ccc) HBV DNA is not predictive of HBV recurrence after liver transplantation. Liver Transpl 2007; 13 (8) 1137-1144