Oral Combination Therapies for Hepatitis C Virus Infection: Successes, Challenges, and Unmet Needs

Annual Review of Medicine

Volumn 68, Issue , 2017, Pages 345-358

  Naggie, Susanna ^a   Muir, Andrew J ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Decompensated cirrhosis, liver transplant; End stage liver disease; HCV, direct acting antiviral, HIV HCV coinfection; Kidney transplant

Indexed keywords

ANTIVIRUS AGENT; BOCEPREVIR; DACLATASVIR; DASABUVIR; ELBASVIR PLUS GRAZOPREVIR; LEDIPASVIR PLUS SOFOSBUVIR; OMBITASVIR PLUS PARITAPREVIR PLUS RITONAVIR; PEGINTERFERON; RIBAVIRIN; SIMEPREVIR; SOFOSBUVIR; SOFOSBUVIR PLUS VELPATASVIR; TELAPREVIR;

ARTICLE; END STAGE RENAL DISEASE; GENOTYPE; HEALTH CARE NEED; HEALTH CARE QUALITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KIDNEY TRANSPLANTATION; LIVER TRANSPLANTATION; MIXED INFECTION; OUTCOME ASSESSMENT; PRIORITY JOURNAL; SUSTAINED VIROLOGIC RESPONSE; TREATMENT INDICATION; VIRUS RESISTANCE; ANTIVIRAL RESISTANCE; CHRONIC KIDNEY FAILURE; COMBINATION DRUG THERAPY; COMPLICATION; GENETICS; HEPACIVIRUS; LIVER CIRRHOSIS; ORAL DRUG ADMINISTRATION; PATHOPHYSIOLOGY; PROCEDURES; RECURRENT DISEASE; SECONDARY PREVENTION; TREATMENT FAILURE; VIROLOGY;

ADMINISTRATION, ORAL; ANTIVIRAL AGENTS; COINFECTION; DRUG RESISTANCE, VIRAL; DRUG THERAPY, COMBINATION; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HIV INFECTIONS; HUMANS; KIDNEY FAILURE, CHRONIC; LIVER CIRRHOSIS; LIVER TRANSPLANTATION; RECURRENCE; SECONDARY PREVENTION; TREATMENT FAILURE;

EID: 85010015264     PISSN: 00664219     EISSN: 1545326X     Source Type: Book Series    
DOI: 10.1146/annurev-med-052915-015720     Document Type: Article

References (68)

1. Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. 2013. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 57:1333-42
2. Wong RJ, Aguilar M, Cheung R, et al. 2015. Nonalcoholic steatohepatitis is the second leading etiology of liver disease among adults awaiting liver transplantation in the United States. Gastroenterology 148:547-55
3. Ly KN, Hughes EM, Jiles RB, Holmberg SD. 2016. Rising mortality associated with hepatitis C virus in the United States, 2003-2013. Clin. Infect. Dis. 62:1287-88
4. Mallet V, Gilgenkrantz H, Serpaggi J, et al. 2008. Brief communication: the relationship of regression of cirrhosis to outcome in chronic hepatitis C. Ann. Intern. Med. 149:399-403
5. McHutchison JG, Lawitz EJ, ShiffmanML, et al. 2009. Peginterferon alfa-2b or alfa-2a with ribavirin for treatment of hepatitis C infection. N. Engl. J. Med. 361:580-93
6. Chung RT, Andersen J, Volberding P, et al. 2004. Peginterferon alfa-2a plus ribavirin versus interferon alfa-2a plus ribavirin for chronic hepatitis C in HIV-coinfected persons. N. Engl. J. Med. 351:451-59
7. Muir AJ, Bornstein JD, Killenberg PG, for the Atlantic Coast Hepatitis Treatment Group. 2004. Peginterferon alfa-2b and ribavirin for the treatment of chronic hepatitis C in blacks and non-Hispanic whites. N. Engl. J. Med. 350:2265-71
8. Berry PA, Thomson SJ. 2013. The patient presenting with decompensated cirrhosis. AcuteMed. 12:232-38
9. Victrelis [package insert]. Whitehouse Station, NJ: Merck & Co., Inc. ; 2011
10. Incivek [package insert]. Cambridge, MA: Vertex Pharmaceuticals, Inc. ; 2011
11. Olysio [package insert]. Titusville, NJ: Janssen Therapeutics; 2013
12. Sovaldi [package insert]. Foster City, CA: Gilead Sciences, Inc. ; 2013
13. Harvoni [package insert]. Foster City, CA: Gilead Sciences, Inc. ; 2014
14. Viekira Pak [package insert]. North Chicago, IL: AbbVie, Inc. ; 2014
15. Technivie [package insert]. North Chicago, IL: AbbVie, Inc. ; 2015
16. Daklinza [package insert]. Princeton, NJ: Bristol-Myers Squibb; 2015
17. Zepatier [package insert]. Whitehouse Station, NJ: Merck & Co., Inc. ; 2016
18. NEW N/A [package insert]. Foster City, CA: Gilead Sciences, Inc. ; 2016
19. Smith DB, Bukh J, Kuiken C, et al. 2014. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource. Hepatology 59:318-27
20. Nelson DR, Cooper JN, Lalezari JP, et al. 2015. All-oral 12-week treatment with daclatasvir (DCV) and sofosbuvir (SOF) in patients infected with hepatitis C virus genotype 3 infection: ALLY-3 phase 3 study. Hepatology 61:1127-35
21. Konerman MA, Mehta SH, Sutcliffe CG, et al. 2014. Fibrosis progression in human immunodeficiency virus/hepatitis C virus coinfected adults: prospective analysis of 435 liver biopsy pairs. Hepatology 59(3):767-75
22. Smith CJ, Ryom L, Weber R, et al. 2014. Trends in underlying causes of death in people with HIV from 1999 to 2011 (D:A:D): a multicohort collaboration. Lancet 384(9939):241-48
23. Naggie S, Cooper C, Saag M, et al. 2015. Ledipasvir and sofosbuvir for HCV in patients coinfected with HIV-1. N. Engl. J. Med. 373(8):705-13
24. Mehta SH, Lucas GM, Mirel LB, et al. 2006. Limited effectiveness of antiviral treatment for hepatitis C in an urban HIV clinic. AIDS 20(18):2361-69
25. Torriani FJ, Rodriguez-Torres M, Rockstroh JK, et al. 2004. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection in HIV-infected patients. N. Engl. J. Med. 351:438-50
26. Dieterich D, Rockstroh JK, Orkin C, et al. 2014. Simeprevir (TMC435) with pegylated interferon/ribavirin in patients coinfected with HCV genotype 1 and HIV-1: a phase 3 study. Clin. Infect. Dis. 59(11):1579-87
27. Rodriguez-Torres M, Gaggar A, Shen G, et al. 2015. Sofosbuvir for chronic hepatitis C virus infection genotype 1-4 in patients coinfected with HIV. J. Acquir. Immune Defic. Syndr. 68:543-49
28. Wyles DL, RuanePJ, SulkowskiMS, et al. 2015. Daclatasvir plus sofosbuvir forHCVin patients coinfected with HIV-1. N. Engl. J. Med. 373(8):714-25
29. Rockstroh JK, Nelson M, KatlamaC, et al. 2015. Efficacy and safety of grazoprevir (MK-5172) and elbasvir (MK-8742) in patients with hepatitisCvirus and HIV co-infection (C-EDGE CO-INFECTION): a nonrandomised, open-label trial. Lancet HIV 2(8):e319-27
30. Wyles D, Brau N, Kottilil S, et al. 2016. Sofosbuvir/velpatasvir for 12 weeks in patients coinfected with HCV and HIV-1: the ASTRAL-5 study. Presented at Int. Congr. Eur. Assoc. Stud. Liver Disease, Apr. 13-17, Barcelona, Spain
31. US Food and Drug Administration. 2016. Chronic hepatitis C virus infection: developing direct-acting antiviral drugs for treatment. Guidance for industry. May 2016 draft. http://www. fda.gov/downloads/drugs/guidancecomplianceregulatoryinformation/guidances/ucm225333.pdf
32. Fink SA, Jacobson IM. 2011. Managing patients with hepatitis-B-related or hepatitis-C-related decompensated cirrhosis. Nat. Rev. Gastroenterol. Hepatol. 8:285-95
33. Charlton M, Ruppert K, Belle SH, et al. 2004. Long-term results and modeling to predict outcomes in recipients with HCV infection: results of the NIDDK liver transplantation database. Liver Transpl. 10:1120-30
34. Berenguer M, Prieto M, Rayon JM, et al. 2000. Natural history of clinically compensated hepatitis C virus-related graft cirrhosis after liver transplantation. Hepatology 32:852-58
35. Forman LM, Lewis JD, Berlin JA, et al. 2002. The association between hepatitis C infection and survival after orthotopic liver transplantation. Gastroenterology 122:889-96
36. Forns X, Charlton M, Denning J, et al. 2015. Sofosbuvir compassionate use program for patients with severe recurrent hepatitis C after liver transplantation. Hepatology 61(5):1485-94
37. Charlton M, Everson GT, Flamm SL, et al. 2015. Ledipasvir and sofosbuvir plus ribavirin for treatment of HCV infection in patients with advanced liver disease. Gastroenterology 149(3):649-59
38. Manns M, Samuel D, Gane EJ, et al. 2016. Ledipasvir and sofosbuvir plus ribavirin in patients with genotype 1 or 4 hepatitis C virus infection and advanced liver disease: a multicentre, open-label, randomised, phase 2 trial. Lancet Infect. Dis. 16:685-97
39. Poordad F, Schiff ER, Vierling JM, et al. 2016. Daclatasvirwith sofosbuvir and ribavirin forHCVinfection with advanced cirrhosis or post-liver transplant recurrence. Hepatology 63:1493-505
40. Curry MP, O'Leary JG, Bzowej N, et al. 2015. Sofosbuvir and velpatasvir for HCV in patients with decompensated cirrhosis. N. Engl. J. Med. 373(27):2618-28
41. Gane EJ. 2008. The natural history of recurrent hepatitis C and what influences this. Liver Transpl. 14(Suppl. 2):S36-44
42. Curry MP, Forns X, Chung RT, et al. 2015. Sofosbuvir and ribavirin prevent recurrence ofHCVinfection after liver transplantation: an open-label study. Gastroenterology 148(1):100-7
43. Afdhal N, Zeuzem S, Kwo P, et al. 2014. Ledipasvir and sofosbuvir for untreated HCV genotype 1 infection. N. Engl. J. Med. 370(20):1889-98
44. Afdhal N, Reddy KR, Nelson DR, et al. 2014. Ledipasvir and sofosbuvir for previously treated HCV genotype 1 infection. N. Engl. J. Med. 370(16):1483-93
45. Noureddine LA, Usman SA, Yu Z, et al. 2010. Hepatitis C increases the risk of progression of chronic kidney disease in patients with glomerulonephritis. Am. J. Nephrol. 32:311-16
46. Tsui JI, Vittinghoff E, Shlipak MG, et al. 2007. Association of hepatitis C seropositivity with increased risk for developing end-stage renal disease. Arch. Intern. Med. 167:1271-76
47. Fabrizi F, Dixit V, Messa P. 2012. Impact of hepatitis C on survival in dialysis patients: a link with cardiovascular mortality J. Viral Hepat. 19:601-7
48. Pereira BJG, Wright TL, Schmid CH, Levey AS. 1995. The impact of pretransplantation hepatitis C infection on the outcome of renal transplantation. Transplantation 60:799-805
49. Burra P, Rodŕguez-Castro KI, Marchini F, et al. 2014. Hepatitis C virus infection in end-stage renal disease and kidney transplantation. Transpl. Int. 27(9):877-91
50. Roth D, Nelson DR, Bruchfeld A, et al. 2015. Grazoprevir plus elbasvir in treatment-naive and treatmentexperienced patients with hepatitis C virus genotype 1 infection and stage 4-5 chronic kidney disease (the C-SURFER study): a combination phase 3 study. Lancet 386(10003):1537-45
51. Kusnir J, Roth D. 2016. Direct-acting antiviral agents for the hepatitis C virus-infected chronic kidney disease population: the dawn of a new era. Semin. Dial. 29:5-6
52. Colombo M, Aghemo A, Liu H, et al. 2016. Ledipasvir/sofosbuvir (LDV/SOF) for 12 or 24 weeks is safe and effective in kidney transplant recipients with chronic genotype 1 or 4 HCV infection. Presented at Int. Congr. Eur. Assoc. Stud. Liver Disease, Apr. 13-17, Barcelona, Spain
53. Foster GR, Afdhal N, Roberts SK, et al. 2015. Sofosbuvir and velpatasvir for HCV genotype 2 and 3 infection. N. Engl. J. Med. 373:2608-17
54. Gower E, Estes C, Blach S, et al. 2014. Global epidemiology and genotype distribution of the hepatitis C virus infection. J. Hepatol. 61:S45-S57
55. Ampeuro J, Romero-Gomez M. 2015. Current and evolving treatments for genotypes 2 and 3. Gastroenterol. Clin. N. Am. 44:845-57
56. Abenavoli L, MasaroneM, Peta V, et al. 2014. Insulin resistance and liver steatosis in chronic hepatitis C infection genotype 3. World J. Gastroenterol. 20(41):15233-40
57. Clark PJ, Thompson AJ, Vock DM, et al. 2012. Hepatitis C virus selectively perturbs the distal cholesterol synthesis pathway in a genotype-specific manner. Hepatology 56(1):49-56
58. Scheel TKH, Rice CM. 2013. Understanding the hepatitis C virus life cycle paves the way for highly effective therapies. Nat. Med. 19:837-49
59. Kwo PY, Wyles DL, Wang S, et al. 2016. 100% SVR12 with ABT-493 and ABT-530 with or without ribavirin in treatment-näve HCV genotype 3-infected patients with cirrhosis. Presented at Int. Congr. Eur. Assoc. Stud. Liver Disease, Apr. 13-17, Barcelona, Spain
60. Muir AJ, Strasser S, Wang S, et al. 2016. High SVR rates with ABT-493 + ABT-530 co-administered for 8 weeks in non-cirrhotic patients with HCV genotype 3 infection. Presented at Int. Congr. Eur. Assoc. Stud. Liver Disease, Apr. 13-17, Barcelona, Spain
61. Rong L, Dahari H, Ribeiro RM, Perelson AS. 2010. Rapid emergence of protease inhibitor resistance in hepatitis C virus. Sci. Transl. Med. 2:30-32
62. Howe AYM, Long J, Nickle D, et al. 2015. Long-term follow-up of patients receiving boceprevir for treatment of chronic hepatitis C. Antivir. Res. 113:71-78
63. Dvory-Sobol H, Wyles D, Ouyang W, et al. 2015. Long-term persistence of HCV NS5A variants after treatment with NS5A inhibitor ledipasvir. J. Hepatol. 62:S221
64. Sarrazin C, Dvory-Sobol H, Svarovskaia E, et al. 2016. Prevalence of resistance-associated substitutions in HCVNS5A, NS5B, orNS3 and outcomes of treatment with ledipasvir and sofosbuvir. Gastroenterology 151:501-12
65. American Association for the Study of Liver Diseases and Infectious Diseases Society of America (AASLD-IDSA). 2016. Recommendations for testing, managing, and treating hepatitis C. http://www. hcvguidelines. org
66. Lawitz E, Flamm S, Yang JC, et al. 2015. Retreatment of patients who failed 8 or 12 weeks of ledipasvir/sofosbuvir-based regimens with ledipasvir/sofosbuvir for 24 weeks. Presented at Annu. Meet. Eur. Assoc. Stud. Liver (EASL), 50th, Apr. 22-26, Vienna, Austria, Abstr. 0005
67. CooperC, Naggie S, Saag M, et al. 2016. Successful re-treatment of hepatitisCvirus in patients coinfected with HIV who relapsed after 12 weeks of ledipasvir/sofosbuvir. Clin. Infect. Dis. 63:528-31
68. Schwarz K, Murray KF, Rosenthal P, et al. 2016. High rate of SVR in adolescents treated with the combination of ledipasvir/sofosbuvir. Presented at Int. Congr. Eur. Assoc. Stud. Liver Disease, Apr. 13-17, Barcelona, Spain