Clinical evidence for the regression of liver fibrosis

Journal of Hepatology

Volumn 56, Issue 5, 2012, Pages 1171-1180

  Ellis, Elizabeth L ^a   Mann, Derek A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; INTERFERON; METHOTREXATE; PEGINTERFERON ALPHA; PEGINTERFERON ALPHA2A PLUS RIBAVIRIN; PEGINTERFERON ALPHA2B PLUS RIBAVIRIN; RIBAVIRIN;

ANTIVIRAL THERAPY; CANCER RISK; HEMOCHROMATOSIS; HEPATITIS B; HEPATITIS C; HUMAN; LIFESTYLE MODIFICATION; LIVER BIOPSY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FIBROSIS; NONALCOHOLIC FATTY LIVER; PHLEBOTOMY; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; REMISSION; REVIEW; WILSON DISEASE;

EID: 84859590655     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2011.09.024     Document Type: Review

References (96)

1. Lazo M, Clark JM. The epidemiology of nonalcoholic fatty liver disease: a global perspective. Semin Liver Dis 2008;28:339-350.
2. Williams CD, Stengel J, Asike MI, Torres DM, Shaw J, Contreras M, et al. Prevalence of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis among a largely middle-aged population utilizing ultrasound and liver biopsy: a prospective study. Gastroenterology 2011;140:124-131.
3. Muddu AK, Guha IN, Elsharkawy AM, Mann DA. Resolving fibrosis in the diseased liver: translating the scientific promise to the clinic. Int J Biochem Cell Biol 2007;39:695-714. (Pubitemid 46366796)
4. Anthony PP, Ishak KG, Nayak NC. The morphology of cirrhosis: definition, nomenclature, and classification. Bull World Health Organ 1977;55:521-540. (Pubitemid 8222040)
5. Lok AS. Long-term management of patients with chronic hepatitis B virus infection. Hepat B Annu 2005;2:127-153.
6. Lok AS, Seeff LB, Morgan TR, di Bisceglie AM, Sterling RK, Curto TM, et al. Incidence of hepatocellular carcinoma and associated risk factors in hepatitis C-related advanced liver disease. Gastroenterology 2009;136:138-148.
7. Macías J, Berenguer J, Japón MA, Girón JA, Rivero A, López-Cortés LF, et al. Fast fibrosis progression between repeated liver biopsies in patients coinfected with human immunodeficiency virus/hepatitis C virus. Hepatology 2009;50:1056-1063.
8. Bonnard P, Lescure FX, Amiel C, Guiard-Schmid JB, Callard P, Gharakhanian S, et al. Documented rapid course of hepatic fibrosis between two biopsies in patients coinfected by HIV and HCV despite high CD4 cell count. J Viral Hepat 2007;14:806-811. (Pubitemid 47561586)
9. Bedossa P, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 2003;38:1449-1457. (Pubitemid 37466971)
10. Kim MY, Cho MY, Baik SK, Park HJ, Jeon HK, Im CK, et al. Histological subclassification of cirrhosis using the Laennec fibrosis scoring system correlates with clinical stage and grade of portal hypertension. J Hepatol 2011;55:1004-1009.
11. Nagula S, Jain D, Groszmann RJ, Garcia-Tsao G. Histological-hemodynamic correlation in cirrhosis - a histological classification of the severity of cirrhosis. J Hepatol 2006;44:111-117. (Pubitemid 41772524)
12. Garcia-Tsao G, Friedman S, Iredale J, Pinzani M. Now there are many (stages) where before there was one: in search of a pathophysiological classification of cirrhosis. Hepatology 2010;51:1445-1449.
13. Schiano TD, Azeem S, Bodian CA, Bodenheimer Jr HC, Merati S, Thung SN, et al. Importance of specimen size in accurate needle liver biopsy evaluation of patients with chronic hepatitis C. Clin Gastroenterol Hepatol 2005;3:930-935. (Pubitemid 41219298)
14. Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol 2002;97:2614-2618.
15. Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD. Liver biopsy. Hepatology 2009;49:1017-1044.
16. Talwalkar JA, Yin M, Fidler JL, Sanderson SO, Kamath PS, Ehman RL. Magnetic resonance imaging of hepatic fibrosis: emerging clinical applications. Hepatology 2008;47:332-342. (Pubitemid 351171070)
17. Friedrich-Rust M, Wunder K, Kriener S, Sotoudeh F, Richter S, Bojunga J, et al. Liver fibrosis in viral hepatitis: noninvasive assessment with acoustic radiation force impulse imaging versus transient elastography. Radiology 2009;252:595-604.
18. Friedrich-Rust M, Ong M, Martens S, Sarrazin C, Bojunga J, Zeuzem S, et al. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 2008;134 (960-974):e968.
19. Boursier J, Vergniol J, Sawadogo A, Dakka T, Michalak S, Gallois Y, et al. The combination of a blood test and Fibroscan improves the non-invasive diagnosis of liver fibrosis. Liver Int 2009;29:1507-1515.
20. Smith JO, Sterling RK. Systematic review: non-invasive methods of fibrosis analysis in chronic hepatitis C. Aliment Pharmacol Ther 2009;30:557-576.
21. Mayo MJ, Parkes J, Adams-Huet B, Combes B, Mills AS, Markin RS, et al. Prediction of clinical outcomes in primary biliary cirrhosis by serum enhanced liver fibrosis assay. Hepatology 2008;48:1549-1557.
22. Mehta SH, Lau B, Afdhal NH, Thomas DL. Exceeding the limits of liver histology markers. J Hepatol 2009;50:36-41.
23. Matthews JNS, Altman DG, Campbell MJ, Royston P. Analysis of serial measurements in medical research. Br Med J 1990;300:230-235. (Pubitemid 20045528)
24. Perez-Tamayo R. Cirrhosis of the liver: a reversible disease? Pathol Annu 1979;14 (Pt. 2):183-213.
25. Masuzaki R, Yoshida H, Omata M. Interferon reduces the risk of hepatocellular carcinoma in hepatitis C virus-related chronic hepatitis/liver cirrhosis. Oncology 2010;78:17-23.
26. Imai Y, Tamura S, Tanaka H, Hiramatsu N, Kiso S, Doi Y, et al. Reduced risk of hepatocellular carcinoma after interferon therapy in aged patients with chronic hepatitis C is limited to sustained virological responders. J Viral Hepat 2010;17:185-191.
27. Singal AG, Volk ML, Jensen D, Di Bisceglie AM, Schoenfeld PS. A Sustained viral response is associated with reduced liver-related morbidity and mortality in patients with hepatitis C virus. Clin Gastroenterol Hepatol 2010;8 (280-288):e281.
28. Singal AK, Singh A, Jaganmohan S, Guturu P, Mummadi R, Kuo Y, et al. Antiviral therapy reduces risk of hepatocellular carcinoma in patients with hepatitis C virus-related cirrhosis. Clin Gastroenterol Hepatol 2010;8:192-199.
29. Wanless IR, Nakashima E, Sherman M. Regression of human cirrhosis. Morphologic features and the genesis of incomplete septal cirrhosis. Arch Pathol Lab Med 2000;124:1599-1607.
30. Serpaggi J, Carnot F, Nalpas B, Canioni D, Guechot J, Lebray P, et al. Direct and indirect evidence for the reversibility of cirrhosis. Hum Pathol 2006;37:1519-1526. (Pubitemid 44792230)
31. Sobesky R, Mathurin P, Charlotte F, Moussalli J, Olivi M, Vidaud M, et al. Modeling the impact of interferon alfa treatment on liver fibrosis progression in chronic hepatitis C: a dynamic view. Gastroenterology 1999;116:378-386. (Pubitemid 29055361)
32. Ghany MG, Kleiner DE, Alter H, Doo E, Khokar F, Promrat K, et al. Progression of fibrosis in chronic hepatitis C. Gastroenterology 2003;124:97-104. (Pubitemid 36055343)
33. Poynard T, McHutchison J, Manns M, Trepo C, Lindsay K, Goodman Z, et al. Impact of pegylated interferon alfa-2b and ribavirin on liver fibrosis in patients with chronic hepatitis C. Gastroenterology 2002;122:1303-1313. (Pubitemid 34465173)
34. George SL, Bacon BR, Brunt EM, Mihindukulasuriya KL, Hoffmann J, Di Bisceglie AM. Clinical, virologic, histologic, and biochemical outcomes after successful HCV therapy: a 5-year follow-up of 150 patients. Hepatology 2009;49:729-738.
35. Veldt BJ, Heathcote EJ, Wedemeyer H, Reichen J, Hofmann WP, Zeuzem S, et al. Sustained virologic response and clinical outcomes in patients with chronic hepatitis C and advanced fibrosis. Ann Intern Med 2007;147:677-684. (Pubitemid 351664462)
36. Bruno S, Stroffolini T, Colombo M, Bollani S, Benvegnú L, Mazzella G, et al. Sustained virological response to interferon-α is with improved outcome in HCV-related cirrhosis: a retrospective study. Hepatology 2007;45:579-587. (Pubitemid 46453759)
37. Mallet V, Gilgenkrantz H, Serpaggi J, Verkarre V, Vallet-Pichard A, Fontaine H, et al. Brief communication: the relationship of regression of cirrhosis to outcome in chronic hepatitis C. Ann Intern Med 2008;149:399-403.
38. Bruno S, Crosignani A, Facciotto C, Rossi S, Roffi L, Redaelli A, et al. Sustained virologic response prevents the development of esophageal varices in compensated, child-pugh class A hepatitis C virus-induced cirrhosis. A 12- year prospective follow-up study. Hepatology 2010;51:2069-2076.
39. Roberts S, Gordon A, McLean C, Pedersen J, Bowden S, Thomson K, et al. Effect of sustained viral response on hepatic venous pressure gradient in hepatitis C-related cirrhosis. Clin Gastroenterol Hepatol 2007;5:932-937. (Pubitemid 47127019)
40. Shamliyan TA, Johnson JR, MacDonald R, Shaukat A, Yuan JM, Kane RL, et al. Systematic review of the literature on comparative effectiveness of antiviral treatments for chronic hepatitis B infection. J Gen Intern Med 2011;26:326-339.
41. Korenman J, Baker B, Waggoner J, Everhart JE, Di Bisceglie AM, Hoofnagle JH. Long-term remission of chronic hepatitis B after alpha-interferon therapy. Ann Intern Med 1991;114:629-634.
42. Niederau C, Heintges T, Lange S, Goldmann G, Niederau CM, Mohr L, et al. Long-term follow-up of HBeAg-positive patients treated with interferon alfa for chronic hepatitis B. N Engl J Med 1996;334:1422-1427. (Pubitemid 26157437)
43. Lin SM, Sheen IS, Chien RN, Chu CM, Liaw YF. Long-term beneficial effect of interferon therapy in patients with chronic hepatitis B virus infection. Hepatology 1999;29:971-975.
44. Lampertico P, Del Ninno E, Viganò M, Romeo R, Donato MF, Sablon E, et al. Long-term suppression of hepatitis B e antigen-negative chronic hepatitis B by 24-month interferon therapy. Hepatology 2003;37:756-763. (Pubitemid 36397385)
45. Papatheodoridis GV, Petraki K, Cholongitas E, Kanta E, Ketikoglou I, Manesis EK. Impact of interferon-alpha therapy on liver fibrosis progression in patients with HBeAg-negative chronic hepatitis B. J Viral Hepat 2005;12:199-206. (Pubitemid 40342179)
46. Wong GLH, Yiu KKL, Wong VWS, Tsoi KKF, Chan HLY. Meta-analysis: Reduction in hepatic events following interferon-alfa therapy of chronic hepatitis B. Aliment Pharmacol Ther 2010;32:1059-1068.
47. Chang TT, Liaw YF, Wu SS, Schiff E, Han KH, Lai CL, 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;52:886-893.
48. Dienstag JL, Goldin RD, Heathcote EJ, Hann HWL, Woessner M, Stephenson SL, et al. Histological outcome during long-term lamivudine therapy. Gastroenterology 2003;124:105-117. (Pubitemid 36055344)
49. Marcellin P, Chang TT, Lee Lim SG, Sievert W, Tong M, Arterburn S, et al. Long-term efficacy and safety of adefovir dipivoxil for the treatment of hepatitis B e antigen-positive chronic hepatitis B. Hepatology 2008;48:750-758.
50. Musso G, Gambino R, Cassader M, Pagano G. A meta-analysis of randomized trials for the treatment of nonalcoholic fatty liver disease. Hepatology 2010;52:79-104.
51. Promrat K, Kleiner DE, Niemeier HM, Jackvony E, Kearns M, Wands JR, et al. Randomized controlled trial testing the effects of weight loss on nonalcoholic steatohepatitis. Hepatology 2010;51:121-129.
52. Nobili V, Manco M, Devito R, Di Ciommo V, Comparcola D, Sartorelli MR, et al. Lifestyle intervention and antioxidant therapy in children with nonalcoholic fatty liver disease: a randomized, controlled trial. Hepatology 2008;48:119-128. (Pubitemid 351975537)
53. Harrison SA, Fecht W, Brunt EM, Neuschwander-Tetri BA. Orlistat for overweight subjects with nonalcoholic steatohepatitis: a randomized, prospective trial. Hepatology 2009;49:80-86.
54. Sanyal AJ, Chalasani N, Kowdley KV, McCullough A, Diehl AM, Bass NM, et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med 2010;362:1675-1685.
55. Malaguarnera M, Gargante MP, Russo C, Antic T, Vacante M, Malaguarnera M, et al. L-Carnitine supplementation to diet: a new tool in treatment of nonalcoholic steatohepatitisa randomized and controlled clinical trial. Am J Gastroenterol 2010;105:1338-1345.
56. Vilar Gomez E, Rodriguez De Miranda A, Gra Oramas B, Arus Soler E, Llanio Navarro R, Calzadilla Bertot L, et al. Clinical trial: a nutritional supplement Viusid, in combination with diet and exercise, in patients with nonalcoholic fatty liver disease. Aliment Pharmacol Therap 2009;30:999-1009.
57. Dixon JB, Bhathal PS, Hughes NR, O'Brien PE. Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology 2004;39:1647-1654. (Pubitemid 38702666)
58. Chavez-Tapia NC, Tellez-Avila FI, Barrientos-Gutierrez T, Mendez-Sanchez N, Lizardi-Cervera J, Uribe M. Bariatric surgery for non-alcoholic steatohepatitis in obese patients. Cochrane Database Syst Rev 2010;CD007340 [Online].
59. Fauerholdt L, Schlichting P, Christensen E. Conversion of micronodular cirrhosis into macronodular cirrhosis. Hepatology 1983;3:928-931. (Pubitemid 14247631)
60. Rambaldi A, Gluud C. Colchicine for alcoholic and non-alcoholic liver fibrosis and cirrhosis. Cochrane Database Syst Rev 2005; CD002148 [Online].
61. Powell Jr WJ, Klatskin G. Duration of survival in patients with Laennec's cirrhosis. Influence of alcohol withdrawal, and possible effects of recent changes in general management of the disease. Am J Med 1968;44:406-420.
62. Verrill C, Markham H, Templeton A, Carr NJ, Sheron N. Alcohol-related cirrhosis - early abstinence is a key factor in prognosis, even in the most severe cases. Addiction 2009;104:768-774.
63. Donato F, Tagger A, Gelatti U, Parrinello G, Boffetta P, Albertini A, et al. Alcohol and hepatocellular carcinoma: the effect of lifetime intake and hepatitis virus infections in men and women. Am J Epidemiol 2002;155:323-331. (Pubitemid 34132050)
64. Lee FI. Cirrhosis and hepatoma in alcoholics. Gut 1966;7:77-85.
65. Morgan TR, Mandayam S, Jamal MM. Alcohol and hepatocellular carcinoma. Gastroenterology 2004;127:S87-S96. (Pubitemid 39423374)
66. Vorobioff J, Groszmann RJ, Picabea E, Gamen M, Vlllavicencio R, Bordato J, et al. Prognostic value of hepatic venous pressure gradient measurements in alcoholic cirrhosis: a 10-year prospective study. Gastroenterology 1996;111:701-709. (Pubitemid 26293235)
67. Czaja AJ, Carpenter HA. Decreased fibrosis during corticosteroid therapy of autoimmune hepatitis. J Hepatol 2004;40:646-652. (Pubitemid 38367787)
68. Cotler SJ, Jakate S, Jensen DM. Resolution of cirrhosis in autoimmune hepatitis with corticosteroid therapy. J Clin Gastroenterol 2001;32:428-430. (Pubitemid 32378277)
69. Dufour JF, DeLellis R, Kaplan MM. Reversibility of hepatic fibrosis in autoimmune hepatitis. Ann Intern Med 1997;127:981-985. (Pubitemid 27516609)
70. Gong Y, Huang ZB, Christensen E, Gluud C. Ursodeoxycholic acid for primary biliary cirrhosis. Cochrane Database Syst Rev 2008;CD000551.
71. Gong Y, Gluud C. Methotrexate for primary biliary cirrhosis. Cochrane Database Syst Rev 2005;CD004385 [Online].
72. Hendrickse MT, Rigney E, Giaffer MH, Soomro I, Triger DR, Underwood JCE, et al. Low-dose methotrexate is ineffective in primary biliary cirrhosis: longterm results of a placebo-controlled trial. Gastroenterology 1999;117:400-407. (Pubitemid 29352949)
73. Kaplan MM, Cheng S, Price LL, Bonis PAL. A randomized controlled trial of colchicine plus ursodiol versus methotrexate plus ursodiol in primary biliary cirrhosis: ten-year results. Hepatology 2004;39:915-923. (Pubitemid 38428929)
74. Combes B, Emerson SS, Flye NL, Munoz SJ, Luketic VA, Mayo MJ, et al. Methotrexate (MTX) plus ursodeoxycholic acid (UDCA) in the treatment of primary biliary cirrhosis. Hepatology 2005;42:1184-1193. (Pubitemid 43112686)
75. Kaplan MM, DeLellis RA, Wolfe HJ. Sustained biochemical and histologic remission of primary biliary cirrhosis in response to medical treatment. Ann Intern Med 1997;126:682-688. (Pubitemid 27184038)
76. Kaplan MM, Bonder A, Ruthazer R, Bonis PAL. Methotrexate in patients with primary biliary cirrhosis who respond incompletely to treatment with ursodeoxycholic acid. Dig Dis Sci 2010;55:3207-3217.
77. Knauer CM, Gamble CN, Monroe LS. The reversal of hemochromatotic cirrhosis by multiple phlebotomies. Report of a case. Gastroenterology 1965;49:667-671.
78. Niederau C, Fischer R, Purschel A, Stremmel W, Haussinger D, Strohmeyer G. Long-term survival in patients with hereditary hemochromatosis. Gastroenterology 1996;110:1107-1119. (Pubitemid 26113751)
79. Deugnier YM, Guyader D, Crantock L, Lopez JM, Turlin B, Yaouanq J, et al. Primary liver cancer in genetic hemochromatosis: a clinical, pathological, and pathogenetic study of 54 cases. Gastroenterology 1993;104:228-234. (Pubitemid 23040027)
80. Loreal O, Deugnier Y, Moirand R, Lauvin L, Guyader D, Jouanolle H, et al. Liver fibrosis in genetic hemochromatosis. Respective roles of iron and non-iron-related factors in 127 homozygous patients. J Hepatol 1992;16:122-127. (Pubitemid 23013187)
81. Falize L, Guillygomarc'h A, Perrin M, Lainè F, Guyader D, Brissot P, et al. Reversibility of hepatic fibrosis in treated genetic hemochromatosis: a study of 36 cases. Hepatology 2006;44:472-477. (Pubitemid 44214887)
82. Frydman M. Genetic aspects of Wilson's disease. J Gastroenterol Hepatol 1990;5:483-490. (Pubitemid 20254152)
83. Cope-Yokoyama S, Finegold MJ, Sturniolo GC, Kim K, Mescoli C, Rugge M, et al. Wilson disease: histopathological correlations with treatment on follow-up liver biopsies. World J Gastroenterol 2010;16:1487-1494.
84. Marcellini M, Di Ciommo V, Callea F, Devito R, Comparcola D, Sartorelli MR, et al. Treatment of Wilson's disease with zinc from the time of diagnosis in pediatric patients: a single-hospital, 10-year follow-up study [Erratum appears in J Lab Clin Med Jul;146(1):44 Note: Carelli, Francesco [corrected to Carelli, Giovanni]]. J Lab Clin Med 2005;2005 (145):139-143.
85. Askari FK, Greenson J, Dick RD, Johnson VD, Brewer GJ. Treatment of Wilson's disease with zinc. XVIII: Initial treatment of the hepatic decompensation presentation with trientine and zinc. J Lab Clin Med 2003;142:385-390. (Pubitemid 38102022)
86. Linn FHH, Houwen RHJ, van Hattum J, van der Kleij S, van Erpecum KJ. Longterm exclusive zinc monotherapy in symptomatic Wilson disease: experience in 17 patients. Hepatology 2009;50:1442-1452.
87. Grand RJ, Vawter GF. Juvenile Wilson disease: histologic and functional studies during penicillamine therapy. J Pediatr 1975;87:1161-1170.
88. Sternlieb I, Feldmann G. Effects of anticopper therapy on hepatocellular mitochondria in patients with Wilson's disease: an ultrastructural and stereological study. Gastroenterology 1976;71:457-461.
89. Shiono Y, Wakusawa S, Hayashi H, Takikawa T, Yano M, Okada T, et al. Iron accumulation in the liver of male patients with Wilson's disease. Am J Gastroenterol 2001;96:3147-3151. (Pubitemid 33095355)
90. Falkmer S, Samuelson G, Sjolin S. Penicillamine-induced normalization of clinical signs, and liver morphology and histochemistry in a case of Wilson's disease. Pediatrics 1970;45:260-268.
91. Popov Y, Schuppan D. Targeting liver fibrosis: strategies for development and validation of anti-fibrotic therapies. Hepatology 2009;50:1294-1306.
92. Fallowfield JA, Iredale JP. Targeted treatments for cirrhosis. Expert Opin Ther Targets 2004;8:423-435. (Pubitemid 39359649)
93. Lotersztajn S, Julien B, Teixeira-Clerc F, Grenard P, Mallat A. Hepatic fibrosis: molecular mechanisms and drug targets. Ann Rev Pharmacol Toxicol 2005:605-628.
94. Sato Y, Murase K, Kato J, Kobune M, Sato T, Kawano Y, et al. Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone. Nat Biotechnol 2008;26:431-442. (Pubitemid 351501817)
95. Abu Dayyeh BK, Yang M, Dienstag JL, Chung RT. The effects of angiotensin blocking agents on the progression of liver fibrosis in the HALT-C Trial cohort. Dig Dis Sci 2011;56:564-568.
96. Friedman SL. Evolving challenges in hepatic fibrosis. Nat Rev Gastroenterol Hepatol 2010;7:425-436.