The impact of hepatitis C burden: An evidence-based approach

Alimentary Pharmacology and Therapeutics

Volumn 39, Issue 5, 2014, Pages 518-531

  Younossi, Z M ^a,b   Kanwal, F ^c   Saab, S ^d   Brown, K A ^e   El Serag, H B ^c   Kim, W R ^f   Ahmed, A ^g   Kugelmas, M ^h   Gordon, S C ^e  

^a BETTY AND GUY BEATTY CENTER FOR INTEGRATED RESEARCH   (United States)

^b INOVA FAIRFAX HOSPITAL   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e HENRY FORD HOSPITAL   (United States)

^f MAYO CLINIC   (United States)

^g STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COST OF ILLNESS; DIABETES MELLITUS, TYPE 2; HEART DISEASES; HEPATITIS C; HUMANS; LIVER DISEASES; LYMPHOMA; MIDDLE AGED; QUALITY OF LIFE; RHEUMATIC DISEASES; UNITED STATES;

EID: 84893810524     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.12625     Document Type: Article

References (109)

1. Sanyal AJ,. The Institute of Medicine report on viral hepatitis: a call to action. Hepatology 2010; 51: 727-8.
2. Freeman RB Jr, Steffick DE, Guidinger MK, Farmer DG, Berg CL, Merion RM,. Liver and intestine transplantation in the United States, 1997-2006. Am J Transplant 2008; 8: 958-76.
3. Velázquez RF, Rodríguez M, Navascués CA, et al,. Prospective analysis of risk factors for hepatocellular carcinoma in patients with liver cirrhosis. Hepatology 2003; 37: 520-7.
4. Yang JD, Kim WR, Coelho R, et al,. Cirrhosis is present in most patients with hepatitis B and hepatocellular carcinoma. Clin Gastroenterol Hepatol 2011; 9: 64-70.
5. Maasoumy B, Wedemeyer H,. Natural history of acute and chronic hepatitis C. Best Pract Res Clin Gastroenterol 2012; 26: 401-12.
6. Omland LH, Krarup H, Jepsen P, et al,. Mortality in patients with chronic and cleared hepatitis C viral infection: a nationwide cohort study. J Hepatol 2010; 53: 36-42.
7. Grady B, van den Berg C, van der Helm J, et al,. No impact of hepatitis C virus infection on mortality among drug users during the first decade after seroconversion. Clin Gastroenterol Hepatol 2011; 9: 786-92.
8. Uto H, Stuver SO, Hayashi K, et al,. Increased rate of death related to presence of viremia among hepatitis C virus antibody-positive subjects in a community-based cohort study. Hepatology 2009; 50: 393-9.
9. Lee MH, Yang HI, Lu SN, et al,. Chronic hepatitis C virus infection increases mortality from hepatic and extrahepatic diseases: a community-based long-term prospective study. J Infect Dis 2012; 206: 469-77.
10. El-Kamary SS, Jhaveri R, Shardell MD,. All-cause, liver-related, and non-liver-related mortality among HCV-infected individuals in the general US population. Clin Infect Dis 2011; 53: 150-7.
11. Neal KR,; Trent Hepatitis C Study Group, Ramsay S, Thomson BJ, Irving WL,. Excess mortality rates in a cohort of patients infected with the hepatitis C virus: a prospective study. Gut 2007; 56: 1098-104.
12. Younossi ZM, Stepanova M, Nader F, Younossi Z, Elsheikh E,. Associations of chronic hepatitis C with metabolic and cardiac outcomes. Aliment Pharmacol Ther 2013; 37: 647-52.
13. Guiltinan AM, Kaidarova Z, Custer B, et al,. Increased all-cause, liver, and cardiac mortality among hepatitis C virus-seropositive blood donors. Am J Epidemiol 2008; 167: 743-50.
14. Ly K, Xing J, Klevens M, Jiles R, Ward J, Holmberg S,. The growing burden of mortality from viral hepatitis in the US, 1999-2007. Ann Intern Med 2012; 156: 271-8.
15. El Khoury AC, Klimack WK, Wallace C, Razavi H,. Economic burden of hepatitis C-associated diseases in the United States. J Viral Hepat 2012; 19: 153-60.
16. Davis GL, Alter MJ, El-Serag H, Poynard T, Jennings LW,. Aging of hepatitis C virus (HCV)-infected persons in the United States: a multiple cohort model of HCV prevalence and disease progression. Gastroenterology 2010; 138: 513-21.
17. Pyenson B, Fitch K, Iwasaki K,. Consequences of Hepatitis C Virus (HCV): Costs of a Baby Boomer Epidemic of Liver Disease. New York, NY: Milliman, Inc; May 18, 2009. Available at: http://publications.milliman.com/research/health-rr/ pdfs/consequences-hepatitis-c-virus-RR05-18-09.pdf. Accessed July 15, 2013.
18. Gordon SC, Pockros PJ, Terrault NA, et al,. Impact of disease severity on healthcare costs in patients with chronic hepatitis C (CHC) virus infection. Hepatology 2012; 56: 1651-60.
19. Institute of Medicine. Hepatitis and Liver Cancer: a National Strategy for Prevention and Control of Hepatitis B and C. Washington, DC: The National Academies Press, 2010.
20. Centers for Disease Control and Prevention. Recommendations for prevention and control of hepatitis C virus (HCV) infection and HCV-related chronic disease. MMWR 1998; 47: 1-39.
21. Centers for Disease Control and Prevention. Recommendations for the identification of chronic hepatitis C virus infection among persons born during 1945-1965. MMWR 2012; 61: 1-18.
22. Moyer VA,; on behalf of the US Preventive Services Task Force. Screening for hepatitis C virus infection in adults: US preventive services task force recommendation statement. Ann Intern Med 2013; 159: 349-57.
23. Pockros PJ,. Interferon-free hepatitis C therapy: how close are we? Drugs 2012; 72: 1825-31.
24. American Heart Association. Available at: http://my.americanheart.org/ idc/groups/ahamah-public/@wcm/@sop/documents/downloadable/ucm-319826.p4. Accessed August 6, 2013.
25. Shiffman RN, Shekelle P, Overhage JM, Slutsky J, Grimshaw J, Deshpande AM,. Standardized reporting of clinical practice guidelines: a proposal from the Conference on Guideline Standardization. Ann Intern Med 2003; 139: 493-8.
26. Kanwal F, Hoang T, Kramer JR, et al,. Increasing prevalence of HCC and cirrhosis in patients with chronic hepatitis C virus infection. Gastroenterology 2011; 140: 1182-8.
27. Thein HH, Yi Q, Dore GJ, Krahn MD,. Estimation of stage-specific fibrosis progression rates in chronic hepatitis C virus infection: a meta-analysis and meta-regression. Hepatology 2008; 48: 418-31.
28. Hui JM, Sud A, Farrell GC, et al,. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression [corrected]. Gastroenterology 2003; 125: 1695-704.
29. Sanyal AL,. Review article: non-alcoholic fatty liver disease and hepatitis C-risk factors and clinical implications. Aliment Pharmacol Ther 2005; 22 (Suppl. 2): 48-51.
30. Petta S, Camma C, Di Marco V, et al,. Insulin resistance and diabetes increase fibrosis in the liver of patients with genotype 1 HCV infection. Am J Gastroenterol 2008; 103: 1136-44.
31. Probst A, Dang T, Bochud M, Egger M, Negro F, Bochud PY,. Role of hepatitis C virus genotype 3 in liver fibrosis progression-a systematic review and meta-analysis. J Viral Hepat 2011; 18: 745-59.
32. Di Bisceglie AM, Lyra AC, Schwartz M, et al,. Hepatitis C-related hepatocellular carcinoma in the United States: influence of ethnic status. Am J Gastroenterol 2003; 98: 2060-3.
33. Donato F, Boffetta P, Puoti M,. A meta-analysis of epidemiological studies on the combined effect of hepatitisB and C virus infections in causing hepatocellular carcinoma. Int J Cancer 1998; 75: 347-54.
34. El-Serag HB, Richardson PA, Everhart JE,. The role of diabetes in hepatocellular carcinoma: a case-control study among United States Veterans. Am J Gastroenterol 2001; 96: 2462-7.
35. Cho LY, Yang JJ, Ko KP, et al,. Coinfection of hepatitis B and C viruses and risk of hepatocellular carcinoma: systematic review and meta-analysis. Int J Cancer 2011; 128: 176-84.
36. Goodgame B, Shaheen NJ, Galanko J, El-Serag HB,. The risk of end stage liver disease and hepatocellular carcinoma among persons infected with hepatitis C virus: publication bias? Am J Gastroenterol 2003; 98: 2535-42.
37. Fattovich G, Stroffolini T, Zagni I, Donato F,. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004; 127 (Suppl. 1): S35-50.
38. Mair RD, Valenzuela A, Ha NB, et al,. Incidence of hepatocellular carcinoma among US patients with cirrhosis of viral or nonviral etiologies. Clin Gastroenterol Hepatol 2012; 10: 1412-7.
39. Alazawi W, Cunningham M, Dearden J, Foster GR,. Systematic review: outcome of compensated cirrhosis due to chronic hepatitis C infection. Aliment Pharmacol Ther 2010; 32: 344-55.
40. Chuang SC, Lee YC, Hashibe M, Dai M, Zheng T, Boffetta P,. Interaction between cigarette smoking and hepatitis B and C virus infection on the risk of liver cancer: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2010; 19: 1261-8.
41. Bravi F, Bosetti C, Tavani A, Gallus S, La Vecchia C,. Coffee reduces risk for hepatocellular carcinoma: an updated meta-analysis. Clin Gastroenterol Hepatol 2013; 11: 1413-21.e1.
42. McMahon BJ, Bruden D, Bruce MG, et al,. Adverse outcomes in Alaska natives who recovered from or have chronic hepatitis C infection. Gastroenterology 2010; 138: 922-31.
43. Seeff LB, Hollinger FB, Alter HJ, et al. Long-term mortality and morbidity of transfusion-associated non-A, non-B, and type C hepatitis: a National Heart, Lung, and Blood Institute collaborative study. Hepatology 2001; 33: 455-63.
44. Harris HE, Ramsay ME, Andrews NJ,; HCV National Register Steering Group. Survival of a national cohort of hepatitis C virus infected patients, 16 years after exposure. Epidemiol Infect 2006; 134: 472-7.
45. Grebely J, Raffa JD, Lai C, et al,. Impact of hepatitis C virus infection on all-cause and liver-related mortality in a large community-based cohort of inner city residents. J Viral Hepat 2011; 18: 32-41.
46. Yamasaki K, Tomohiro M, Nagao Y, et al,. Effects and outcomes of interferon treatment in Japanese hepatitis C patients. BMC Gastroenterol 2012; 12: 139.
47. Amin J, Law MG, Bartlett M, Kaldor JM, Dore GJ,. Causes of death after diagnosis of hepatitis B or hepatitis C infection: a large community-based linkage study. Lancet 2006; 368: 938-45.
48. Duberg AS, Törner A, Davidsdóttir L, et al,. Cause of death in individuals with chronic HBV and/or HCV infection, a nationwide community-based register study. J Viral Hepat 2008; 15: 538-50.
49. Kristiansen MG, Løchen ML, Gutteberg TJ, Mortensen L, Eriksen BO, Florholmen J,. Total and cause-specific mortality rates in a prospective study of community-acquired hepatitis C virus infection in northern Norway. J Viral Hepat 2011; 18: 237-44.
50. Wang CS, Wang ST, Yao WJ, Chang TT, Chou P,. Community-based study of hepatitis C virus infection and type 2 diabetes: an association affected by age and hepatitis severity status. Am J Epidemiol 2003; 158: 1154-60.
51. Zein CO, Levy C, Basu A, Zein NN,. Chronic hepatitis C and type II diabetes mellitus: a prospective cross-sectional study. Am J Gastroenterol 2005; 100: 48-55.
52. Thuluvath PJ, John PR,. Association between hepatitis C, diabetes mellitus, and race. a case-control study. Am J Gastroenterol 2003; 98: 438-41.
53. Arase Y, Kobayashi M, Suzuki F, et al,. Effect of type 2 diabetes on risk for malignancies includes hepatocellular carcinoma in chronic hepatitis C. Hepatology 2013; 57: 964-73.
54. Giordanino C, Bugianesi E, Smedile A, et al,. Incidence of type 2 diabetes mellitus and glucose abnormalities in patients with chronic hepatitis C infection by response to treatment: results of a cohort study. Am J Gastroenterol 2008; 103: 2481-7.
55. Romero-Gómez M, Fernández-Rodríguez CM, Andrade RJ, et al,. Effect of sustained virological response to treatment on the incidence of abnormal glucose values in chronic hepatitis C. J Hepatol 2008; 48: 721-7.
56. Arase Y, Suzuki F, Suzuki Y, et al,. Sustained virological response reduces incidence of onset of type 2 diabetes in chronic hepatitis C. Hepatology 2009; 49: 739-44.
57. El-Serag HB, Hampel H, Yeh C, Rabeneck L,. Extrahepatic manifestations of hepatitis C among United States male veterans. Hepatology 2002; 36: 1439-45.
58. Stefanova-Petrova DV, Tzvetanska AH, Naumova EJ, et al,. Chronic hepatitis C virus infection: prevalence of extrahepatic manifestations and association with cryoglobulinemia in Bulgarian patients. World J Gastroenterol 2007; 13: 6518-28.
59. Franceschi S, Lise M, Trépo C, et al,. Infection with hepatitis B and C viruses and risk of lymphoid malignancies in the European Prospective Investigation into Cancer and Nutrition (EPIC). Cancer Epidemiol Biomarkers Prev 2011; 20: 208-14.
60. Cowgill KD, Loffredo CA, Eissa SA, et al,. Case-control study of non-Hodgkin's lymphoma and hepatitis C virus infection in Egypt. Int J Epidemiol 2004; 33: 1034-9.
61. Rabkin CS, Tess BH, Christianson RE, et al,. Prospective study of hepatitis C viral infection as a risk factor for subsequent B-cell neoplasia. Blood 2002; 99: 4240-2.
62. Ishizaka N, Ishizaka Y, Takahashi E,. Association between hepatitis C virus seropositivity, carotid-artery plaque, and intima-media thickening. Lancet 2002; 359: 133-5.
63. Vassalle C, Masini S, Bianchi F, Zucchelli GC,. Evidence for association between hepatitis C virus seropositivity and coronary artery disease. Heart 2004; 90: 565-6.
64. Adinolfi LE, Restivo L, Zampino R, et al,. Chronic HCV infection is a risk of atherosclerosis. Role of HCV and HCV-related steatosis. Atherosclerosis 2012; 221: 496-502.
65. Miyajima I, Kawaguchi T, Fukami A, et al,. Chronic HCV infection was associated with severe insulin resistance and mild atherosclerosis: a population-based study in an HCV hyperendemic area. J Gastroenterol 2013; 48: 93-100.
66. Lee MH, Yang HI, Wang CH, et al,. Hepatitis C virus infection and increased risk of cerebrovascular disease. Stroke 2010; 41: 2894-900.
67. Freiberg MS, Chang CC, Skanderson M, et al,. The risk of incident coronary heart disease among veterans with and without HIV and hepatitis C. Circ Cardiovasc Qual Outcomes 2011; 4: 425-32.
68. Hsu CS, Kao JH, Chao YC, et al,. Interferon-based therapy reduces risk of stroke in chronic hepatitis C patients: a population-based cohort study in Taiwan. Aliment Pharmacol Ther 2013; 38: 415-23.
69. Organ Procurement and Transplantation Network (OPTN) and Scientific Registry of Transplant Recipients (SRTR). OPTN/SRTR 2011 Annual Data Report. Rockville, MD: Department of Health and Human Services, Health Resources and Services Administration, Healthcare Systems Bureau, Division of Transplantation, 2012.
70. Garcia-Retortillo M, Forns X, Feliu A, et al,. Hepatitis C virus kinetics during and immediately after liver transplantation. Hepatology 2002; 35: 680-7.
71. Gane EJ,. The natural history of recurrent hepatitis C and what influences this. Liver Transpl 2008; 14 (Suppl): S36-44.
72. Berenguer M, Prieto M, Rayón JM, et al,. Natural history of clinically compensated hepatitis C virus-related graft cirrhosis after liver transplantation. Hepatology 2000; 32: 852-8.
73. Berenguer M, Ferrell L, Watson J, et al,. HCV-related fibrosis progression following liver transplantation: increase in recent years. J Hepatol 2000; 32: 673-84.
74. Poynard T, Bedossa P, Opolon P,. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 1997; 349: 825-32.
75. Forman LM, Lewis JD, Berlin JA, Feldman HI, Lucey MR,. The association between hepatitis C infection and survival after orthotopic liver transplantation. Gastroenterology 2002; 122: 889-96.
76. Berenguer M, Prieto M, San Juan F, et al,. Contribution of donor age to the recent decrease in patient survival among HCV-infected liver transplant recipients. Hepatology 2002; 36: 202-10.
77. Thuluvath PJ, Krok KL, Segev DL, Yoo HY,. Trends in post-liver transplant survival in patients with hepatitis C between 1991 and 2001 in the United States. Liver Transpl 2007; 13: 719-24.
78. Futagawa Y, Terasaki PI, Waki K, Cai J, Gjertson DW,. No improvement in long-term liver transplant graft survival in the last decade: an analysis of the UNOS data. Am J Transplant 2006; 6: 1398-406.
79. Lake JR, Shorr JS, Steffen BJ, Chu AH, Gordon RD, Wiesner RH,. Differential effects of donor age in liver transplant recipients infected with hepatitis B, hepatitis C and without viral hepatitis. Am J Transplant 2005; 5: 549-57.
80. Uemura T, Nikkel LE, Hollenbeak CS, Ramprasad V, Schaefer E, Kadry Z,. How can we utilize livers from advanced aged donors for liver transplantation for hepatitis C? Transpl Int 2012; 25: 671-9.
81. Gane EJ, Naoumov NV, Qian KP, et al,. A longitudinal analysis of hepatitis C virus replication following liver transplantation. Gastroenterology 1996; 110: 167-77.
82. Rosen HR, Shackleton CR, Higa L, et al,. Use of OKT3 is associated with early and severe recurrence of hepatitis C after liver transplantation. Am J Gastroenterol 1997; 92: 1453-7.
83. Brillanti S, Vivarelli M, De Ruvo N, et al,. Slowly tapering off steroids protects the graft against hepatitis C recurrence after liver transplantation. Liver Transpl 2002; 8: 884-8.
84. Yoo HY, Maheshwari A, Thuluvath PJ,. Retransplantation of liver: primary graft nonfunction and hepatitis C virus are associated with worse outcome. Liver Transpl 2003; 9: 897-904.
85. Pelletier SJ, Schaubel DE, Punch JD, Wolfe RA, Port FK, Merion RM,. Hepatitis C is a risk factor for death after liver retransplantation. Liver Transpl 2005; 11: 434-40.
86. McCashland T, Watt K, Lyden E, et al,. Retransplantation for hepatitis C: results of a US multicenter retransplant study. Liver Transpl 2007; 13: 1246-53.
87. Berenguer M,. Systematic review of the treatment of established recurrent hepatitis C with pegylated interferon in combination with ribavirin. J Hepatol 2008; 49: 274-87.
88. Picciotto FP, Tritto G, Lanza AG, et al,. Sustained virological response to antiviral therapy reduces mortality in HCV reinfection after liver transplantation. J Hepatol 2007; 46: 459-65.
89. Berenguer M, Palau A, Aguilera V, Rayón JM, Juan FS, Prieto M,. Clinical benefits of antiviral therapy in patients with recurrent hepatitis C following liver transplantation. Am J Transplant 2008; 8: 679-87.
90. Seeff LB, Buskell-Bales Z, Wright EC, et al,. Long-term mortality after transfusion-associated non-A, non-B hepatitis. The National Heart, Lung, and Blood Institute Study Group. N Engl J Med 1992; 327: 1906-11.
91. Kielland KB, Skaug K, Amundsen EJ, Dalgard O,. All-cause and liver-related mortality in hepatitis C infected drug users followed for 33 years: a controlled study. J Hepatol 2013; 58: 31-7.
92. Just SA, Grau K, Georgsen J, et al,. Long-term follow-up among Danish transfusion recipients identified in the national hepatitis C lookback. Transfusion 2012; 52: 582-8.
93. Morgan TR, Ghany MG, Kim HY, et al,. Outcome of sustained virological responders with histologically advanced chronic hepatitis C. Hepatology 2010; 52: 833-44.
94. Veldt BJ, Heathcote EJ, Wedemeyer H, et al,. Sustained virologic response and clinical outcomes in patients with chronic hepatitis C and advanced fibrosis. Ann Intern Med 2007; 147: 677-84.
95. Butt AA, Wang X, Moore CG,. Effect of hepatitis C virus and its treatment on survival. Hepatology 2009; 50: 387-92.
96. Backus LI, Boothroyd DB, Phillips BR, Belperio P, Halloran J, Mole LA,. A sustained virologic response reduces risk of all-cause mortality in patients with hepatitis C. Clin Gastroenterol Hepatol 2011; 9: 509-16.
97. Ghany MG, Strader DB, Thomas DL, Seeff LB,; American Association for the Study of Liver Diseases. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 2009; 49: 1335-74.
98. DiBonaventura MD, Wagner JS, Yuan Y, L'Italien G, Langley P, Ray Kim W,. Humanistic and economic impacts of hepatitis C infection in the United States. J Med Econ 2010; 13: 709-18.
99. McCombs JS, Yuan Y, Shin J, Saab S,. Economic burden associated with patients diagnosed with hepatitis C. Clin Ther 2011; 33: 1268-80.
100. Davis KL, Mitra D, Medjedovic J, Beam C, Rustgi V,. Direct economic burden of chronic hepatitis C virus in a United States managed care population. J Clin Gastroenterol 2011; 45: e17-24.
101. John-Baptiste AA, Tomlinson G, Hsu PC, et al,. Sustained responders have better quality of life and productivity compared with treatment failures long after antiviral therapy for hepatitis C. Am J Gastroenterol 2009; 104: 2439-48.
102. Peery AF, Dellon ES, Lund J, et al,. Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 2012; 143: 1179-87.
103. Testa MA, Simonson DC,. Assesment of quality-of-life outcomes. N Engl J Med 1996; 334: 835-40.
104. Martin LM, Younossi ZM,. Health-related quality of life (HRQL) in chronic liver disease. Dig Liver Dis 2005; 37: 819-20.
105. Ware JE, Snow KK, Kosinski M, Gandek B,. SF-36 Health Survey Manual and Interpretation Guide. Boston, MA: The Health Institute, New England Medical Center, 1993.
106. Bonkovsky HL, Snow KK, Malet PF, et al,. Health-related quality of life in patients with chronic hepatitis C and advanced fibrosis. J Hepatol 2007; 46: 420-31.
107. Hsu PC, Federico CA, Krajden M, et al,. Health utilities and psychometric quality of life in patients with early- and late-stage hepatitis C virus infection. J Gastroenterol Hepatol 2012; 27: 149-57.
108. Tillmann HL, Wiese M, Braun Y, et al,. Quality of life in patients with various liver diseases: patients with HCV show greater mental impairment, while patients with PBC have greater physical impairment. J Viral Hepat 2011; 18: 252-61.
109. Dan AA, Kallman JB, Srivastava R, Younoszai Z, Kim A, Younossi ZM,. Impact of chronic liver disease and cirrhosis on health utilities using SF-6D and the health utility index. Liver Transpl 2008; 14: 321-6.