Retransplantation of the liver for recurrent hepatitis B virus infection: The Paul Brousse experience
Bruno Roche
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorCorresponding Author
Professeur Didier Samuel MD
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Centre Hépato-Biliaire, Hôpital Paul Brousse 94800 Villejuif, FranceSearch for more papers by this authorCyrille Feray
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorPietro Majno
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorMichele Gigou
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorMichel Reynes
Service d'Anatomopathologie, Hôpital Paul Brousse, Villejuif; Université Paris Sud, CRI 9804, UPRES Virus hepatotropes et cancer, France
Search for more papers by this authorHenri Bismuth
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorBruno Roche
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorCorresponding Author
Professeur Didier Samuel MD
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Centre Hépato-Biliaire, Hôpital Paul Brousse 94800 Villejuif, FranceSearch for more papers by this authorCyrille Feray
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorPietro Majno
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorMichele Gigou
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorMichel Reynes
Service d'Anatomopathologie, Hôpital Paul Brousse, Villejuif; Université Paris Sud, CRI 9804, UPRES Virus hepatotropes et cancer, France
Search for more papers by this authorHenri Bismuth
Centre Hépato-Biliaire UPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, FranceUPRES Virus hepatotropes et cancer, France
Search for more papers by this authorAbstract
Recurrent hepatitis B virus (HBV) infection of the liver graft is characterized by a severe outcome and high level of HBV replication. For many investigators, retransplantation appears contraindicated because of constant recurrence and a high mortality. We report our experience in this setting. Between January 1985 and December 1995, 10 patients who underwent retransplantation for HBV graft reinfection were studied. According to the antiviral treatment administered after HBV recurrence on the first liver graft and the protocol of antiviral prophylaxis after retransplantation, two groups were defined: group 1 underwent retransplantation before January 1992 (n = 5), and group 2 underwent retransplantation after January 1992 (n = 5). At the time of reinfection, serum HBV DNA was positive in all patients, hepatitis Be antigen (HBeAg) was positive in 6 patients. Antiviral therapy was administered to 7 patients (group 1, adenine arabinoside mono phosphate [ara-Amp; n = 3]; group 2, ara-Amp [n = 5], ganciclovir [n = 4]). After retransplantation, long-term antibody to HB surface antigen (anti-HBs) immunoglobulins were administered to achieve an anti-HBs titer greater than 100 IU/L in group 1 and to achieve an anti-HBs titer greater than 500 IU/L associated with prophylactic intravenous ganciclovir administration (5 mg/kg three times weekly) for 2 years in group 2. In group 1, all patients died, either perioperatively or secondary to HBV recurrence (1 year survival, 0%). In group 2, 1 patient died 50 months after retransplantation of HBV cirrhosis on the second graft, and 4 patients remained HBsAg negative at a mean of 41 months (range, 24 to 68 months) after retransplantation. The prognosis of retransplantation for HBV recurrence was dramatically improved by the administration of antiviral therapy before retransplantation and the maintenance of a high anti-HBs level combined with antiviral therapy after retransplantation.
References
- 1 Samuel D, Muller R, Alexander G, Fassati L, Ducot B, Benhamou JP, et al. Liver transplantation in European patients with the hepatitis B surface antigen. N Engl J Med 1993; 329: 1842–1847. MEDLINE
- 2 Todo S, Demetris AJ, Van Thiel D, Teperman L, Fung JJ, Starzl TE. Orthotopic liver transplantation for patients with hepatitis B virus–related liver disease. Hepatology 1991; 13: 619–626. MEDLINE
- 3 O'Grady JG, Smith HM, Davies S, Daniels HM, Donaldson PT, Tan KC, et al. Hepatitis B virus re-infection after liver transplantation: Serological and clinical implications. J Hepatol 1992; 14: 104–111. MEDLINE
- 4 König V, Hopf U, Neuhaus P, Bauditz J, Schmidt CA, Blumhardt G, et al. Long-term follow-up of hepatitis B virus–infected recipients after orthotopic liver transplantation. Transplantation 1994; 58: 553–559. MEDLINE
- 5 Davies S, Portmann B, O'Grady J, Aldis P, Chaggar K, Alexander G, et al. Hepatic histological findings after transplantation for chronic hepatitis B virus infection, including a unique pattern of fibrosing cholestatic hepatitis. Hepatology 1991; 13: 150–157. MEDLINE
- 6 Lau JYN, Bain VG, Davies SE, O'Grady JG, Alberti A, Alexander GJM, et al. High-level expression of hepatitis B viral antigens in fibrosing cholestatic hepatitis. Gastroenterology 1992; 102: 956–962. MEDLINE
- 7 Tur-Kaspa R, Laub O. Corticosteroids stimulate hepatitis B virus DNA, mRNA and protein production in a stable expression system. J Hepatol 1990; 11: 34–36. MEDLINE
- 8 Crippin J, Foster B, Carlen S, Borcich A, Bodenheimer H. Retransplantation in hepatitis B—A multicenter experience. Transplantation 1994; 57: 823–826. MEDLINE
- 9 Terrault NA, Zhou S, Combs C, Hahn JA, Lake JR, Roberts JP, et al. Prophylaxis in liver transplant recipients using a fixed dosing schedule of hepatitis B immunoglobulin. Hepatology 1996; 24: 1327–1333. MEDLINE
- 10 Lake JR. Should liver transplantation be performed for patients with chronic hepatitis B? Yes! Liver Transpl Surg 1995; 1: 260–265. MEDLINE
- 11 Kiyasu PK, Ishitani MB, McGory RW, Gaffey MJ, Dickson RC, Caldwell SH, et al. Prevention of hepatitis B “rerecurrence” after a second liver transplant—The role of maintenance polyclonal HBIg therapy. Transplantation 1994; 58: 954–956. MEDLINE
- 12 Ishitani M, McGory R, Dickson R, Caldwell S, Bickston S, McCullough C, et al. Retransplantation of patients with severe posttransplant hepatitis B in the first allograft. Transplantation 1997; 64: 410–414. MEDLINE
- 13 McGory RW, Ishitani M, Oliveira WM, Stevenson WC, McCullough CS, Dickson RC, et al. Improved outcome of orthotopic liver transplantation for chronic hepatitis B cirrhosis with aggressive passive immunization. Transplantation 1996; 61: 1358–1364. MEDLINE
- 14 Gish RG, Lau JYN, Brooks L, Fang JWS, Steady SL, Imperial JC, et al. Ganciclovir treatment of hepatitis B virus infection in liver transplant recipients. Hepatology 1996; 23: 1–7. MEDLINE
- 15 Krüger M, Tillmann HL, Trautwein C, Bode U, Oldhafer K, Maschek H, et al. Famciclovir treatment of hepatitis B virus recurrence after liver transplantation: A pilot study. Liver Transpl Surg 1996; 2: 253–262. MEDLINE
- 16 Haller GW, Bechstein WO, Platz KP, Neuhaus R, Hopf U, Neuhaus P. Treatment of recurrent hepatitis B infection after liver transplantation with famciclovir [abstr]. J Hepatol 1995; 23: 152.
- 17 Bain VG, Kneteman NM, Ma MM, Gutfreund K, Shapiro JA, Fischer K, et al. Efficacy of lamivudine in chronic hepatitis B patients with active viral replication and decompensated cirrhosis undergoing liver transplantation. Tranplantation 1996; 62: 1456–1462.
- 18 Grellier L, Mutimer D, Ahmed M, Brown D, Burroughs AK, Rolles K, et al. Lamivudine prophylaxis against re-infection in liver transplantation for hepatitis B cirrhosis. Lancet 1996; 348: 1212–1215. MEDLINE
- 19 Gugenheim J, Samuel D, Saliba F, Castaing D, Bismuth H. Use of flexible triple-drug immunosuppressive therapy in liver transplantation. Transplant Proc 1987; 19: 3805–3807. MEDLINE
- 20 Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. the METAVIR Cooperative Study Group. Hepatology 1996; 24: 289–293. MEDLINE
- 21 Samuel D, Bismuth A, Mathieu D, Arulnaden JL, Reynes M, Benhamou JP, et al. Passive immunoprophylaxis after liver transplantation in HBsAg-positive patients. Lancet 1991; 337: 813–815. MEDLINE
- 22 Gugenheim J, Crafa F, Fabiani P, Goubaux B, Ouzan D, Mouiel J. Long-term passive immunoprophylaxis of B virus recurrence after liver transplantation in Hbs antigen–positive patients. Transplant Proc 1993; 25: 1349–1350. MEDLINE
- 23 Muller R, Gubernatis G, Farle M, Niehoff G, Klein H, Wittekind C. Liver transplantation in Hbs antigen (HBsAg) carriers: Prevention of hepatitis B virus (HBV) recurrence by passive immunization. J Hepatol 1991; 13: 90–96. MEDLINE
- 24 Mora N, Klintmalm G, Poplawski S, Cofer J, Husberg B, Gonwa TA, et al. Recurrence of hepatitis B after liver transplantation: Does hepatitis B immunoglobulin modify the recurrent disease? Transplant Proc 1990; 22: 1549–1550. MEDLINE
- 25 Rimoldi P, Belli L, Rondinara G, Alberti A, DeCarlis L, Minola E. Recurrent HBV/HDV infections under different immunoprophylaxis protocols. Transplant Proc 1993; 25: 2675–2676. MEDLINE
- 26 Marcellin P, Samuel D, Loriot MA, Areias J, Bismuth H, Benhamou JP. Anti-viral effect of adenine arabinoside monophosphate (ara-Amp) in patients with recurrence of hepatitis B virus (HBV) infection after liver transplantation [abstr]. Hepatology 1990; 12: 966A.
- 27 Terrault NA, Holland CC, Ferrell L, Hahn JA, Lake JR, Roberts JP, et al. Interferon alfa for recurrent hepatitis B infection after liver transplantation. Liver Transpl Surg 1996; 2: 132–138. MEDLINE
- 28 Feray C, Samuel D, Gigou M, Paradis V, David MF, Lemonnier C, et al. An open trial of interferon alpha recombinant for hepatitis C after liver transplantation: Anti-viral effects and risk of rejection. Hepatology 1995; 22: 1084–1089. MEDLINE
- 29 Marcellin P, Samuel D, Areias J, Loriot MA, Arulnaden JL, Gigou M, et al. Pretransplantation interferon treatment and recurrence of hepatitis B virus infection after liver transplantation for hepatitis B–related end-stage liver disease. Hepatology 1994; 19: 6–12. MEDLINE
- 30 Dienstag JL, Perrillo RP, Schiff ER, Bartholomew M, Vicary C, Rubin M. A preliminary trial of lamivudine for chronic hepatitis B virus infection. N Engl J Med 1995; 333: 1657–1661. MEDLINE
- 31 Perrillo RP, Rakela J, Martin P, Levy GL, Schiff ER, Wright T, et al. Lamivudine for hepatitis B after liver transplantation. Hepatology 1996; 24: 182A.
- 32 Ling R, Mutimer D, Ahmed M, Boxall EH, Elias E, Dusheiko GM, et al. Selection of mutations in the hepatitis B virus polymerase during therapy of transplant recipients with lamivudine. Hepatology 1996; 24: 711–713. MEDLINE
- 33 Wang Y, Bowden DS, Shaw T, Civitico G, Chan Y, Qiao M, et al. Inhibition of duck hepatitis B virus replication in vivo by the nucleoside analogue ganciclovir. Antiviral Chem Chemother 1991; 2: 107–114.
- 34 Chossegros P, Pouteil-Noble C, Samuel D, Causse X, Ouzan D, Bizollon T, et al. Ganciclovir is an effective anti-viral agent for post-transplantation chronic HBV infections, maintenance therapy may be required in some cases [abstr]. Gastroenterology 1993; 104: A888.
- 35
De la Mata M,
Montero JL,
Fraga E,
Costan G,
Delgado M,
Lopez R, et al.
Efficacy of ganciclovir in the treatment of hepatitis B virus infection of the liver graft. Long-term results [abstr].
Hepatology
1995;
22: 130A.
10.1016/0270-9139(95)94245-9 Google Scholar