Changes in the relationship between hepatitis B virus and liver transplantation in the last decades

Abstract

In the last decade, both hepatitis B virus (HBV) prevalence and mortality related to HBV infection have decreased promptly. Worldwide HBV vaccination programs, precautions against HBV transmission and effective anti-viral drugs on market play crucial role for this encouraging result. Besides stopping or reversing the hepato-fibrogenesis induced by HBV infection, fighting against HBV related acute severe hepatitis are also improved recently. HBV associated cirrhosis is still the major cause of LTx, particularly in developing countries,whereas in developed countries, the rate of LTx due to HBV induced cirrhosis has declined over time. With the expanding use of NUCs before LTx, and the use of NUCs and HBIg even after LTx, HBV recurrence after LTx is no longer an important reason for graft loss or patient death. However, this positive impact is not yet reflecting survival, probably because of increasing recipient and donor ages. On the other hand, in the era of Milan criteria, overall hepatocellular carcinoma (HCC) survival has so increased that the number of transplanted HCC cases has almost doubled. However tumor recurrence is still the major cause of death, and treatment is still problematic.

Keywords

• hepatitis B virus,acute or chronic infection,cirrhosis,hepatocellular carcinoma,liver transplantation,vaccine

Hepatit B virus enfeksiyonu nedenli karaciğer nakillerde son yıllardaki değişim

Abstract

Hepatit B virus (HBV) enfeksiyonu prevelansındaki ve HBV ilişkili mortalitesindeki azalma son yıllarda oldukça dikkat çekicidir. Dünya çapında yaygın olarak uygulanan HBV aşı programları ve HBV’ye karşı kullanımda olan anti-viral ilaçların etkinliği bu başarıda başat rol oynamaktadır. HBV ile mücadelede, sadece HBV’ye bağlı karaciğer fibrozunun ilerlemesi veya geriye döndürülmesi değil, aynı zamanda HBV ilişkili şiddetli akut hepatit tablosunun tedavisinde güzel sonuçlar alınmaktadır. Gelişmekte olan ülkelerde HBV ilişkili siroz karaciğer nakli konusunda halen esas sebep iken, gelişmiş ülkelerde zaman içinde HBV nedenli karaciğer nakil sıklıkları ciddi oranda düşüş göstermiştir. Anti-viral ilaçların karaciğer nakli öncesi etkin kullanımı, HBIg tedavisinin nakil sonrasında yaygın olarak kullanımı sayesinde karaciğer nakli sonrası HBV nüksü, mortalite ve greft kaybı konusunda eskisi kadar sorun olmaktan çıkmıştır. Bu başarının nakil sonrası sürviler üzerine bariz bir yansıması henüz olmamıştır. Buradaki esas sebep ise, alıcı ve verici yaşının son yıllarda önemli oranda artış göstermesi olarak gösterilmektedir. Ekolarak, Milan kriterlerinin yaygın olarak klinik pratiğe girmesiyle karaciğer nakli yapılan hepatosellüler kanser (HCC) hasta sayısı da neredeyse ikiye katlamıştır. Ancak, HCC rekürrensi, nakil sonrası en önemli ölüm nedeni olarak devam etmektedir.

Keywords

• Hepatit B virus,akut ve kronik HBV enfeksiyonu,siroz,hepatosellüler kanser,karaciğer nakli,aşı

References

1. 1. A review of chronic hepatitis B epidemiology and management issues in selected countries in the Middle East. J Viral Hepat 2012. 19(1): p. 9-22.
2. 2. Schweitzer, A., et al., Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet, 2015.
3. 3. Locarnini, S., et al., Strategies to control hepatitis B: Public policy, epidemiology, vaccine and drugs. J Hepatol, 2015. 62(1 Suppl): p. S76-86.
4. 4. Shepard, C.W., et al., Hepatitis B virus infection: epidemiology and vaccination. Epidemiol Rev, 2006. 28: p. 112-25.
5. 5. Degertekin, H. and G. Gunes, Horizontal transmission of hepatitis B virus in Turkey. Public Health, 2008. 122(12): p. 1315-7.
6. 6. Goyal, A. and J.M. Murray, The impact of vaccination and antiviral therapy on hepatitis B and hepatitis D epidemiology. PLoS One, 2014. 9(10): p. e110143.
7. 7. Liang, X., et al., Epidemiological serosurvey of hepatitis B in China--declining HBV prevalence due to hepatitis B vaccination. Vaccine, 2009. 27(47): p. 6550-7.
8. 8. Rantala, M. and M.J. van de Laar, Surveillance and epidemiology of hepatitis B and C in Europe - a review. Euro Surveill, 2008. 13(21).

9. 9. Altinbas, S., M. Erdogan, and N. Danisman, The seroprevalences of HBs Ag and anti-HCV in pregnant women in Ankara. Arch Gynecol Obstet, 2010. 281(2): p. 371.
10. 10. EASL clinical practice guidelines: Management of chronic hepatitis B virus infection. J Hepatol, 2012. 57(1): p. 167-85.
11. 11. Lok, A.S. and B.J. McMahon, Chronic hepatitis B: update 2009. Hepatology, 2009. 50(3): p. 661-2.
12. 12. Han, G.R., et al., A prospective and open-label study for the efficacy and safety of telbivudine in pregnancy for the prevention of perinatal transmission of hepatitis B virus infection. J Hepatol, 2011. 55(6): p. 1215-21.
13. 13. Nunez, M., Routine hepatitis B virus DNA testing in human immunodeficiency virus-infected patients with positive hepatitis B core antibody but negative hepatitis B surface antigen is not justified by current evidence. Hepatology, 2010. 51(3): p. 1087-8.
14. 14. McMahon, B.J., et al., Acute hepatitis B virus infection: relation of age to the clinical expression of disease and subsequent development of the carrier state. J Infect Dis, 1985. 151(4): p. 599-603.
15. 15. Tillmann, H.L., K. Zachou, and G.N. Dalekos, Management of severe acute to fulminant hepatitis B: to treat or not to treat or when to treat? Liver Int, 2012. 32(4): p. 544-53.
16. 16. Kuruuzum, Z., et al., Rate of chronicity and time of disappearance of HBsAg following acute hepatitis B. Hepatogastroenterology, 2009. 56(90): p. 466-9.
17. 17. Zhang, H.W., et al., Risk factors for acute hepatitis B and its progression to chronic hepatitis in Shanghai, China. Gut, 2008. 57(12): p. 1713-20.
18. 18. Altinbas, A., et al., Spontaneous HBsAg seroconversion after severe flare of chronic hepatitis B infection. Ann Hepatol, 2010. 9(2): p. 194-7.
19. 19. Cornberg, M., et al., Prophylaxis, diagnosis and therapy of hepatitis B virus (HBV) infection: the German guidelines for the management of HBV infection. Z Gastroenterol, 2007. 45(12): p. 1281-328.
20. 20. Tillmann, H.L., et al., Safety and efficacy of lamivudine in patients with severe acute or fulminant hepatitis B, a multicenter experience. J Viral Hepat, 2006. 13(4): p. 256-63.
21. 21. Miyake, Y., et al., Lamivudine treatment improves the prognosis of fulminant hepatitis B. Intern Med, 2008. 47(14): p. 1293-9.
22. 22. Hadem, J., et al., Etiologies and outcomes of acute liver failure in Germany. Clin Gastroenterol Hepatol, 2012. 10(6): p. 664-9 e2.
23. 23. Fujiwara, K., et al., Fulminant hepatitis and late onset hepatic failure in Japan. Hepatol Res, 2008. 38(7): p. 646-57.
24. 24. Kumar, M., et al., A randomized controlled trial of lamivudine to treat acute hepatitis B. Hepatology, 2007. 45(1): p. 97-101.
25. 25. Torii, N., et al., Effectiveness and long-term outcome of lamivudine therapy for acute hepatitis B. Hepatol Res, 2002. 24(1): p. 34.
26. 26. Kondili, L.A., H. Osman, and D. Mutimer, The use of lamivudine for patients with acute hepatitis B (a series of cases). J Viral Hepat, 2004. 11(5): p. 427-31.
27. 27. Yu, J.W., et al., Lamivudine treatment is associated with improved survival in fulminant hepatitis B. Liver Int, 2011. 31(4): p. 499-506.
28. 28. Yu, J.W., et al., The study of efficacy of lamivudine in patients with severe acute hepatitis B. Dig Dis Sci, 2010. 55(3): p. 775-83.
29. 29. Dao, D.Y., et al., Use of nucleoside (tide) analogues in patients with hepatitis B-related acute liver failure. Dig Dis Sci, 2012. 57(5): p. 1349-57.
30. 30. Lange, C.M., et al., Severe lactic acidosis during treatment of chronic hepatitis B with entecavir in patients with impaired liver function. Hepatology, 2009. 50(6): p. 2001-6.
31. 31. Yuen, M.F., Anti-viral therapy in hepatitis B virus reactivation with acute-on-chronic liver failure. Hepatol Int, 2015. 9(3): p. 373-7.
32. 32. Wong, V.W., et al., Entecavir treatment in patients with severe acute exacerbation of chronic hepatitis B. J Hepatol, 2011. 54(2): p. 236-42.
33. 33. Chen, C.H., et al., Entecavir vs. lamivudine in chronic hepatitis B patients with severe acute exacerbation and hepatic decompensation. J Hepatol, 2014. 60(6): p. 1127-34.
34. 34. Tsai, W.L., et al., Early entecavir treatment for chronic hepatitis B with severe acute exacerbation. Antimicrob Agents Chemother, 2014. 58(4): p. 1918-21.
35. 35. Adam, R., et al., Evolution of indications and results of liver transplantation in Europe. A report from the European Liver Transplant Registry (ELTR). J Hepatol, 2012. 57(3): p. 675-88.
36. 36. Campsen, J., et al., Outcomes of living donor liver transplantation for acute liver failure: the adult-to-adult living donor liver transplantation cohort study. Liver Transpl, 2008. 14(9): p. 1273-80.
37. 37. Ostapowicz, G., et al., Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann Intern Med, 2002. 137(12): p. 947-54.
38. 38. de Villa, V.H., C.M. Lo, and C.L. Chen, Ethics and rationale of living-donor liver transplantation in Asia. Transplantation, 2003. 75(3 Suppl): p. S2-5.
39. 39. Liu, C.L., et al., Right-lobe live donor liver transplantation improves survival of patients with acute liver failure. Br J Surg, 2002. 89(3): p. 317-22.
40. 40. Kayaalp, C., V. Ersan, and S. Yilmaz, Acute liver failure in Turkey: a systematic review. Turk J Gastroenterol, 2014. 25(1): p. 35-40.
41. 41. Matsui, Y., et al., Living donor liver transplantation for fulminant hepatic failure. Hepatol Res, 2008. 38(10): p. 987-96.
42. 42. Park, S.J., et al., Emergency adult-to-adult living-donor liver transplantation for acute liver failure in a hepatitis B virus endemic area. Hepatology, 2010. 51(3): p. 903-11.
43. 43. Germani, G., et al., Liver transplantation for acute liver failure in Europe: outcomes over 20 years from the ELTR database. J Hepatol, 2012. 57(2): p. 288-96.
44. 44. Ikegami, T., et al., Living donor liver transplantation for acute liver failure: a 10-year experience in a single center. J Am Coll Surg, 2008. 206(3): p. 412-8.
45. 45. Qiu, J., M. Ozawa, and P.I. Terasaki, Liver transplantation in the United States. Clin Transpl, 2005: p. 17-28.
46. 46. Vagefi, P.A., et al., Use of living donor liver transplantation varies with the availability of deceased donor liver transplantation. Liver Transpl, 2012. 18(2): p. 160-5.
47. 47. Carlisle, E.M. and G. Testa, Adult to adult living related liver transplantation: where do we currently stand? World J Gastroenterol, 2012. 18(46): p. 6729-36.
48. 48. Mutimer, D.J. and A. Lok, Management of HBV- and HCV-induced end stage liver disease. Gut, 2012. 61 Suppl 1: p. i59-67.
49. 49. Ertle, J., et al., Non-alcoholic fatty liver disease progresses to hepatocellular carcinoma in the absence of apparent cirrhosis. Int J Cancer, 2011. 128(10): p. 2436-43.
50. 50. Altinbas, A., et al., Retrospective analysis of total direct medical costs associated with hepatitis B patients with oral antiviral versus pegylated interferon therapy in Turkey. J Viral Hepat, 2014. 21(11): p. 794-801.
51. 51. Kim, W.R., Epidemiology of hepatitis B in the United States. Hepatology, 2009. 49(5 Suppl): p. S28-34.
52. 52. Bernal, W., et al., Outcome after wait-listing for emergency liver transplantation in acute liver failure: a single centre experience. J Hepatol, 2009. 50(2): p. 306-13.
53. 53. Liaw, Y.F., et al., Efficacy and safety of entecavir versus adefovir in chronic hepatitis B patients with hepatic decompensation: a randomized, open-label study. Hepatology, 2011. 54(1): p. 91-100.
54. 54. Marcellin, P., et al., Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet, 2013. 381(9865): p. 468-75.
55. 55. Lau, G.K., et al., Peginterferon Alfa-2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N Engl J Med, 2005. 352(26): p. 2682-95.
56. 56. Marcellin, P., et al., Peginterferon alfa-2a alone, lamivudine alone, and the two in combination in patients with HBeAg-negative chronic hepatitis B. N Engl J Med, 2004. 351(12): p. 1206-17.
57. 57. Hoofnagle, J.H., et al., Interferon alfa for patients with clinically apparent cirrhosis due to chronic hepatitis B. Gastroenterology, 1993. 104(4): p. 1116-21.
58. 58. Perrillo, R., et al., Low-dose, titratable interferon alfa in decompensated liver disease caused by chronic infection with hepatitis B virus. Gastroenterology, 1995. 109(3): p. 908-16.
59. 59. Lok, A.S., et al., Long-term safety of lamivudine treatment in patients with chronic hepatitis B. Gastroenterology, 2003. 125(6): p. 1714-22.
60. 60. Dienstag, J.L., et al., Histological outcome during long-term lamivudine therapy. Gastroenterology, 2003. 124(1): p. 105-17.
61. 61. Hadziyannis, S.J., et al., Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B for up to 5 years. Gastroenterology, 2006. 131(6): p. 1743-51.
62. 62. Chang, T.T., et al., Long-term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology, 2010. 52(3): p. 886-93.
63. 63. Heathcote, E.J., et al., Three-year efficacy and safety of tenofovir disoproxil fumarate treatment for chronic hepatitis B. Gastroenterology, 2011. 140(1): p. 132-43.
64. 64. Yao, F.Y., et al., Lamivudine treatment is beneficial in patients with severely decompensated cirrhosis and actively replicating hepatitis B infection awaiting liver transplantation: a comparative study using a matched, untreated cohort. Hepatology, 2001. 34(2): p. 411-6.
65. 65. Koklu, S., et al., Long-term efficacy and safety of lamivudine, entecavir, and tenofovir for treatment of hepatitis B virus-related cirrhosis. Clin Gastroenterol Hepatol, 2013. 11(1): p. 88-94.
66. 66. Liaw, Y.F., et al., Tenofovir disoproxil fumarate (TDF), emtricitabine/TDF, and entecavir in patients with decompensated chronic hepatitis B liver disease. Hepatology, 2011. 53(1): p. 62-72.
67. 67. Shim, J.H., et al., Efficacy of entecavir in treatment-naive patients with hepatitis B virus-related decompensated cirrhosis. J Hepatol, 2010. 52(2): p. 176-82.
68. 68. Burra, P., et al., Liver transplantation for HBV-related cirrhosis in Europe: an ELTR study on evolution and outcomes. J Hepatol, 2013. 58(2): p. 287-96.
69. 69. Mascarenhas, R. and A. Gurakar, Recent advances in liver transplantation for the practicing gastroenterologist. Gastroenterol Hepatol (N Y), 2009. 5(6): p. 443-50.
70. 70. Gane, E.J., et al., Lamivudine plus low-dose hepatitis B immunoglobulin to prevent recurrent hepatitis B following liver transplantation. Gastroenterology, 2007. 132(3): p. 931-7.
71. 71. Gane, E., Posttransplant prophylaxis strategies for hepatitis B. Am J Transplant, 2010. 10(8): p. 1721-2.
72. 72. Perrillo, R., et al., Entecavir and hepatitis B immune globulin in patients undergoing liver transplantation for chronic hepatitis B. Liver Transpl, 2013. 19(8): p. 887-95.
73. 73. Cholongitas, E. and G.V. Papatheodoridis, High genetic barrier nucleos(t)ide analogue(s) for prophylaxis from hepatitis B virus recurrence after liver transplantation: a systematic review. Am J Transplant, 2013. 13(2): p. 353-62.
74. 74. Burroughs, A.K., et al., 3-month and 12-month mortality after first liver transplant in adults in Europe: predictive models for outcome. Lancet, 2006. 367(9506): p. 225-32.
75. 75. Karam, V., et al., Quality control of the European Liver Transplant Registry: results of audit visits to the contributing centers. Transplantation, 2003. 75(12): p. 2167-73.
76. 76. Yamashiki, N., et al., Outcomes after living donor liver transplantation for acute liver failure in Japan: results of a nationwide survey. Liver Transpl, 2012. 18(9): p. 1069-77.
77. 77. Clavien, P.A., et al., Recommendations for liver transplantation for hepatocellular carcinoma: an international consensus conference report. Lancet Oncol, 2012. 13(1): p. e11-22.
78. 78. Yim, S.Y., et al., The management and prognosis of patients with hepatocellular carcinoma: what has changed in 20 years? Liver Int, 2015.
79. 79. Kim, W.R., et al., Impact of long-term tenofovir disoproxil fumarate on incidence of hepatocellular carcinoma in patients with chronic hepatitis B. Cancer, 2015. 121(20): p. 3631-8.
80. 80. Mancuso, A. and G. Perricone, Hepatocellular Carcinoma and Liver Transplantation: State of the Art. J Clin Transl Hepatol, 2014. 2(3): p. 176-81.
81. 81. Kwon, H. and A.S. Lok, Does antiviral therapy prevent hepatocellular carcinoma? Antivir Ther, 2011. 16(6): p. 787-95.
82. 82. Yang, H.I., et al., Hepatitis B e antigen and the risk of hepatocellular carcinoma. N Engl J Med, 2002. 347(3): p. 168-74.
83. 83. Lee, M.H., et al., Prediction models of long-term cirrhosis and hepatocellular carcinoma risk in chronic hepatitis B patients: risk scores integrating host and virus profiles. Hepatology, 2013. 58(2): p. 546-54.
84. 84. Loomba, R., et al., Synergistic effects of family history of hepatocellular carcinoma and hepatitis B virus infection on risk for incident hepatocellular carcinoma. Clin Gastroenterol Hepatol, 2013. 11(12): p. 1636-45 e1-3.
85. 85. de Lope, C.R., et al., Management of HCC. J Hepatol, 2012. 56 Suppl 1: p. S75-87.
86. 86. Forner, A., J.M. Llovet, and J. Bruix, Hepatocellular carcinoma. Lancet, 2012. 379(9822): p. 1245-55.
87. 87. Chen, Q.W., et al., Radiofrequency ablation plus chemoembolization versus radiofrequency ablation alone for hepatocellular carcinoma: A systematic review and meta-analysis. Clin Res Hepatol Gastroenterol, 2015.
88. 88. Lok, A.S., Does antiviral therapy for hepatitis B and C prevent hepatocellular carcinoma? J Gastroenterol Hepatol, 2011. 26(2): p. 221-7.
89. 89. Leroy, V. and T. Asselah, Universal hepatitis B vaccination: the only way to eliminate hepatocellular carcinoma? J Hepatol, 2015.
90. 90. Chang, M.H., et al., Decreased incidence of hepatocellular carcinoma in hepatitis B vaccinees: a 20-year follow-up study. J Natl Cancer Inst, 2009. 101(19): p. 1348-55.
91. 91. Yang, Y.F., et al., Interferon therapy in chronic hepatitis B reduces progression to cirrhosis and hepatocellular carcinoma: a meta-analysis. J Viral Hepat, 2009. 16(4): p. 265-71.
92. 92. Lin, S.M., et al., Interferon therapy in HBeAg positive chronic hepatitis reduces progression to cirrhosis and hepatocellular carcinoma. J Hepatol, 2007. 46(1): p. 45-52.
93. 93. Sung, J.J., et al., Meta-analysis: Treatment of hepatitis B infection reduces risk of hepatocellular carcinoma. Aliment Pharmacol Ther, 2008. 28(9): p. 1067-77.
94. 94. Idilman, R., et al., Long-term entecavir or tenofovir disoproxil fumarate therapy in treatment-naive chronic hepatitis B patients in the real-world setting. J Viral Hepat, 2015. 22(5): p. 504-10.
95. 95. Hosaka, T., et al., Long-term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology, 2013. 58(1): p. 98-107.
96. 96. Cho, J.Y., et al., Patients with chronic hepatitis B treated with oral antiviral therapy retain a higher risk for HCC compared with patients with inactive stage disease. Gut, 2014. 63(12): p. 1943-50.
97. 97. Kim, S.S., et al., Effect of virological response to entecavir on the development of hepatocellular carcinoma in hepatitis B viral cirrhotic patients: comparison between compensated and decompensated cirrhosis. Am J Gastroenterol, 2014. 109(8): p. 1223-33.
98. 98. Kurokawa, M., et al., Long-term effect of lamivudine treatment on the incidence of hepatocellular carcinoma in patients with hepatitis B virus infection. J Gastroenterol, 2012. 47(5): p. 577-85.
99. 99. Liu, G.M., et al., Adjuvant antiviral therapy for hepatitis B virus-related hepatocellular carcinoma after curative treatment: A systematic review and meta-analysis. Hepatol Res, 2015.
100. 100. Sun, P., et al., Nucleot(s)ide analogues for hepatitis B virus-related hepatocellular carcinoma after curative treatment: a systematic review and meta-analysis. PLoS One, 2014. 9(7): p. e102761.
101. 101. An, H.J., et al., Sustained low hepatitis B viral load predicts good outcome after curative resection in patients with hepatocellular carcinoma. J Gastroenterol Hepatol, 2010. 25(12): p. 1876-82.
102. 102. Xu, J., et al., Effect of adjuvant interferon therapy on hepatitis b/c virus-related hepatocellular carcinoma after curative therapy - meta-analysis. Adv Clin Exp Med, 2015. 24(2): p. 331-40.
103. 103. Han, S.H., et al., Clinical outcomes of liver transplantation for HBV-related hepatocellular carcinoma: data from the NIH HBV OLT study. Clin Transplant, 2011. 25(2): p. E152-62.
104. 104. Poon, R.T., et al., Difference in tumor invasiveness in cirrhotic patients with hepatocellular carcinoma fulfilling the Milan criteria treated by resection and transplantation: impact on long-term survival. Ann Surg, 2007. 245(1): p. 51-8.
105. 105. Otto, G., et al., Response to transarterial chemoembolization as a biological selection criterion for liver transplantation in hepatocellular carcinoma. Liver Transpl, 2006. 12(8): p. 1260-7.
106. 106. Garwood, E.R., et al., Morbidity and mortality following transarterial liver chemoembolization in patients with hepatocellular carcinoma and synthetic hepatic dysfunction. Liver Transpl, 2013. 19(2): p. 164-73.
107. 107. Collett, D., et al., Comparison of the incidence of malignancy in recipients of different types of organ: a UK Registry audit. Am J Transplant, 2010. 10(8): p. 1889-96.
108. 108. Welker, M.W., et al., Recurrent hepatocellular carcinoma after liver transplantation - an emerging clinical challenge. Transpl Int, 2013. 26(2): p. 109-18.