Liver Fibrosis Reversion After Suppression of Hepatitis B Virus

Clinics in Liver Disease

Volumn 20, Issue 4, 2016, Pages 667-679

  Rockey, Don C ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Cirrhosis; Hepatocellular carcinoma; HIV; Portal hypertension; Regression; Stellate cell; Viral suppression

Indexed keywords

ADEFOVIR; ENTECAVIR; LAMIVUDINE; TENOFOVIR; ANTIVIRUS AGENT; VIRUS DNA;

ANTIFIBROTIC THERAPY; ANTIVIRAL THERAPY; CANCER RISK; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; LIVER BIOPSY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FIBROSIS; NONHUMAN; PATHOGENESIS; PORTAL HYPERTENSION; REMISSION; REVIEW; RISK ASSESSMENT; VIRUS INHIBITION; VIRUS REPLICATION; CHRONIC HEPATITIS B; COMPLICATION; DRUG EFFECTS; GENETICS; GLOBAL HEALTH; INCIDENCE; VIROLOGY;

ANTIVIRAL AGENTS; DNA, VIRAL; GLOBAL HEALTH; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; INCIDENCE; LIVER CIRRHOSIS;

EID: 84992183690     PISSN: 10893261     EISSN: 15578224     Source Type: Journal    
DOI: 10.1016/j.cld.2016.06.003     Document Type: Review

References (62)

1. 1 Rockey, D.C., Bell, P.D., Hill, J.A., Fibrosis–a common pathway to organ injury and failure. N Engl J Med 372:12 (2015), 1138–1149.
2. 2 Lozano, R., Naghavi, M., Foreman, K., et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:9859 (2012), 2095–2128.
3. 3 Iredale, J.P., Benyon, R.C., Pickering, J., et al. Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J Clin Invest 102:3 (1998), 538–549.
4. 4 Rockey, D.C., Translating an understanding of the pathogenesis of hepatic fibrosis to novel therapies. Clin Gastroenterol Hepatol 11:3 (2013), 224–231.e1-5.
5. 5 Rockey, D.C., Antifibrotic therapy in chronic liver disease. Clin Gastroenterol Hepatol 3:2 (2005), 95–107.
6. 6 Rockey, D.C., Chung, J.J., Endothelin antagonism in experimental hepatic fibrosis. Implications for endothelin in the pathogenesis of wound healing. J Clin Invest 98:6 (1996), 1381–1388.
7. 7 Ellis, E.L., Mann, D.A., Clinical evidence for the regression of liver fibrosis. J Hepatol 56:5 (2012), 1171–1180.
8. 8 Crespo-Leiro, M.G., Robles, O., Paniagua, M.J., et al. Reversal of cardiac cirrhosis following orthotopic heart transplantation. Am J Transplant 8:6 (2008), 1336–1339.
9. 9 Czaja, A.J., Carpenter, H.A., Decreased fibrosis during corticosteroid therapy of autoimmune hepatitis. J Hepatol 40:4 (2004), 646–652.
10. 10 Liaw, Y.F., Sung, J.J., Chow, W.C., et al. Lamivudine for patients with chronic hepatitis B and advanced liver disease. N Engl J Med 351:15 (2004), 1521–1531.
11. 11 El-Husseini, R., Kaplan, M.M., Reversal of portal hypertension in a patient with primary biliary cirrhosis: disappearance of esophageal varices and thrombocytopenia. Am J Gastroenterol 99:9 (2004), 1859–1860.
12. 12 Hammel, P., Couvelard, A., O'Toole, D., et al. Regression of liver fibrosis after biliary drainage in patients with chronic pancreatitis and stenosis of the common bile duct. N Engl J Med 344:6 (2001), 418–423.
13. 13 Wanless, I.R., Nakashima, E., Sherman, M., Regression of human cirrhosis. Morphologic features and the genesis of incomplete septal cirrhosis. Arch Pathol Lab Med 124:11 (2000), 1599–1607.
14. 14 Dufour, J.F., DeLellis, R., Kaplan, M.M., Reversibility of hepatic fibrosis in autoimmune hepatitis. Ann Intern Med 127:11 (1997), 981–985.
15. 15 Kweon, Y.O., Goodman, Z.D., Dienstag, J.L., et al. Decreasing fibrogenesis: an immunohistochemical study of paired liver biopsies following lamivudine therapy for chronic hepatitis B. J Hepatol 35:6 (2001), 749–755.
16. 16 Chang, T.T., Liaw, Y.F., Wu, S.S., et al. Long-term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology 52:3 (2010), 886–893.
17. 17 Marcellin, P., Gane, E., Buti, M., et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet 381:9865 (2013), 468–475.
18. 18 Liaw, Y.F., Reversal of cirrhosis: an achievable goal of hepatitis B antiviral therapy. J Hepatol 59:4 (2013), 880–881.
19. 19 Shiratori, Y., Imazeki, F., Moriyama, M., et al. Histologic improvement of fibrosis in patients with hepatitis C who have sustained response to interferon therapy. Ann Intern Med 132:7 (2000), 517–524.
20. 20 Poynard, T., McHutchison, J., Manns, M., et al. Impact of pegylated interferon alfa-2b and ribavirin on liver fibrosis in patients with chronic hepatitis C. Gastroenterology 122:5 (2002), 1303–1313.
21. 21 Mallet, V., Gilgenkrantz, H., Serpaggi, J., et al. Brief communication: the relationship of regression of cirrhosis to outcome in chronic hepatitis C. Ann Intern Med 149:6 (2008), 399–403.
22. 22 Farci, P., Roskams, T., Chessa, L., et al. Long-term benefit of interferon alpha therapy of chronic hepatitis D: regression of advanced hepatic fibrosis. Gastroenterology 126:7 (2004), 1740–1749.
23. 23 Powell, L.W., Kerr, J.F., Reversal of “cirrhosis” in idiopathic haemochromatosis following long-term intensive venesection therapy. Australas Ann Med 19:1 (1970), 54–57.
24. 24 Blumberg, R.S., Chopra, S., Ibrahim, R., et al. Primary hepatocellular carcinoma in idiopathic hemochromatosis after reversal of cirrhosis. Gastroenterology 95:5 (1988), 1399–1402.
25. 25 Sorensen, T.I., Orholm, M., Bentsen, K.D., et al. Prospective evaluation of alcohol abuse and alcoholic liver injury in men as predictors of development of cirrhosis. Lancet 2:8397 (1984), 241–244.
26. 26 Berhe, N., Myrvang, B., Gundersen, S.G., Reversibility of schistosomal periportal thickening/fibrosis after praziquantel therapy: a twenty-six month follow-up study in Ethiopia. Am J Trop Med Hyg 78:2 (2008), 228–234.
27. 27 Sohara, N., Znoyko, I., Levy, M.T., et al. Reversal of activation of human myofibroblast-like cells by culture on a basement membrane-like substrate. J Hepatol 37:2 (2002), 214–221.
28. 28 Deleve, L.D., Wang, X., Guo, Y., Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology 48:3 (2008), 920–930.
29. 29 Troeger, J.S., Mederacke, I., Gwak, G.Y., et al. Deactivation of hepatic stellate cells during liver fibrosis resolution in mice. Gastroenterology 143:4 (2012), 1073–1083.e22.
30. 30 Iredale, J.P., Stellate cell behavior during resolution of liver injury. Semin Liver Dis 21:3 (2001), 427–436.
31. 31 Preaux, A.M., D'Ortho, M.P., Bralet, M.P., et al. Apoptosis of human hepatic myofibroblasts promotes activation of matrix metalloproteinase-2. Hepatology 36:3 (2002), 615–622.
32. 32 Li, L., Tao, J., Davaille, J., et al. 15-deoxy-Delta 12,14-prostaglandin J2 induces apoptosis of human hepatic myofibroblasts. A pathway involving oxidative stress independently of peroxisome-proliferator-activated receptors. J Biol Chem 276:41 (2001), 38152–38158.
33. 33 Thoen, L.F., Guimaraes, E.L., Grunsven, L.A., Autophagy: a new player in hepatic stellate cell activation. Autophagy 8:1 (2012), 126–128.
34. 34 Thoen, L.F., Guimaraes, E.L., Dolle, L., et al. A role for autophagy during hepatic stellate cell activation. J Hepatol 55:6 (2011), 1353–1360.
35. 35 Hernndez-Gea, V., Friedman, S.L., Autophagy fuels tissue fibrogenesis. Autophagy 8:5 (2012), 849–850.
36. 36 Hernandez-Gea, V., Ghiassi-Nejad, Z., Rozenfeld, R., et al. Autophagy releases lipid that promotes fibrogenesis by activated hepatic stellate cells in mice and in human tissues. Gastroenterology 142:4 (2012), 938–946.
37. 37 Schnabl, B., Purbeck, C.A., Choi, Y.H., et al. Replicative senescence of activated human hepatic stellate cells is accompanied by a pronounced inflammatory but less fibrogenic phenotype. Hepatology 37:3 (2003), 653–664.
38. 38 Krizhanovsky, V., Yon, M., Dickins, R.A., et al. Senescence of activated stellate cells limits liver fibrosis. Cell 134:4 (2008), 657–667.
39. 39 Kong, X., Feng, D., Wang, H., et al. Interleukin-22 induces hepatic stellate cell senescence and restricts liver fibrosis in mice. Hepatology 56:3 (2012), 1150–1159.
40. 40 Marcellin, P., Asselah, T., Long-term therapy for chronic hepatitis B: hepatitis B virus DNA suppression leading to cirrhosis reversal. J Gastroenterol Hepatol 28:6 (2013), 912–923.
41. 41 Dienstag, J.L., Goldin, R.D., Heathcote, E.J., et al. Histological outcome during long-term lamivudine therapy. Gastroenterology 124:1 (2003), 105–117.
42. 42 Rizzetto, M., Tassopoulos, N.C., Goldin, R.D., et al. Extended lamivudine treatment in patients with HBeAg-negative chronic hepatitis B. J Hepatol 42:2 (2005), 173–179.
43. 43 Hadziyannis, S.J., Tassopoulos, N.C., Heathcote, E.J., et al. Long-term therapy with adefovir dipivoxil for HBeAg-negative chronic hepatitis B for up to 5 years. Gastroenterology 131:6 (2006), 1743–1751.
44. 44 Marcellin, P., Chang, T.T., Lim, S.G., et al. Long-term efficacy and safety of adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. Hepatology 48:3 (2008), 750–758.
45. 45 Schiff, E., Simsek, H., Lee, W.M., et al. Efficacy and safety of entecavir in patients with chronic hepatitis B and advanced hepatic fibrosis or cirrhosis. Am J Gastroenterol 103:11 (2008), 2776–2783.
46. 46 Yokosuka, O., Takaguchi, K., Fujioka, S., et al. Long-term use of entecavir in nucleoside-naive Japanese patients with chronic hepatitis B infection. J Hepatol 52:6 (2010), 791–799.
47. 47 Rockey, D.C., Caldwell, S.H., Goodman, Z.D., et al. Liver biopsy. Hepatology 49:3 (2009), 1017–1044.
48. 48 Rockey, D.C., Bissell, D.M., Noninvasive measures of liver fibrosis. Hepatology 43:2 Suppl 1 (2006), S113–S120.
49. 49 Barry-Hamilton, V., Spangler, R., Marshall, D., et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 16:9 (2010), 1009–1017.
50. 50 Fontana, R.J., Hann, H.W., Perrillo, R.P., et al. Determinants of early mortality in patients with decompensated chronic hepatitis B treated with antiviral therapy. Gastroenterology 123:3 (2002), 719–727.
51. 51 Schiff, E.R., Lai, C.L., Hadziyannis, S., et al. Adefovir dipivoxil therapy for lamivudine-resistant hepatitis B in pre- and post-liver transplantation patients. Hepatology 38:6 (2003), 1419–1427.
52. 52 Shim, J.H., Lee, H.C., Kim, K.M., et al. Efficacy of entecavir in treatment-naive patients with hepatitis B virus-related decompensated cirrhosis. J Hepatol 52:2 (2010), 176–182.
53. 53 Liaw, Y.F., Raptopoulou-Gigi, M., Cheinquer, H., et al. Efficacy and safety of entecavir versus adefovir in chronic hepatitis B patients with hepatic decompensation: a randomized, open-label study. Hepatology 54:1 (2011), 91–100.
54. 54 Liaw, Y.F., Sheen, I.S., Lee, C.M., et al. Tenofovir disoproxil fumarate (TDF), emtricitabine/TDF, and entecavir in patients with decompensated chronic hepatitis B liver disease. Hepatology 53:1 (2011), 62–72.
55. 55 Chan, H.L., Chen, Y.C., Gane, E.J., et al. Randomized clinical trial: efficacy and safety of telbivudine and lamivudine in treatment-naive patients with HBV-related decompensated cirrhosis. J Viral Hepat 19:10 (2012), 732–743.
56. 56 Zoutendijk, R., Reijnders, J.G., Zoulim, F., et al. Virological response to entecavir is associated with a better clinical outcome in chronic hepatitis B patients with cirrhosis. Gut 62:5 (2013), 760–765.
57. 57 Kim, W.R., Terrault, N.A., Pedersen, R.A., et al. Trends in waiting list registration for liver transplantation for viral hepatitis in the United States. Gastroenterology 137:5 (2009), 1680–1686.
58. 58 Matsumoto, A., Tanaka, E., Rokuhara, A., et al. Efficacy of lamivudine for preventing hepatocellular carcinoma in chronic hepatitis B: a multicenter retrospective study of 2795 patients. Hepatol Res 32:3 (2005), 173–184.
59. 59 Miyake, Y., Kobashi, H., Yamamoto, K., Meta-analysis: the effect of interferon on development of hepatocellular carcinoma in patients with chronic hepatitis B virus infection. J Gastroenterol 44:5 (2009), 470–475.
60. 60 Papatheodoridis, G.V., Lampertico, P., Manolakopoulos, S., et al. Incidence of hepatocellular carcinoma in chronic hepatitis B patients receiving nucleos(t)ide therapy: a systematic review. J Hepatol 53:2 (2010), 348–356.
61. 61 Papatheodoridis, G.V., Manolakopoulos, S., Touloumi, G., et al. Virological suppression does not prevent the development of hepatocellular carcinoma in HBeAg-negative chronic hepatitis B patients with cirrhosis receiving oral antiviral(s) starting with lamivudine monotherapy: results of the nationwide HEPNET. Greece cohort study. Gut 60:8 (2011), 1109–1116.
62. 62 Arends, P., Sonneveld, M.J., Zoutendijk, R., et al. Entecavir treatment does not eliminate the risk of hepatocellular carcinoma in chronic hepatitis B: limited role for risk scores in Caucasians. Gut 64:8 (2015), 1289–1295.