Effects of ribavirin monotherapy on the viral population in patients with chronic hepatitis C genotype 1: Direct sequencing and pyrosequencing of the HCV regions

Journal of Medical Virology

Volumn 86, Issue 11, 2014, Pages 1886-1897

  Quiles Perez R ^a,b   Muñoz de Rueda, Paloma ^a,b   Martin Lagos Maldonado A ^a   Martin Alvarez A ^a   Quer, J ^b,c   Salmeron, J ^a,b  

^a HOSPITAL UNIVERSITARIO SAN CECILIO   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Anaemia; Chronic hepatitis C; Mutagenesis; RBV plasma; Viral kinetics

Indexed keywords

ALANINE AMINOTRANSFERASE; HEMOGLOBIN; NONSTRUCTURAL PROTEIN 5A; NONSTRUCTURAL PROTEIN 5B; PEGINTERFERON ALPHA2A; RIBAVIRIN; VIRUS RNA; ALPHA INTERFERON; ANTIVIRUS AGENT; MACROGOL DERIVATIVE; NS-5 PROTEIN, HEPATITIS C VIRUS; RECOMBINANT PROTEIN; VIRUS PROTEIN;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; AMPLICON; ANEMIA; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; DEPRESSION; DIRECT SEQUENCING; DRUG WITHDRAWAL; FATIGUE; FEMALE; GENE MUTATION; GENETIC DISTANCE; GENETIC VARIABILITY; HAPLOTYPE; HEMOGLOBIN BLOOD LEVEL; HEPATITIS C; HEPATITIS C VIRUS GENOTYPE 1; HUMAN; INSOMNIA; MALE; MEDICATION COMPLIANCE; MIDDLE AGED; MINIMUM PLASMA CONCENTRATION; MUTAGENIC ACTIVITY; MUTATION RATE; PILOT STUDY; PROSPECTIVE STUDY; PRURITUS; PYROSEQUENCING; STEADY STATE; TREATMENT RESPONSE; VIROLOGICAL RESPONSE; VIRUS LOAD; CLASSIFICATION; DNA SEQUENCE; GENETICS; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; ISOLATION AND PURIFICATION; POINT MUTATION; TREATMENT OUTCOME; VIROLOGY;

ADULT; ANTIVIRAL AGENTS; FEMALE; GENETIC VARIATION; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; INTERFERON-ALPHA; MALE; MIDDLE AGED; PILOT PROJECTS; POINT MUTATION; POLYETHYLENE GLYCOLS; RECOMBINANT PROTEINS; RIBAVIRIN; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; TREATMENT OUTCOME; VIRAL LOAD; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84908174040     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.24035     Document Type: Article

References (58)

1. Akuta N, Suzuki F, Sezaki H, Suzuki Y, Hosaka T, Someya T, Kobayashi M, Saitoh S, Watahiki S, Sato J, Matsuda M, Kobayashi M, Arase Y, Ikeda K, Kumada H. 2005. Association of amino acid substitution pattern in core protein of hepatitis C virus genotype 1b high viral load and non-virological response to interferon-ribavirin combination therapy. Intervirology 48:372-380.
2. Anderson JP, Daifuku R, Loeb LA. 2004. Viral error catastrophe by mutagenic nucleosides. Annu Rev Microbiol 58:183-205.
3. Asahina Y, Izumi N, Enomoto N, Uchihara M, Kurosaki M, Onuki Y, Nishimura Y, Ueda K, Tsuchiya K, Nakanishi H, Kitamura T, Miyake S. 2005. Mutagenic effects of ribavirin and response to interferon/ribavirin combination therapy in chronic hepatitis C. J Hepatol 43:623-629.
4. Bodenheimer HC Jr, Lindsay KL, Davis GL, Lewis JH, Thung SN, SeeffLB. 1997. Tolerance and efficacy of oral ribavirin treatment of chronic hepatitis C: A multicenter trial. Hepatology 26:473-477.
5. Brillanti S, Buonfiglioli F, Feletti V, Laterza L, Roda E. 2009. Ribavirin priming enhances efficacy of chronic hepatitis C retreatment in patients who had not responded to previous combination therapy. Hepatology 50:32.
6. Brillanti S, Mazzella G, Roda E. 2011. Ribavirin for chronic hepatitis C: And the mystery goes on. Dig Liver Dis 43:425-430.
7. Brochot E, Duverlie G, Castelain S, Morel V, Wychowski C, Dubuisson J, Francois C. 2007. Effect of ribavirin on the hepatitis C virus (JFH-1) and its correlation with interferon sensitivity. Antivir Ther 12:805-813.
8. Brok J, Gluud LL, Gluud C. 2006. Ribavirin monotherapy for chronic hepatitis C infection: A Cochrane Hepato-Biliary Group systematic review and meta-analysis of randomized trials. Am J Gastroenterol 101:842-847.
9. Bull JJ, Sanjuan R, Wilke CO. 2007. Theory of lethal mutagenesis for viruses. J Virol 81:2930-2939.
10. Caballero T, Perez-Milena A, Masseroli M, O'Valle F, Salmeron FJ, Del Moral RM, Sanchez-Salgado G. 2001. Liver fibrosis assessment with semiquantitative indexes and image analysis quantification in sustained-responder and non-responder interferontreated patients with chronic hepatitis C. J Hepatol 34:740-747.
11. Caraballo Cortes K, Zagordi O, Laskus T, Ploski R, Bukowska-Osko I, Pawelczyk A, Berak H, Radkowski M. 2013. Ultradeep pyrosequencing of hepatitis C virus hypervariable region 1 in quasispecies analysis. Biomed Res Int 2013:626083.
12. Contreras AM, Hiasa Y, He W, Terella A, Schmidt EV, Chung RT. 2002. Viral RNA mutations are region specific and increased by ribavirin in a full-length hepatitis C virus replication system. J Virol 76:8505-8517.
13. Crotty S, Cameron CE, Andino R. 2001. RNA virus error catastrophe: direct molecular test by using ribavirin. P Natl Acad Sci USA 98:6895-6900.
14. Cuevas JM, Gonzalez-Candelas F, Moya A, Sanjuan R. 2009. Effect of ribavirin on the mutation rate and spectrum of hepatitis C virus in vivo. J Virol 83:5760-5764.
15. Chevaliez S, Brillet R, Lazaro E, Hezode C, Pawlotsky JM. 2007. Analysis of ribavirin mutagenicity in human hepatitis C virus infection. J Virol 81:7732-7741.
16. Chung RT, Gale M Jr, Polyak SJ, Lemon SM, Liang TJ, Hoofnagle JH. 2008. Mechanisms of action of interferon and ribavirin in chronic hepatitis C: Summary of a workshop. Hepatology 47:306-320.
17. Di Bisceglie AM, Conjeevaram HS, Fried MW, Sallie R, Park Y, Yurdaydin C, Swain M, Kleiner DE, Mahaney K, Hoofnagle JH. 1995. Ribavirin as therapy for chronic hepatitis C. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 123:897-903.
18. Dietz J, Schelhorn SE, Fitting D, Mihm U, Susser S, Welker MW, Fuller C, Daumer M, Teuber G, Wedemeyer H, Berg T, Lengauer T, Zeuzem S, Herrmann E, Sarrazin C. 2013. Deep sequencing reveals mutagenic effects of ribavirin during monotherapy of HCV genotype 1-infected patients. J Virol 87: 6172-6181.
19. Feld JJ, Lutchman GA, Heller T, Hara K, Pfeiffer JK, LeffRD, Meek C, Rivera M, Ko M, Koh C, Rotman Y, Ghany MG, Haynes-Williams V, Neumann AU, Liang TJ, Hoofnagle JH. 2010. Ribavirin improves early responses to peginterferon through improved interferon signaling. Gastroenterology 139:154-162.
20. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Goncales FL Jr, Haussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J. 2002. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 347:975-982.
21. Furusyo N, Kubo N, Toyoda K, Takeoka H, Nabeshima S, Murata M, Nakamuta M, Hayashi J. 2005. Helper T cell cytokine response to ribavirin priming before combined treatment with interferon alpha and ribavirin for patients with chronic hepatitis C. Antiviral Res 67:46-54.
22. Herrmann E, Lee JH, Marinos G, Modi M, Zeuzem S. 2003. Effect of ribavirin on hepatitis C viral kinetics in patients treated with pegylated interferon. Hepatology 37:1351-1358.
23. Hezode C, Forestier N, Dusheiko G, Ferenci P, Pol S, Goeser T, Bronowicki JP, Bourliere M, Gharakhanian S, Bengtsson L, McNair L, George S, Kieffer T, Kwong A, Kauffman RS, Alam J, Pawlotsky JM, Zeuzem S. 2009. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med 360:1839-1850.
24. Hofmann WP, Polta A, Herrmann E, Mihm U, Kronenberger B, Sonntag T, Lohmann V, Schonberger B, Zeuzem S, Sarrazin C. 2007. Mutagenic effect of ribavirin on hepatitis C nonstructural 5B quasispecies in vitro and during antiviral therapy. Gastroenterology 132:921-930.
25. Hofmann WP, Herrmann E, Sarrazin C, Zeuzem S. 2008. Ribavirin mode of action in chronic hepatitis C: From clinical use back to molecular mechanisms. Liver Int 28:1332-1343.
26. Inoue Y, Hiramatsu N, Oze T, Yakushijin T, Mochizuki K, Fukuda K, Mita E, Haruna Y, Inoue A, Imai Y, Hosui A, Miyagi T, Yoshida Y, Tatsumi T, Kiso S, Kanto T, Kasahara A, Takehara T, Hayashi N. 2011. Amino acid substitution in the core protein has no impact on relapse in hepatitis C genotype 1 patients treated with peginterferon and ribavirin. J Med Virol 83: 419-427.
27. Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, Bzowej NH, Marcellin P, Muir AJ, Ferenci P, Flisiak R, George J, Rizzetto M, Shouval D, Sola R, Terg RA, Yoshida EM, Adda N, Bengtsson L, Sankoh AJ, Kieffer TL, George S, Kauffman RS, Zeuzem S. 2011. Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med 364:2405-2416.
28. Kau A, Vermehren J, Sarrazin C. 2008. Treatment predictors of a sustained virological response in hepatitis B and C. J Hepatol 49:634-651.
29. Kumthip K, Pantip C, Chusri P, Thongsawat S, O'Brien A, Nelson KE, Maneekarn N. 2011. Correlation between mutations in the core and NS5A genes of hepatitis C virus genotypes 1a, 1b, 3a, 3b, 6f and the response to pegylated interferon and ribavirin combination therapy. J Viral Hepat 18:e117-125.
30. Lanford RE, Chavez D, Guerra B, Lau JY, Hong Z, Brasky KM, Beames B. 2001. Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J Virol 75:8074-8081.
31. Larrat S, Stanke-Labesque F, Plages A, Zarski JP, Bessard G, Souvignet C. 2003. Ribavirin quantification in combination treatment of chronic hepatitis C. Antimicrob Agents Ch 47:124-129.
32. Lionetti R, Tisone G, Palmieri G, Almerighi C, Anselmo A, Tariciotti L, Lenci I, De Luca L, Monaco A, Angelico M. 2010. Maintenance ribavirin monotherapy delays fibrosis progression in liver transplant recipients with recurrent hepatitis C at high risk of progression. Digest Liver Dis 42:297-303.
33. Loustaud-Ratti V, Alain S, Rousseau A, Hubert IF, Sauvage FL, Marquet P, Denis F, Lunel F, Cales P, Lefebvre A, Fauchais AL, Liozon E, Vidal E. 2008. Ribavirin exposure after the first dose is predictive of sustained virological response in chronic hepatitis C. Hepatology 47:1453-1461.
34. Lutchman G, Danehower S, Song BC, Liang TJ, Hoofnagle JH, Thomson M, Ghany MG. 2007. Mutation rate of the hepatitis C virus NS5B in patients undergoing treatment with ribavirin monotherapy. Gastroenterology 132:1757-1766.
35. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, Goodman ZD, Koury K, Ling M, Albrecht JK. 2001. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: A randomised trial. Lancet 358:958-965.
36. McHutchison JG, Gordon SC, SchiffER, Shiffman ML, Lee WM, Rustgi VK, Goodman ZD, Ling MH, Cort S, Albrecht JK. 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.
37. Merli M, Giannelli V, Gentili F, Giusto M, Simmaco M, Lionetto L, Corradini SG, Biliotti E, Attili AF, Rossi M, Taliani G. 2011. Ribavirin priming improves the virological response to antiviral treatment in transplanted patients with recurrent hepatitis C: a pilot study. Antivir Ther 16:879-885.
38. Mihm U, Welker MW, Teuber G, Wedemeyer H, Berg T, Sarrazin C, Bohm S, Alshuth U, Herrmann E, Zeuzem S. 2014. Impact of ribavirin priming on viral kinetics and treatment response in chronic hepatitis C genotype 1 infection. J Viral Hepat 21:42-52.
39. Munoz de Rueda P, Casado J, Paton R, Quintero D, Palacios A, Gila A, Quiles R, Leon J, Ruiz-Extremera A, Salmeron J. 2008. Mutations in E2-PePHD, NS5A-PKRBD, NS5A-ISDR, and NS5A-V3 of hepatitis C virus genotype 1 and their relationships to pegylated interferon-ribavirin treatment responses. J Virol 82:6644-6653.
40. Munoz-de-Rueda P, Ruiz-Extremera A, Candel JM, Quiles R, Martin AB, Diago M, Andrade R, Navarro JM, Gila A, Leon J, Carazo A, Quintero D, Salmeron J. 2012. Plasma ribavirin trough concentrations during treatment of chronic hepatitis C in genotype-1 patients. J Clin Gastroenterol 46:328-333.
41. Murayama M, Katano Y, Nakano I, Ishigami M, Hayashi K, Honda T, Hirooka Y, Itoh A, Goto H. 2007. A mutation in the interferon sensitivity-determining region is associated with responsiveness to interferon-ribavirin combination therapy in chronic hepatitis patients infected with a Japan-specific subtype of hepatitis C virus genotype 1B. J Med Virol 79:35-40.
42. Nasu A, Marusawa H, Ueda Y, Nishijima N, Takahashi K, Osaki Y, Yamashita Y, Inokuma T, Tamada T, Fujiwara T, Sato F, Shimizu K, Chiba T. 2011. Genetic heterogeneity of hepatitis C virus in association with antiviral therapy determined by ultradeep sequencing. PLoS One 6:e24907.
43. Ogawa K, Hige S, Nakanishi M, Yamamoto Y, Chuma M, Nagasaka A, Asaka M. 2009. Immunological and mutagenic actions of ribavirin monotherapy preceding combination therapy with interferon for patients with chronic hepatitis C. Antivir Ther 14:513-522.
44. Palmer M, Rubin R, Rustgi V. 2012. Randomised clinical trial: predosing with taribavirin before starting pegylated interferon vs. standard combination regimen in treatment-naive patients with chronic hepatitis C genotype 1. Aliment Pharm Therap 36:370-378.
45. Pfeiffer JK, Kirkegaard K. 2003. A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity. P Natl Acad Sci USA 100:7289-7294.
46. Poordad F, McCone J Jr, Bacon BR, Bruno S, Manns MP, Sulkowski MS, Jacobson IM, Reddy KR, Goodman ZD, Boparai N, DiNubile MJ, Sniukiene V, Brass CA, Albrecht JK, Bronowicki JP. 2011. Boceprevir for untreated chronic HCV genotype 1 infection. N Engl J Med 364:1195-1206.
47. Poynard T, Marcellin P, Lee SS, Niederau C, Minuk GS, Ideo G, Bain V, Heathcote J, Zeuzem S, Trepo C, Albrecht J. 1998. Randomised trial of interferon alpha2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alpha2b plus placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. International Hepatitis Interventional Therapy Group (IHIT). Lancet 352:1426-1432.
48. Reichard O, Andersson J, Schvarcz R, Weiland O. 1991. Ribavirin treatment for chronic hepatitis C. Lancet 337:1058-1061.
49. Rho J, Ryu JS, Hur W, Kim CW, Jang JW, Bae SH, Choi JY, Jang SK, Yoon SK. 2008. Hepatitis C virus (HCV) genotyping by annealing reverse transcription-PCR products with genotypespecific capture probes. J Microbiol 46:81-87.
50. Rotman Y, Noureddin M, Feld JJ, Guedj J, Witthaus M, Han H, Park YJ, Park SH, Heller T, Ghany MG, Doo E, Koh C, Abdalla A, Gara N, Sarkar S, Thomas E, Ahlenstiel G, Edlich B, Titerence R, Hogdal L, Rehermann B, Dahari H, Perelson AS, Hoofnagle JH, Liang TJ. 2013. Effect of ribavirin on viral kinetics and liver gene expression in chronic hepatitis C. Gut 63:161-169.
51. Schiappa DA, Mittal C, Brown JA, Mika BP. 2002. Relationship of hepatitis C genotype 1 NS5A sequence mutations to early phase viral kinetics and interferon effectiveness. J Infect Dis 185:868-877.
52. Sievert W, Dore GJ, McCaughan GW, Yoshihara M, Crawford DH, Cheng W, Weltman M, Rawlinson W, Rizkalla B, Depamphilis JK, Roberts SK. 2011. Virological response is associated with decline in hemoglobin concentration during pegylated interferon and ribavirin therapy in hepatitis C virus genotype 1. Hepatology 53:1109-1117.
53. Sulkowski MS, Shiffman ML, Afdhal NH, Reddy KR, McCone J, Lee WM, Herrine SK, Harrison SA, Poordad FF, Koury K, Deng W, Noviello S, Pedicone LD, Brass CA, Albrecht JK, McHutchison JG. 2010. Hepatitis C virus treatment-related anemia is associated with higher sustained virological response rate. Gastroenterology 139:1602-1611.
54. Susser S, Welsch C, Wang Y, Zettler M, Domingues FS, Karey U, Hughes E, Ralston R, Tong X, Herrmann E, Zeuzem S, Sarrazin C. 2009. Characterization of resistance to the protease inhibitor boceprevir in hepatitis C virus-infected patients. Hepatology 50:1709-1718.
55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEG A5: Molecular evolutionary genetics analysis using maximum likelihood evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739.
56. Tox U, Schulte S, Heindl B, Goeser T, Drebber U, Stelzer A, Steffen HM. 2008. Ribavirin priming in patients with chronic hepatitis C and normal ALT: A pilot study. Hepato-Gastroenterol 55:1666-1670.
57. Zeuzem S, Asselah T, Angus P, Zarski JP, Larrey D, Mullhaupt B, Gane E, Schuchmann M, Lohse A, Pol S, Bronowicki JP, Roberts S, Arasteh K, Zoulim F, Heim M, Stern JO, Kukolj G, Nehmiz G, Haefner C, Boecher WO. 2011. Efficacy of the protease inhibitor BI 201335, polymerase inhibitor BI 207127, and ribavirin in patients with chronic HCV infection. Gastroenterology 141: 2047-2055.
58. Zhou S, Liu R, Baroudy BM, Malcolm BA, Reyes GR. 2003. The effect of ribavirin and IMPDH inhibitors on hepatitis C virus subgenomic replicon RNA. Virology 310:333-342.