Persistence of hepatitis C virus during and after otherwise clinically successful treatment of chronic hepatitis C with standard pegylated interferon α-2b and ribavirin therapy

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Chen, Annie Y ^a   Zeremski, Marija ^b   Chauhan, Ranjit ^a   Jacobson, Ira M ^b   Talal, Andrew H ^b,c   Michalak, Tomasz I ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRAL AGENTS; FEMALE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; INTERFERON-ALPHA; LIMIT OF DETECTION; MALE; POLYETHYLENE GLYCOLS; RECOMBINANT PROTEINS; RIBAVIRIN; RNA, VIRAL; VIRUS REPLICATION;

EID: 84894284109     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080078     Document Type: Article

References (44)

1. Lavanchy D (2009) The global burden of hepatitis C. Liver Intl 29(suppl): 74-81.
2. Seeff LB (2002) Natural history of chronic hepatitis C. Hepatology 36: S35-S46.
3. Feinstone SM, Alter HJ, Dienes HP, Shimizu Y, Popper H, et al. (1981) Non-A, non-B hepatitis in chimpanzees and marmosets. J Infect Dis 144: 588-598.
4. Katayama K, Kumagai J, Komiya Y, Mizui M, Yugi H, et al. (2004) Titration of hepatitis C virus in chimpanzees for determining the copy number required for transmission. Intervirology 47: 57-64.
5. MacParland SA, Pham TNQ, Guy CS, Michalak TI (2009) Hepatitis C virus persisting after clinically apparent sustained virological response to antiviral therapy retains infectivity in vitro. Hepatology 49: 1431-1441.
6. Pham TNQ, MacParland SA, Mulrooney PM, Cooksley H, Naoumov NV, et al (2004) Hepatitis C virus persistence after spontaneous or treatment-induced resolution of hepatitis C. J Virol 78: 5867-5874.
7. Pham TNQ, Coffin CS, Michalak TI (2010) Occult hepatitis C virus infection: what does it mean? Liver Intl 30: 502-511.
8. Radkowski M, Gallegos-Orozco JF, Jablonska J, Colby TV, Walewska-Zielecka B, et al. (2005) Persistence of hepatitis C virus in patients successfully treated for chronic hepatitis C. Hepatology 41: 106-114.
9. Castillo I, Rodriguez-Inigo E, Lopez-Alcorocho JM, Pardo M, Bartolome J, et al. (2006) Hepatitis C virus replicates in the liver of patients who have a sustained response to antiviral treatment. Clin Infect Dis 43: 1277-1283.
10. Hoare M, Gelson WTH, Rushbrook SM, Curran MD, Woodall T, et al. (2008) Histological changes in HCV antibody-positive, HCV RNA-negative subjects suggest persistent virus infection. Hepatology 48: 1737-1745.
11. Pham TNQ, Coffin CS, Churchill ND, Urbanski SJ, Lee SS, et al. (2012) Hepatitis C virus persistence after sustained virological response to antiviral therapy in patients with or without past exposure to hepatitis B virus. J Viral Hepat 19: 103-111.
12. Makiyama A, Itoh Y, Kasahara A, Imai Y, Kawata S, et al. (2004) Characteristics of patients with chronic hepatitis C who developed hepatocellular carcinoma after a sustained response to interferon therapy. Cancer 101: 1616-1622.
13. Kobayashi S, Takeda T, Enomoto M, Tamori A, Kawada N, et al. (2007) Development of hepatocellular carcinoma in patients with chronic hepatitis C who had a sustained virological response to interferon therapy: a multicenter, retrospective cohort study of 1224 patients. Liver Intl 27: 186-191.
14. Scherzer T-M, Reddy KR, Wrba F, Hofer H, Staufer K, et al. (2008) Hepatocellular carcinoma in long-term sustained virological responders following combinantion tharapy for chronic hepatitis C. J Viral Hepat 15: 659-665.
15. Sewell JL, Stick K, Monto A (2009) Hepatocellular carcinoma after sustained virologic response in hepatitis C patients without cirrhosis on a pre-treatment liver biopsy. Eur J Gastroenterol 21: 225-229.
16. Morgan TR, Ghany MG, Kim H-Y, Snow KK, Shiffman ML, et al. (2010) Outcome of sustained virological responders with histologically advanced chronic hepatitis C. Hepatology 52: 833-844.
17. van der Meer A, Veldt BJ, Field JJ, Wedemeyer H, Dufour J-F, et al. (2012) Association between sustained virological response and all-cause mortality among patients with chronic hepatitis C and advanced hepatic fibrosis. JAMA 308: 2584-2595.
18. Pham TNQ, MacParland SA, Coffin CS, Lee SS, Bursey FR, et al. (2005) Mitogen-induced upregulation of hepatitis C virus expression in human lymphoid cells. J Gen Virol 86: 657-666.
19. Bartolome J, Lopez-Alcorocho JM, Castillo I, Rodriguez-Inigo E, Quiroga JA, et al. (2007) Ultracentrifugation of serum samples allows detection of hepatitis C virus RNA in patients with occult hepatitis C. J Virol 81: 7710-7715.
20. Pham TNQ, King D, MacParland SA, McGrath JS, Reddy SB, et al. (2008) Hepatitis C virus replicates in the same immune cell subsets in chronic hepatitis C and occult infection. Gastroenterology 134: 812-822.
21. Quiroga JA, Llorente S, Castillo I, Rodriguez-Inigo E, Lopez-Alcorocho JM, et al. (2006) Virus-specific T-cell responses associated with hepatitis C virus (HCV) persistence in the liver after apparent recovery from HCV infection. J Med Virol 78: 1190-1197.
22. Pham TNQ, Mulrooney-Cousins PM, Mercer SE, MacParland SA, Inglot M, et al. (2007) Antagonistic expression of hepatitis C virus and alpha interferon in lymphoid cells during persistent occult infection. J Viral Hepat 14: 537-548.
23. Pham TNQ, Mercer SE, Michalak TI (2009) Chronic hepatitis C and persistent occult hepatitis C virus infection are characterized by distinct immune cell cytokine expression profiles. J Viral Hepat 16: 547-556.
24. Michalak TI, Pasquinelli C, Guilhot S, Chisari FV (1994) Hepatitis B virus persistence after recovery from acute viral hepatitis. J Clin Invest 93: 230-239.
25. Michalak TI, Pardoe IU, Coffin CS, Churchill ND, Freake DS, et al. (1999) Occult life-long persistence of infectious hepadnavirus and residual liver inflammation in woodchucks convalescent from acute viral hepatitis. Hepatology 29: 928-938.
26. Sarhan MA, Pham TNQ, Chen AY, Michalak TI (2012) Hepatitis C virus infection of human T lymphocytes is mediated by CD5. J Virol 86: 3723-3735.
27. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) Molecular evolutionary genetics analysis using maximum likelihood, evolution distance, and maximum parsimony methods. Molec Biol Evol 28: 2731-2739.
28. Navas S, Martin J, Quiroga JA, Castillo I, Carreno V (1998) Genetic diversity and tissue compartmentalization of the hepatitis C virus genome in blood mononuclear cells, liver and serum from chronic hepatitis C patients. J Virol 72: 1640-1646.
29. Ducoulombier D, Roque-Afonso A-M, Di Liberto G, Penin F, Kara R, et al. (2004) Frequent compartmentalization of hepatitis C virus variants in circulating B cells and monocytes. Hepatology 39: 817-825.
30. Pal S, Sullivan DG, Kim S, Lai KK, Kae J, et al. (2006) Productive replication of hepatitis C virus in perihepatic lymph nodes in vivo: implications of HCV lymphotropism. Gastroenterology 130: 1107-1116.
31. MacParland SA, Pham TNQ, Gujar SA, Michalak TI (2006) De novo infection and propagation of wild-type hepatitis C virus in human T lymphocytes in vitro. J Gen Virol 87: 3577-3586.
32. Michalak TI, Pham TNQ, Mulrooney-Cousins PM (2007) Molecular diagnosis of occult HCV and HBV infections. Future Virol 2: 451-465.
33. Fishman SL, Murray JM, Eng FJ, Walewski JL, Morgello S, et al. (2008) Molecular and bioinformatic evidence of hepatitis C virus evolution in brain. J Inf Dis 197: 597-607.
34. Ghany MG, Nelson DR, Strader DB, Thomas DL, Seeff L (2011) An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 54: 1433-1444.
35. Di Liberto G, Roque-Afonso AM, Kara R, Ducoulombier D, Fallo G, et al. (2006) Clinical and therapeutic implications of hepatitis C virus compartmentalization. Gastroenterology 131: 76-84.
36. Camma C, Giunta M, Pinzello G, Pinzello G, Morabito A, et al. (1999) Chronic hepatitis C and interferon alpha: conventional and cumulative meta-analyses of randomized controlled trials. Am J Gastroenterol 94: 581-595.
37. George SL, Bacon BR, Brunt EM, Mihindukulasuriya KL, Hoffmann J, et al. (2009) Clinical, virologic, histologic, and biochemical outcomes after successful HCV therapy: a 5-year follow-up of 150 patients. Hepatology 49: 729-738.
38. Manns MP, Pockros PJ, Norkrans G, Smith CI, Morgan TR, et al. (2013) Longterm clearance of hepatitis C virus following interferon a-2b, alone or in combination with ribavirin. J Viral Hepat doi:10.1111/jvh.12074 (in press).
39. Lee WM, Polson JE, Carney DS, Sahin B, Gale M Jr (2005) Reemergence of hepatitis C virus after 8.5 years in a patient with hypogammaglobulinemia: evidence for an occult viral reservoir. J Infect Dis 192: 1088-1092.
40. Nudo CG, Cortes RA, Weppler D, Schiff ER, Tzakis AG, et al. (2008) Effect of pretransplant hepatitis C virus RNA status on posttransplant outcome. Transplant Proc 40: 1449-1455.
41. Lin A, Thadareddy A, Goldstein MJ, Lake-Bakaar G (2008) Immune suppression leading to hepatitis C virus re-emergence after sustained virological response. J Med Virol 80: 1720-1722.
42. Torres HA, Davila M (2012) Reactivation of hepatitis B virus and hepatitis C virus in patients with cancer. Nat Rev Clin Oncol 9: 156-166.
43. Raimondo G, Caccamo G, Filomia R, Pollicino T (2013) Occult HBV infection. Semin Immunopathol 35: 39-52.
44. Lin K, Perni EB, Kwong AD, Lin C (2006) VX-950, a novel hepatitis C virus (HCV) NS3-4A protease inhibitor, exhibits potent antiviral activities in HCV replicon cells. Antimicrob Agents Chemother 50: 1813-1822.