Nonresponse to Interferon-α Based Treatment for Chronic Hepatitis C Infection Is Associated with Increased Hazard of Cirrhosis

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Cozen, Myrna L ^a   Ryan, James C ^a   Shen, Hui ^a   Lerrigo, Robert ^a   Yee, Russell M ^b   Sheen, Edward ^c   Wu, Richard ^a   Monto, Alexander ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Columbia University ^*  (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; PEGINTERFERON ALPHA; RIBAVIRIN;

ADULT; AGED; ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG TREATMENT FAILURE; FEMALE; FOLLOW UP; HEPATITIS C; HUMAN; HUMAN TISSUE; LIVER BIOPSY; LIVER CIRRHOSIS; LIVER FIBROSIS; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PATIENT ATTITUDE; RETROSPECTIVE STUDY; RISK ASSESSMENT; RISK FACTOR; TREATMENT OUTCOME; COMPLICATION; DISEASE COURSE; HEPATITIS C, CHRONIC; MIDDLE AGED; RECURRENT DISEASE; REPRODUCIBILITY; SURVIVAL; TIME; TREATMENT FAILURE;

HEPATITIS C VIRUS;

AGED; DISEASE PROGRESSION; FEMALE; HEPATITIS C, CHRONIC; HUMANS; INTERFERON-ALPHA; LIVER CIRRHOSIS; MALE; MIDDLE AGED; RECURRENCE; REPRODUCIBILITY OF RESULTS; RETROSPECTIVE STUDIES; RISK FACTORS; SURVIVAL ANALYSIS; TIME FACTORS; TREATMENT FAILURE;

EID: 84876698826     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061568     Document Type: Article

References (55)

1. Armstrong GL, Wasley A, Simard EP, McQuillan GM, Kuhnert WL, et al. (2006) The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 144: 705-714.
2. Bialek SR, Terrault NA, (2006) The changing epidemiology and natural history of hepatitis C virus infection. Clin Liver Dis 10: 697-715.
3. Hoofnagle JH, Seeff LB, (2006) Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med. 355: 2444-2451.
4. McHutchison JG, Gordon SC, Schiff ER, Shiffman ML, Lee WM, et al. (1998) Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. Hepatitis Interventional Therapy Group. N Engl J Med 339: 1485-1492.
5. McHutchison JG, Manns M, Patel K, Poynard T, Lindsay KL, et al. (2002) Adherence to combination therapy enhances sustained response in genotype-1-infected patients with chronic hepatitis C. Gastroenterology. 123: 1061-1069.
6. Yee HS, Chang MF, Pocha C, Lim J, Ross D, et al. (2012) Update on the management and treatment of hepatitis C virus infection: recommendations from the Department of Veterans Affairs Hepatitis C Resource Center Program and the National Hepatitis C Program Office. Am J Gastroenterol 107: 669-689; quiz 690.
7. Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, et al. (2011) Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med 364: 2405-2416.
8. Pawlotsky JM, (2011) The results of Phase III clinical trials with telaprevir and boceprevir presented at the Liver Meeting 2010: a new standard of care for hepatitis C virus genotype 1 infection, but with issues still pending. Gastroenterology 140: 746-754.
9. Poordad F, McCone J, Bacon BR, Bruno S, Manns MP, et al. (2011) Boceprevir for untreated chronic HCV genotype 1 infection. N Engl J Med 364: 1195-1206.
10. Heathcote EJ, Shiffman ML, Cooksley WG, Dusheiko GM, Lee SS, et al. (2000) Peginterferon alfa-2a in patients with chronic hepatitis C and cirrhosis. N Engl J Med 343: 1673-1680.
11. Poynard T, McHutchison J, Manns M, Trepo C, Lindsay K, et al. (2002) Impact of pegylated interferon alfa-2b and ribavirin on liver fibrosis in patients with chronic hepatitis C. Gastroenterology. 122: 1303-1313.
12. Shiffman ML, Hofmann CM, Thompson EB, Ferreira-Gonzalez A, Contos MJ, et al. (1997) Relationship between biochemical, virological, and histological response during interferon treatment of chronic hepatitis C. Hepatology. 26: 780-785.
13. Mallat A, Preaux AM, Blazejewski S, Rosenbaum J, Dhumeaux D, et al. (1995) Interferon alfa and gamma inhibit proliferation and collagen synthesis of human Ito cells in culture. Hepatology 21: 1003-1010.
14. Goodman ZD, Stoddard AM, Bonkovsky HL, Fontana RJ, Ghany MG, et al. (2009) Fibrosis progression in chronic hepatitis C: morphometric image analysis in the HALT-C trial. Hepatology 50: 1738-1749.
15. Pockros PJ, Hamzeh FM, Martin P, Lentz E, Zhou X, et al. (2010) Histologic outcomes in hepatitis C-infected patients with varying degrees of virologic response to interferon-based treatments. Hepatology 52: 1193-1200.
16. Shiffman ML, Hofmann CM, Contos MJ, Luketic VA, Sanyal AJ, et al. (1999) A randomized, controlled trial of maintenance interferon therapy for patients with chronic hepatitis C virus and persistent viremia. Gastroenterology 117: 1164-1172.
17. Poynard T, McHutchison J, Davis GL, Esteban-Mur R, Goodman Z, et al. (2000) Impact of interferon alfa-2b and ribavirin on progression of liver fibrosis in patients with chronic hepatitis C. Hepatology. 32: 1131-1137.
18. Shiratori Y, Ito Y, Yokosuka O, Imazeki F, Nakata R, et al. (2005) Antiviral therapy for cirrhotic hepatitis C: association with reduced hepatocellular carcinoma development and improved survival. Ann Intern Med 142: 105-114.
19. Poynard T, Bruix J, Schiff ER, Diago M, Berg T, et al. (2012) Improved inflammatory activity with peginterferon alfa-2b maintenance therapy in non-cirrhotic prior non-responders: A randomized study. J Hepatol.
20. Dienstag JL, Ghany MG, Morgan TR, Di Bisceglie AM, Bonkovsky HL, et al. (2011) A prospective study of the rate of progression in compensated, histologically advanced chronic hepatitis C. Hepatology. 54: 396-405.
21. Bruce-Chwatt LJ, (1965) Declaration of Helsinki. Recommendations Guiding Doctors in Clinical Research. WHO Chron 19: 31-32.
22. Seeff LB, (2002) Natural history of chronic hepatitis C. Hepatology. 36: S35-46.
23. Harris DR, Gonin R, Alter HJ, Wright EC, Buskell ZJ, et al. (2001) The relationship of acute transfusion-associated hepatitis to the development of cirrhosis in the presence of alcohol abuse. Ann Intern Med 134: 120-124.
24. Batts KP, Ludwig J, (1995) Chronic hepatitis. An update on terminology and reporting. Am J Surg Pathol 19: 1409-1417.
25. Brunt EM, (2000) Grading and staging the histopathological lesions of chronic hepatitis: the Knodell histology activity index and beyond. Hepatology 31: 241-246.
26. Sofair AN, Barry V, Manos MM, Thomas A, Zaman A, et al. (2009) The epidemiology and clinical characteristics of patients with newly diagnosed alcohol-related liver disease: results from population-based surveillance. J Clin Gastroenterol 44: 301-307.
27. Bini EJ, Brau N, Currie S, Shen H, Anand BS, et al. (2005) Prospective multicenter study of eligibility for antiviral therapy among 4,084 U.S. veterans with chronic hepatitis C virus infection. Am J Gastroenterol 100: 1772-1779.
28. Ghany MG, Strader DB, Thomas DL, Seeff LB, (2009) Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 49: 1335-1374.
29. Allison PD (1995) Survival Analysis Using the SAS® System: A Practical Guide Cary, NC: SAS Institute Inc. 292 p.
30. Etzioni R, Pepe M, Longton G, Hu C, Goodman G, (1999) Incorporating the time dimension in receiver operating characteristic curves: a case study of prostate cancer. Med Decis Making 19: 242-251.
31. Luo Z, Gardiner JC, Bradley CJ, (2010) Applying propensity score methods in medical research: pitfalls and prospects. Med Care Res Rev 67: 528-554.
32. Shah BR, Laupacis A, Hux JE, Austin PC, (2005) Propensity score methods gave similar results to traditional regression modeling in observational studies: a systematic review. J Clin Epidemiol 58: 550-559.
33. Dominitz JA, Boyko EJ, Koepsell TD, Heagerty PJ, Maynard C, et al. (2005) Elevated prevalence of hepatitis C infection in users of United States veterans medical centers. Hepatology 41: 88-96.
34. Kayali Z, Tan S, Shinkunas L, Voigt M, LaBrecque DR, et al. (2007) Risk factors for hepatitis C fibrosis: a prospective study of United States veterans compared with nonveterans. J Viral Hepat 14: 11-21.
35. Conjeevaram HS, Fried MW, Jeffers LJ, Terrault NA, Wiley-Lucas TE, et al. (2006) Peginterferon and ribavirin treatment in African American and Caucasian American patients with hepatitis C genotype 1. Gastroenterology 131: 470-477.
36. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, et al. (2009) Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461: 399-401.
37. Terrault NA, Im K, Boylan R, Bacchetti P, Kleiner DE, et al. (2008) Fibrosis progression in African Americans and Caucasian Americans with chronic hepatitis C. Clin Gastroenterol Hepatol. 6: 1403-1411.
38. Butt AA, Wang X, Moore CG, (2009) Effect of hepatitis C virus and its treatment on survival. Hepatology 50: 387-392.
39. Coverdale SA, Khan MH, Byth K, Lin R, Weltman M, et al. (2004) Effects of interferon treatment response on liver complications of chronic hepatitis C: 9-year follow-up study. Am J Gastroenterol 99: 636-644.
40. Singal AG, Volk ML, Jensen D, Di Bisceglie AM, Schoenfeld PS (2010) A sustained viral response is associated with reduced liver-related morbidity and mortality in patients with hepatitis C virus. Clin Gastroenterol Hepatol 8: 280-288, 288 e281.
41. Thomas H, Foster G, Platis D, (2003) Mechanisms of action of interferon and nucleoside analogues. J Hepatol 39Suppl 1: S93-98.
42. Brinkmann V, Geiger T, Alkan S, Heusser CH, (1993) Interferon alpha increases the frequency of interferon gamma-producing human CD4+ T cells. J Exp Med 178: 1655-1663.
43. Tam RC, Pai B, Bard J, Lim C, Averett DR, et al. (1999) Ribavirin polarizes human T cell responses towards a Type 1 cytokine profile. J Hepatol 30: 376-382.
44. Kamal SM, Ismail A, Graham CS, He Q, Rasenack JW, et al. (2004) Pegylated interferon alpha therapy in acute hepatitis C: relation to hepatitis C virus-specific T cell response kinetics. Hepatology 39: 1721-1731.
45. Veldt BJ, Heathcote EJ, Wedemeyer H, Reichen J, Hofmann WP, et al. (2007) Sustained virologic response and clinical outcomes in patients with chronic hepatitis C and advanced fibrosis. Ann Intern Med 147: 677-684.
46. Koretz RL, Pleguezuelo M, Arvaniti V, Barrera Baena P, Ciria R, et al. (2013) Interferon for interferon nonresponding and relapsing patients with chronic hepatitis C. Cochrane Database Syst Rev Art. No.: CD003617. DOI: 10.1002/14651858.
47. Singal AG, Waljee AK, Shiffman M, Bacon BR, Schoenfeld PS, (2010) Meta-analysis: re-treatment of genotype I hepatitis C nonresponders and relapsers after failing interferon and ribavirin combination therapy. Aliment Pharmacol Ther 32: 969-983.
48. Poynard T, Bruix J, Schiff ER, Diago M, Berg T, et al. (2013) Improved inflammatory activity with peginterferon alfa-2b maintenance therapy in non-cirrhotic prior non-responders: A randomized study. J Hepatol 58: 452-459.
49. Dienstag JL, Ghany MG, Morgan TR, Di Bisceglie AM, Bonkovsky HL, et al. (2011) A prospective study of the rate of progression in compensated, histologically advanced chronic hepatitis C. Hepatology. 54: 396-405.
50. Di Bisceglie AM, Stoddard AM, Dienstag JL, Shiffman ML, Seeff LB, et al. (2011) Excess mortality in patients with advanced chronic hepatitis C treated with long-term peginterferon. Hepatology 53: 1100-1108.
51. Shiratori Y, Imazeki F, Moriyama M, Yano M, Arakawa Y, et al. (2000) Histologic improvement of fibrosis in patients with hepatitis C who have sustained response to interferon therapy. Ann Intern Med 132: 517-524.
52. Yoshida H, Arakawa Y, Sata M, Nishiguchi S, Yano M, et al. (2002) Interferon therapy prolonged life expectancy among chronic hepatitis C patients. Gastroenterology 123: 483-491.
53. Bosco JL, Silliman RA, Thwin SS, Geiger AM, Buist DS, et al. (2010) A most stubborn bias: no adjustment method fully resolves confounding by indication in observational studies. J Clin Epidemiol 63: 64-74.
54. Stukel TA, Fisher ES, Wennberg DE, Alter DA, Gottlieb DJ, et al. (2007) Analysis of observational studies in the presence of treatment selection bias: effects of invasive cardiac management on AMI survival using propensity score and instrumental variable methods. JAMA 297: 278-285.
55. Suppiah V, Gaudieri S, Armstrong NJ, O'Connor KS, Berg T, et al. (2011) IL28B, HLA-C, and KIR variants additively predict response to therapy in chronic hepatitis C virus infection in a European Cohort: a cross-sectional study. PLoS Med 8: e1001092.