Transplanting Solid Organs from HBsAg Negative Donors Positive for Antibody to Hepatitis B Core Antigen: The Implications

Rosenthal J.T. Expanded criteria for cadaver organ donation in renal transplantation. Urol Clin North Am 1994; 21: 283–7.

Terasaki P.I. , Cho Y.W. , Cecka J.M. Strategy for eliminating the kidney shortage. Clin Transplant 1997; 265–7.

Cho Y.W. Expanded criteria donors. Clin Transplant 1998; 421–36.

Cho Y.W. , Terasaki P.I. , Cecka J.M. , Gjertson D.W. Transplantation of kidneys from donors whose hearts have stopped beating. N Engl J Med 1998; 338: 221–5.

Gonzalez-Peralta R.P. , Andres J.M. , Tung F.Y. , Fang J.W. , Brunson M.E. , Davis G.L. , Lau Y.N. Transplantation of a hepatitis B surface-antigen positive donor liver into a hepatitis B virus negative recipient. Transplantation 1994; 58: 114–6.

Hoft R.H. , Pflugfelder S.C. , Forster R.K. , Ullman S. , Polack F.M. , Schiff E.R. Clinical evidence for hepatitis B transmission resulting from corneal transplantation. Cornea 1997; 16: 132–7.

Chan M.K. , Chang W.K. Renal transplantation from HBsAg positive donors to HBsAg negative recipients (letter). Br Med J 1988; 297: 522–3.

Landreneau M.D. , DeVault G.A. , Rohr M.S. , Kilpatrick J.S. , King J.W. , Rhynes V.K. , Gonzalez E. , McDonald J.C. Transmission of hepatitis B by renal transplantation despite active immunization with hepatitis B vaccine. Clin Transplant 1988; 2: 265–9.

Wolf J.L. , Perkins H.A. , Schreeder M.T. , Vincenti F. The transplanted kidney as a source of hepatitis B infection. Ann Intern Med 1979; 91: 412–4.

Lutwick L.I. , Sywassink J.M. , Corry R.J. , Shorey J.W. The transmission of hepatitis B by renal transplantation. Clin Nephrol 1983; 19: 317–9.

Mathurin P. , Mouquet C. , Poynard T. , Sylla C. , Benalia H. , Fretz C. , Thibault V. , Cadranel J.F. , Bernard B. , Opolon P. , Coriat P. , Bitker M.O. Impact of hepatitis B and C virus on kidney transplantation outcome. Hepatology 1999; 29: 257–3.

Hiesse C. , Buffet C. , Neyrat N. , Ricu P. , Charpentier B. , Etienne J.P. , Fries D. Impact of HBs antigenemia on long-term patient survival and causes of death after renal transplantation. Clin Transplant 1992; 46: 461–7.

Pfaff W.W. , Blanton J.W. Hepatitis antigenemia and survival after renal transplantation. Clin Transplant 1997; 11: 476–9.

Breitenfeldt M.K. , Rasenack J. , Berthold H. , Olschewski M. , Schroff J. , Strey C. , Grotz W.H. Impact of hepatitis B and C on graft loss and mortality of patients after kidney transplantation. Clin Transplant 2002; 16: 130–6.

Lee W.C. , Shu K.H. , Cheng C.H. , Wu M.J. , Chen C.H. , Lian J.D. Long-term impact of hepatitis B, C virus infection on renal transplantation. Am J Nephrol 2001; 21: 300–6.

Kairaritis L.K. , Gottlieb T. , George C.R. Fatal hepatitis B virus infection with fibrosing cholestatic hepatitis following renal transplantation. Nephrol Dial Transplant 1998; 13: 1571–3.

Hanson C.A. , Sutherland D.E. , Snover D.C. Fulminant hepatic failure in an HBsAg carrier renal transplant patient following cessation of immunosuppressive therapy. Transplantation 1985; 39: 311–2.

Fabrizi F. , Martin P. Hepatitis in kidney transplantation. In: Danovitch G. , ed. Handbook of kidney transplantation. Philadelphia: Lippincott Williams & Wilkins, 2001; pp. 263–71.

Kasiske B. , Cangro C.B. , Hariharan S. , Hricik D.E. , Kerman R.H. , Roth D. , Rush D.N. , Vazquez M.A. , Weir M.R. The evaluation of renal transplant candidates: clinical practice guidelines. Am J Transplant 2001; 2(suppl 1): S5–95.

Lee W.M. Hepatitis B virus infection. N Engl J Med 1997; 337: 1733–45.

Chung R.T. , Feng S. , Delmonico F.L. Approach to the management of allograft recipients following the detection of hepatitis B virus in the prospective organ donor. Am J Transplant 2001; 1: 185–91.

Levy P. , Marcellin P. , Martinot-Peignoux M. , Degott C. , Nataf J. , Benhamou J.P. Clinical course of spontaneous reactivation of hepatitis B virus infection in patients with chronic hepatitis B. Hepatology 1990; 12: 570–4.

Hoofnagle J.H. , Dusheiko G.M. , Schafer D.F. , Jones E.A. , Micetich K.C. , Young R.C. , Costa J. Reactivation of chronic hepatitis B virus infection by cancer chemotherapy. Ann Intern Med 1982; 96: 447–9.

Lok A.S.F. , Liang R.H.S. , Chiu E.K.W. , Wong K.L. , Chan T.K. , Todd D. Reactivation of hepatitis B virus replication in patients receiving cytotoxic therapy. Report of a prospective study. Gastroenterology 1991; 100: 182–8.

Brechot C. , Degos F. , Lugassy C. , Thiers V. , Zafrani S. , Franco D. , Bismuth H. , Trepo C. , Benhamou J.P. , Wands J. Hepatitis B virus DNA in patients with chronic liver disease and negative tests for hepatitis B surface antigen. N Engl J Med 1985; 312: 270–6.

Kuhns M. , McNamara A. , Mason A. , Campbell C. , Perrillo R. Serum and liver hepatitis B virus DNA in chronic hepatitis B after sustained loss of surface antigen. Gastroenterology 1992; 103: 1649–56.

Fong T.L. , Di Bisceglie A.M. , Gerber M.A. , Waggoner J.G. , Hoofnagle J.H. Persistence of hepatitis B virus DNA in the liver after loss of HBsAg in chronic hepatitis B. Hepatology 1993; 18: 1313–8.

Michalak T.I. , Pasquinelli C. , Guilhot S. , Chisari F.V. Hepatitis B virus persistence after recovery from acute viral hepatitis. J Clin Invest 1994; 93: 230–9.

Rehermann B. , Lau D. , Hoofnagle J.H. , Chisari F.V. The hepatitis B virus persists for decades after patients' recovery from acute viral hepatitis despite active maintenance of a cytotoxic T-lymphocyte response. Nat Med 1996; 2: 1104–8.

Penna A. , Artini M. , Cavalli A. , Levrero M. , Bertoletti A. , Pilli M. , Chisari F.V. , Rehermann B. , Fiaccadori F. , Ferrari C. Long-lasting memory T cell responses following self-limited acute hepatitis B. J Clin Invest 1996; 98: 1185–94.

Cabrerizo M. , Bartolomè J. , De Sequera P. , Caramelo C. , Carreno V. Hepatitis B virus DNA in serum and blood cells of hepatitis B surface antigen-negative hemodialysis and staff. J Am Soc Nephrol 1997; 8: 1443–7.

Conjeevaram H.S. , Lok A.S.F. Occult hepatitis B virus infection: a hidden menace? Hepatology 2001; 34: 204–6.

Noborg U. , Gusdal A. , Horal P. , Lindh M. Levels of viraemia in subjects with serological markers of past or chronic hepatitis B virus infection. Scand J Infect Dis 2000; 32: 249–52.

Brechot C. , Thiers V. , Kremsdorf D. , Nalpas B. , Pol S. , Paterlini-Brechot P. Persistent hepatitis B virus infection in subjects without hepatitis B surface antigen: Clinically significant or purely “occult”? Hepatology 2001; 3: 194–203.

Cacciola I. , Pollicino T. , Squadrito G. , Cerenzia G. , Orlando M.E. , Raimondo G. Occult hepatitis B virus infection in patients with chronic hepatitis C liver disease. N Engl J Med 1999; 341: 22–6.

Hoofnagle J.H. , Seeff L.B. , Bales Z.B. , Zimmermann H.J. Type B hepatitis after transfusion with blood containing antibody to hepatitis B core antigen. N Engl J Med 1978; 298: 1379–83.

Thiers V. , Kremsdorf D. , Schellekens H. , Goudeau A. , Sinski J. , Nakaijma E. , Mack D. , Driss F. , Wands J. , Tiollais P. , Brechot C. Transmission of hepatitis B from hepatitis B seronegative subjects. Lancet 1988; i: 1273–6.

Alter M.J. , Mast E.E. The epidemiology of viral hepatitis in the United States. Gastroenterol Clin North Am 1994; 23: 437–55.

Anderson N.A.B. , Raafat A. , Shwe K.E. , Barbara J. , Contreras M. , Fraser I.D. , Gunson H.H. , Martlew V. , Mijovic V. , Goldie D.J. UK multicentre study on blood donors for surrogate markers of non-A non-B hepatitis. Part 1: Alanine transferase and anti-HBc testing. Transfus Med 1992; 2: 301–5.

Dusheiko G. , Song E. , Bowyer S. , Whitcutt M. , Maier G. , Meyers A. , Kew M.C. Natural history of hepatitis B virus infection in renal transplant recipients- a fifteen-year follow-up. Hepatology 1983; 3: 330–6.

Nagington J. , Cossart Y.E. , Cohen B.J. Reactivation of hepatitis B after transplantation operations. Lancet 1977; i: 558–60.

Waters J. , Pignatelli M. , Galpin S. , Ishikara K. , Thomas H.C. Virus-neutralizing antibodies to hepatitis B virus: the nature of an immunogenic epitope on the S gene peptide. J Gen Virol 1986; 67: 2467–73.

Treichel U. , Meyer zum Buschenfelde K.H. , Stockert R.J. , Poralla T. , Gerken G. The asialoglycoprotein receptor mediates hepatic binding and uptake of natural hepatitis B virus particles derived from viraemic carriers. J Gen Virol 1994; 75: 3021–9.

Grotz W. , Rasenack J. , Benzing T. , Berthold H. , Peters T. , Walter E. , Schollmeyer P. , Rump L.C. Occurrence and management of hepatitis B virus reactivation following kidney transplantation. Clin Nephrol 1998; 49: 385–8.

Marcellin P. , Giostra E. , Martinot-Peignoux M. , Loriot M.A. , Jaegle M.L. , Wolf P. , Degott C. , Degos F. , Benhamou J.P. Redevelopment of hepatitis B surface antigen after renal transplantation. Gastroenterology 1991; 100: 1432–4.

Blanpain C. , Knoop C. , Delforge M.L. , Antoine M. , Peny M.O. , Liesnard C. , Vereerstreaeten P. , Cogan E. , Adler M. , Abramowicz D. Reactivation of hepatitis B after transplantation in patients with pre-existing anti-hepatitis B surface antigen antibodies. Transplantation 1998; 66: 883–6.

Kidd-Liungren K. , Simonsen O. Reappearance of hepatitis B 10 years after kidney transplantation (letter). N Engl J Med 1999; 341: 127–8.

Chen P.M. , Fan S. , Liu J.H. , Chiou T.J. , Hsieh S.R. , Liu R.S. , Tzeng C.H. Reactivation of hepatitis B virus in two chronic GVHD patients after transplant. Int J Hematol 1993; 58: 183–8.

Locasciulli A. , Testa M. , Valsecchi M.G. , Vecchi L. , Longoni D. , Sparano P. , Rovelli A. , Uderzo C. , Masera G. , Alberti A. Morbidity and mortality due to liver disease in children undergoing allogeneic bone marrow transplantation: A 10-year prospective study. Blood 1997; 90: 3799–805.

Grumayer E.R. , Panzer S. , Ferneci P. , Gadner H. Recurrence of hepatitis B in children with serologic evidence of past hepatitis B virus infection undergoing antileukemic chemotherapy. J Hepatol 1989; 8: 232–5.

Lazizi Y. , Grangeot-Keros L. , Delfraissy J.F. , Boue F. , Dubreuil P. , Badur S. , Pillot J. Reappearance of hepatitis B virus in immune patients infected with the human immunodeficiency virus type I. J Infect Dis 1988; 158: 666–7.

Vento S. , Di Perri G. , Luzzati R. , Cruciani L. , Garofano T. , Mengoli C. , Concia E. , Bassetti D. Clinical reactivation of hepatitis B in anti-HBs-positive patients with AIDS. (letter) Lancet 1989; 2: 332.

Bouslama K. , Knani L. , Cabane J. , Picard O. , Lebas J. , Poupon R. , Imbert J.C. Reactivation of B hepatitis in an anti-HBs positive patient in HIV co-infection. An Med Interna 1991; 142: 63–4.

Maguire D. , Heaton N.D. , Smith H.M. Failure of reactivation of hepatitis B after liver transplantation in hepatitis B surface antigen-negative, core antibody-positive recipients. Transplantation 2002; 72: 481–2.

Pontisso P. , Ruvoletto M.G. , Fattovich G. , Chemello L. , Gallorini A. , Ruol A. , Alberti A. Clinical and virological profiles in patients with multiple hepatitis virus infections. Gastroenterology 1994; 105: 1529–33.

Roche B. , Samuel D. , Gigou M. , Feray C. , Virot V. , Schmets L. , David M.F. , Arulnaden J.L. , Bismuth A. , Reynes M. , Bismuth H. De novo and apparent de novo hepatitis B virus infection after liver transplantation. J Hepatol 1997; 26: 517–26.

Farza H. , Salmon A.M. , Hadchoeul M. , Moreau J.L. , Babinet C. , Tiollais P. , Pourcel C. Hepatitis B surface antigen gene expression is regulated by sex steroids and glucocorticoids in transgenic mice. Proc Natl Acad Sci USA 1987; 84: 1187–91.

Tur Kaspa R. , Burk R.D. , Shaul Y. , Moore D.D. , Shafrotz D.A. Hepatitis B virus DNA contains a glucocorticoid responsive element. Proc Natl Acad Sci USA 1986; 83: 1627–31.

McMillan J.S. , Shaw T. , Angus P.W. , Locarnini S.A. Effect of immunosuppressive and antiviral agents on hepatitis B virus replication in vitro. Hepatology 1995; 22: 36–43.

Cote P.J. , Tennat B.C. , Baldwin B. , Korba B.E. , Gerin J.L. Modulation of WHV infection and disease with cyclosporine A and dexamethasone. International Symposium on Viral Hepatitis and Liver Diseases, Houston, 1990.

Aldersley M.A. , Eglin R.E. , O'Grady J.G. Liver transplantation and de novo hepatitis B infection (letter). Lancet 1994; 343: 677.

Chazouilleres O. , Mamish D. , Kim M. , Carey K. , Ferrell L. , Roberts J.P. , Ascher N.L. , Wright T.L. ‘Occult’ hepatitis B virus as source of infection in liver transplant recipients. Lancet 1994; 343: 142–6.

Wachs M. , Amend W.J. , Ascher N.L. , Bretan P.N. , Emond J. , Lake J.R. , Melzer H.S. , Roberts J.P. , Tomlanovich S.J. , Vincenti F. , Stock P. The risk of transmission of hepatitis B from HBsAg (-), HBcAb (-), HBIgM (-) organ donors. Transplantation 1995; 59: 230–4.

Lowell J.A. , Howard T.K. , White H.M. , Shenoy S. , Huettner P.C. , Brennan D.C. , Peters M.G. Serological evidence of past hepatitis B infection in liver donor and hepatitis B infection in liver allografts. Lancet 1995; 345: 1084–5.

Radomski J.S. , Moritz M.J. , Armenti V.T. , Munoz S.J. Hepatitis B transmission from a liver donor who tested negative for hepatitis B surface antigen and positive for hepatitis B core antibody. Liver Transpl Surg 1996; 2: 130–1.

Douglas D.D. , Rakela J. , Wright T.L. , Krom R.A.F. , Wiesner R.H. The clinical course of transplantation associated de novo hepatitis B infection in the liver transplant recipient. Liver Transpl Surg 1997; 3: 105–11.

Uemoto S. , Sugiyama K. , Marusawa H. , Inomata Y. , Asonuma K. , Egawa H. , Kiuchi T. , Miyake Y. , Tanaka K. , Chiba T. Transmission of hepatitis B virus from hepatitis B core antibody-positive donors in living related liver transplants. Transplantation 1998; 65: 494–9.

Dickson R.C. , Everhart J.E. , Lake J.R. , Wei Y. , Seaberg E.C. , Wiesner R.H. , Zetterman R.K. , Pruett T.L. , Ishitani M.B. , Hoofnagle J.H. , and The National Institute of Diabetes and Digestive and Kidney Diseases Liver Transplantation Database. Transmission of hepatitis B by transplantation of livers from donors positive for antibody to hepatitis B core antigen. The National Institute of Diabetes and Digestive and Kidney Diseases Liver Transplantation Database. Gastroenterology 1997; 113: 1668–74.

Todo S. , Demetris A.J. , van Thiel D.H. , Fung J.J. , Iwaki Y. , Sysyn G. , Ming W. , Trager J. , Starzl T.E. Evolution of hepatitis B virus liver disease after hepatic replacement. Am J Pathol 1990; 137: 667–76.

Davies S.E. , Portmann B.C. , O'Grady J.G. , Aldis P.M. , Chaggar K. , Alexander G.J.M. , Williams R. Hepatic histologic findings after transplantation for chronic hepatitis B virus infection; including a unique pattern of fibrosing cholestatic hepatitis. Hepatology 1991; 13: 150–7.

Lucey M.R. , Graham D.M. , Martin P. , Di Bisceglie A. , Rosenthal S. , Waggoner J.G. , Merion R.M. , Campbell D.A. , Nostrant T.T. , Appelman H.D. Recurrence of hepatitis B and delta hepatitis after orthotopic liver transplantation. Gut 1992; 33: 1390–6.

Konig V. , Hopf U. , Neuhaus P. , Bauditz A. , Schmidt C.A. , Blumhardt G. , Bechstein W.O. , Neuhaus R. , Lobeck H. Long-term follow-up of hepatitis B virus-infected recipients after orthotopic liver transplantation. Transplantation 1994; 58: 553–9.

Dodson S.F. , Issa S. , Araya V. , Gayowski T. , Pinna A. , Eghtesad B. , Iwatsuki S. , Montalvo E. , Rakela J. , Fung J.J. Infectivity of hepatic allografts with antibodies to hepatitis B virus. Transplantation 1997; 64: 1582–4.

Chen Y.S. , Wang C.C. , de Villa V.H. , Wang S.H. , Cheng Y.F. , Huang T.L. , Iawan B. , Chiu K.W. , Chen C.L. Prevention of de novo hepatitis B virus infection in living donor liver transplantation using hepatitis B core antibody positive donors. Clin Transplant 2002; 16: 405–9.

Dodson S.F. , Bonham C.A. , Geller D.A. , Cacciarelli T.V. , Rakela J. , Fung J.J. Prevention of de novo hepatitis B infection in recipients of hepatic allografts from anti-HBc positive donors. Transplantation 1999; 68: 1058–61.

Joya-Vazquez P.P. , Dodson F.S. , Dvorchik I. , Gray E. , Chesky A. , Demetris A.J. , Shakil O. , Fung J.J. , Vargas H.E. Impact of anti-hepatitis B core-positive grafts on the outcome of liver transplantation for HBV-related cirrhosis. Transplantation 2002; 73: 1598–602.

Satterthwaite R. , Ozgu I. , Shibdan H. , Aswad S. , Sunga V. , Zapanta R. , Asai P. , Bogaard T. , Khetan U. , Mendez R.G. , Mendez R. Risks of transplanting kidneys from hepatitis B surface antigen-negative, hepatitis B core antibody-positive donors. Transplantation 1997; 64: 432–5.

Madayag R.M. , Johnson L.B. , Bartlett S.T. , Schweitzer E.J. , Constantine N.T. , McCarter R.J. , Kuo P.C. , Keay S. , Oldach D.W. Use of renal allografts from donors positive for hepatitis B core antibody confers minimal risk for subsequent development of clinical hepatitis B virus disease. Transplantation 1997; 64: 1781–6.

Krieger N.R. , Vial C.M. , Millan M.T. , Imperial J. , Dafoe D.C. , Scandling J.D. Revisiting the use of hepatitis B core antibody-positive donor kidneys. Transplant Proc 2001; 33: 1535–6.

Kadian M. , Hawkins K. , Schwartz H. , Miller C. Use of hepatitis B core antibody-positive multi-organ donors. J Transplant Coord 1994; 4: 57–60.

Fong T.L. , Bunnapradist S. , Jordan S.C. , Cho Y.W. Impact of hepatitis B core antibody status on outcomes of cadaveric renal transplantation: analysis of United Network of Organ Sharing database between 1994 and 1999. Transplantation 2002; 73: 85–9.

Cirocco R. , Zucker K. , Contreras N. , Olson L. , Cravero J. , Markou M. , Babischkin S. , Fernandez E. , Burke G.W. , Esquenazi V. , Tzakis A. , Miller J. The presence of hepatitis B core antibody does not preclude kidney donation. Lack of viral DNA in the serum and biopsies of core antibody positive donors and clinical follow-up (letter). Transplantation 1997; 63: 1702–4.

Turner D.P. , Zuckerman M. , Alexander G.J.M. , Waite J. , Wreghitt T. Risk of inappropriate exclusion of organ donors by introduction of hepatitis B core antibody testing. Transplantation 1997; 63: 775–8.

Kroes A.C.M. , Quint W.G.V. , Heijtink R.A. Significance of isolated hepatitis B core antibodies detected by enzyme immunoassay in a high risk population. J Med Virol 1991; 35: 96–9.

Hughes W. , Barr A. , Dow B.C. , Follett E.A.C. , Barbara J.A.J. A multicentre assessment of the specificity of ten anti-HBc screening tests. Transfus Med 1995; 5: 225–9.

Delmonico F.L. , Snydman D.R. Organ donor screening for infectious diseases. Transplantation 1998; 65: 603–10.

Terrault N. , Zhou S. , Combs C. , Hahn J.A. , Lake J.R. , Roberts J.P. , Ascher N.L. , Wright T.L. Prophylaxis in liver transplant recipients using a fixed dosing schedule of hepatitis B immunoglobulin. Hepatology 1996; 24: 1327–33.

Mutimer D. , Dusheiko G. , Barrett C. , Grellier L. , Ahmed M. , Anschuetz G. , Burroughs A. , Hubscher S. , Dhillon A.P. , Rolles K. , Elias E. Lamivudine without HBIg for prevention of graft reinfection by hepatitis B: long-term follow-up. Transplantation 2000; 70: 809–15.

Markowitz J.S. , Martin P. , Conrad A.J. , Markmann J.F. , Seu P. , Yersiz H. , Goss J.A. , Schmidt P. , Pakrasi A. , Artinian L. , Murray N.G. , Imagawa D.K. , Holt C. , Goldstein L.I. , Stribling R. , Busuttil R.W. Prophylaxis against hepatitis B recurrence following liver transplantation using combination lamivudine and hepatitis B immune globulin. Hepatology 1998; 28: 585–9.

Han S.F. , Ofman J. , Holt C. , King K. , Kunder G. , Chen P. , Dawson S. , Goldstein L. , Yersiz H. , Farmer D.G. , Ghobrial R.M. , Busuttil R.W. , Martin P. 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: 741–8.

Douglas D.R.J. , Mamish D. , Wright T. , Krom R. , Wiesner R. Transmission of hepatitis B virus infection from orthotopic donor livers. (abstract). Hepatology 1992; 16: 49A.