Gastroenterology
Volume 138, Issue 2 , Pages 513-521.e6 , February 2010

Aging of Hepatitis C Virus (HCV)-Infected Persons in the United States: A Multiple Cohort Model of HCV Prevalence and Disease Progression

  • Gary L. Davis

      Affiliations

    • Division of Hepatology, Baylor University Medical Center and Baylor Regional Transplant Institute, Dallas, Texas
    • Corresponding Author InformationReprint requests Address requests for reprints to: Gary L. Davis, MD, Hepatology, 4 Roberts, Baylor University Medical Center, 3500 Gaston Avenue, Dallas, Texas 75246. fax: (214) 820-8168
  • ,
  • Miriam J. Alter

      Affiliations

    • Infectious Disease Epidemiology Program, University of Texas Medical Branch, Galveston, Texas
  • ,
  • Hashem El–Serag

      Affiliations

    • Baylor College of Medicine and Michael E. DeBakey Veterans Affairs Medical Center, Houston, Texas
  • ,
  • Thierry Poynard

      Affiliations

    • Assistance Publique Hôpitaux de Paris, Université Pierre et Marie Curie Liver Center, Paris, France
  • ,
  • Linda W. Jennings

      Affiliations

    • Division of Hepatology, Baylor University Medical Center and Baylor Regional Transplant Institute, Dallas, Texas

Received 15 July 2009 ,Accepted 28 September 2009.

References 

  1. Alter MJ, Kruszon-Moran D, Nainan OV, et al. The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med. 1999;341:556–562
  2. Armstrong GL, Wasley A, Simard EP, et al. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med. 2006;144:705–714
  3. Alter MJ, Hadler SC, Judson FN, et al. Risk factors for acute non-A, non-B hepatitis in the United States and association with hepatitis C virus infection. JAMA. 1990;264:2231–2235
  4. Seeff LB, Buskell-Bales Z, Wright EC, et al. Long-term mortality after transfusion-associated non-A, non-B hepatitis. New Engl J Med. 1992;327:1906–1911
  5. El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med. 1999;340:745–750
  6. Everhart JE, Ruhl CE. Burden of digestive disease in the United States Part III: liver, biliary tract and pancreas. Gastroenterology. 2009;136:1134–1144
  7. National Ambulatory Medical Care Survey (NAMCS), National Hospital Medical Care Survey (NHMCS), National Hospital Discharge Survey), National Center for Health Statistics. http://www.cdc.gov/nchs/products/pubs/pubd/vsus/vsus.htmhttp://www.cdc.gov/nchs/express.htmAccessed July 26, 2008
  8. Kim WR, Gross JB, Poterucha JJ, et al. Outcome of hospital care of liver disease associated with hepatitis C in the United States. Hepatology. 2001;33:201–206
  9. Vong S, Bell BP. Chronic liver disease mortality in the United States, 1990−1998. Hepatology. 2004;39:476–483
  10. Wise M, Bialek S, Finelli L, et al. Changing trends in hepatitis C-related mortality in the United States, 1995–2004. Hepatology. 2008;47:1128–1135
  11. Manos MM, Leyden WA, Murphy RC, et al. Limitations of conventionally derived chronic liver disease mortality rates: Results of a comprehensive assessment. Hepatology. 2008;47:1150–1157
  12. Neal RK Trent Hepatitis C Study Group. Excess mortality in a cohort of persons infected with the hepatitis C virus: a prospective study. Gut. 2007;56:1098–1104
  13. Davis GL, Albright JE, Cook SF, Rosenberg DM. Projecting the future healthcare burden from hepatitis C in the United States. Liver Transpl. 2003;9:331–338
  14. Armstrong GL, Alter MJ, McQuillan GM, Margolis HS. The past incidence of hepatitis C virus infection: Implications for the future burden of chronic liver disease in the United States. Hepatology. 2000;31:777–782
  15. Deuffic S, Buffat L, Poynard T, Valleron AJ. Modeling the hepatitis C epidemic in France. Hepatology. 1999;29:1591–1601
  16. Wong JB, McQuillan GM, McHutchison JG, Poynard T. Estimating future hepatitis C morbidity, mortality and costs in the United States. Am J Public Health. 2000;90:1562–1569
  17. Yi Q, Yi Q, Wang PP, Krahn M. Improving the accuracy of long-term prognostic estimates in hepatitis C virus infection. J Viral Hepat. 2004;11:166–174
  18. Datz C, Cramp M, Haas T, et al. The natural course of hepatitis C virus infection 18 years after an epidemic outbreak of non-A, non-B hepatitis in a plasmapheresis centre. Gut. 1999;44:563–567
  19. Poynard T, Ratziu V, Charlotte F, et al. Rates and risk factors of liver fibrosis progression in persons with chronic hepatitis C. J Hepatology. 2001;34:730–739
  20. 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;167:743–750
  21. Cruts G, Buster M, Vincente J, et al. Estimating the total mortality among problem drug users. Subst Use Misuse. 2008;43:733–747
  22. Zarski JP, McHutchison JG, Bronowicki JP, et al. Rate of natural disease progression in persons with chronic hepatitis C. J Hepatology. 2003;38:207–314
  23. 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;48:418–431
  24. Pradat P, Voirin N, Tillmann HL, et al. Progression to cirrhosis in hepatitis C persons: an age-dependent process. Liver Int. 2007;27:335–339
  25. Wright M, Goldin R, Fabre A, et al. Measurement and determinants of the natural history of liver fibrosis in hepatitis C virus infection: a cross sectional and longitudinal study. Gut. 2003;52:574–579
  26. Ryder SD Trent Hepatitis C Study Group. Progression of hepatic fibrosis in persons with hepatitis C: a prospective repeat liver biopsy study. Gut. 2004;53:451–455
  27. Bruno S, Stroffolini T, Colombo M, et al. Sustained virological response to interferon-alpha is associated with improved outcome in HCV-related cirrhosis: a retrospective study. Hepatology. 2007;45:579–587
  28. Freeman AJ, Law MG, Kaldor JM, Dore GJ. Predicting progression to cirrhosis in chronic hepatitis C virus infection. J Viral Hepatol. 2003;10:285–293
  29. Fattovich G, Giustina G, Degos F, et al. Morbidity and mortality in compensated cirrhosis type C: a retrospective follow-up study of 384 persons. Gastroenterology. 1997;112:463–472
  30. Sangiovanni A, Prati GM, Fasani P, et al. The natural history of compensated cirrhosis due to hepatitis C virus: A 17-year cohort study of 214 persons. Hepatology. 2006;43:1303–1310
  31. Chiaramonte M, Stroffolini T, Vian A, et al. Rate of incidence of hepatocellular carcinoma in persons with compensated viral cirrhosis. Cancer. 1999;85:2132–2137
  32. Degos F, Christidis C, Ganne-Carrie N, et al. Hepatitis C virus related cirrhosis: time to occurrence of hepatocellular carcinoma and death. Gut. 2000;47:131–136
  33. Yoshida H, Tateishi R, Arakawa Y, et al. Benefit of interferon therapy in hepatocellular carcinoma prevention for individual persons with chronic hepatitis C. Gut. 2004;53:425–430
  34. El-Serag HB. Epidemiology of hepatocellular carcinoma in USA. Hepatol Res. 2007;37(Suppl 2):S88–S94
  35. Disease burden from hepatitis A, B and C in the United States. http://www.cdc.gove/hepatitis/PDFs/disease burden.pdfAccessed November 25, 2008
  36. Alter MJ, Margolis HS, Krawczynski K, et al. The natural history of community-acquired hepatitis C in the United States (The Sentinel Counties Chronic non-A, non-B Hepatitis Study Team). N Engl J Med. 1992;327:1899–1905
  37. Centers for Disease Control and Prevention. Mortality tables. http://www.cdc.gov/nchs/datawh/statab/unpubd/mortabs.htmAccessed July 26, 2008
  38. Franchini M, Rossetti G, Tagliaferri A, et al. The natural history of chronic hepatitis C in a cohort of HIV-negative Italian persons with hereditary bleeding disorders. Blood. 2001;98:1836–1841
  39. Kenny-Walsh E Irish Hepatology Research Group. Clinical outcomes after hepatitis C infection from contaminated anti-D immune globulin. N Engl J Med. 1999;340:1228–1233
  40. Levine RA, Sanderson SO, Ploutz-Snyder R, et al. Assessment of fibrosis progression in untreated Irish women with chronic hepatitis C contracted from immunoglobulin anti-D. Gastroenterol Hepatol. 2006;4:1271–1277
  41. Seeff LB, Miller RN, Rabkin CS, et al. 45-Year follow-up of hepatitis C virus infection in healthy young adults. Ann Intern Med 132:105−111.
  42. Seeff LB. Natural history of chronic hepatitis C. Hepatology. 2002;36(5 Suppl 1):S35–S46
  43. Di Bisceglie AM, Goodman ZD, Ishak KG, et al. Long-term clinical and histopathological follow-up of chronic posttransfusion hepatitis. Hepatology. 1991;14:969–974
  44. Farci P, Alter HJ, Shimoda A, et al. Hepatitis C virus associated fulminant hepatitic failure. N Engl J Med. 1996;335:631–634
  45. Yousuf M, Nakano Y, Sodeyama T, Kiyosawa K. Persistence of viremia in persons with type-C chronic hepatitis during long term follow-up. Scand J Gastroenterol. 1992;27:812–816
  46. El-Serag HB. Hepatocellular carcinoma and hepatitis C in the United States. Hepatology. 2002;36(5 Suppl 1):S74–S83
  47. El-Serag HB. Hepatocellular carcinoma: recent trends in the United States. Gastroenterology. 2004;127(5 Suppl 1):S27–S34
  48. Altekruse SF, McGlynn KA, Reichman ME. Hepatocellular carcinoma incidence, mortality, and survival trends in the United States from 1975 to 2005. J Clin Oncol. 2009;27:1485–1491
  49. Snowberger N, Chinnakotla S, Lepe RM, et al. Alpha fetoprotein, ultrasound, computerized tomography and magnetic resonance imaging for detection of hepatocellular carcinoma in persons with advanced cirrhosis. Aliment Pharmacol Ther. 2007;26:1187–1194
  50. Sersté T, Bourgeois N. Aging and the liver. Acta Gastroenterol Belg. 2006;69:296–298
  51. Ferenci P, Ferenci S, Datz C, et al. Morbidity and mortality in paid Austrian plasma donors infected with hepatitis C at plasma donation in the 1970s. J Hepatol. 2007;47:31–36
  52. Thabut D, Le Calvez S, Thibault V, et al. Hepatitis C in 6,865 persons 65 yr or older: a severe and neglected curable disease?. Am J Gastroenterol. 2006;101:1260–1267
  53. Mindikoglu AL, Miller RR. Hepatitis C in the elderly: epidemiology, natural history, and treatment. Clin Gastroenterol Hepatol. 2009;7:128–134
  54. D'Souza RD, Glynn MJ, Ushiro-Lumb I, et al. Prevalence of hepatitis C cirrhosis in elderly Asian patients infected during childhood. Clin Gastroenterol Hepatol. 2005;3:910–917
  55. Seeff LB, Everhart JE. Is cirrhosis an inevitable consequence of chronic hepatitis C virus infection?. Clin Gastroenterol Hepatol. 2005;3:840–842
  56. Davila JA, Morgan RO, Shaib Y, et al. Hepatitis C infection and the increasing incidence of hepatocellular carcinoma: a population-based study. Gastroenterology. 2004;127:1372–1380
  57. Kim WR, Poterucha JJ, Benson JT, Therneau TM. The impact of competing risks on the observed rate of chronic hepatitis C progression. Gastroenterology. 2004;127:749–755
  58. Missiha SB, Ostrowski M, Heathcote EJ. Disease progression in chronic hepatitis C: modifiable and nonmodifiable factors. Gastroenterology. 2008;134:1699–1714
  59. Hui JM, Sud A, Farrell GC, et al. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression. Gastroenterology. 2003;125:1695–1704
  60. El Serag HB, Hampel H, Javadi F. The association between diabetes and hepatocellular carcinoma: a systemic review of epidemiologic evidence. Clin Gastroenterol Hepatol. 2006;4:369–380
  61. Russmann S, Dowlatshahi EA, Printzen G, et al. Prevalence and associated factors of viral hepatitis and transferrin elevations in 5036 persons admitted to the emergency room of a Swiss university hospital: cross-sectional study. BMC Gastroenterol. 2007;7:5
  62. Irving WL, Smith S, Cater R, et al. Clinical pathways for persons with newly diagnosed hepatitis C - what actually happens. J Viral Hepat. 2006;13:264–271
  63. Morrill JA, Shrestha M, Grant RW. Barriers to the treatment of hepatitis C (Patient, provider, and system factors). J Gen Intern Med. 2005;20:754–758
  64. Shehab RM, Sonnad SS, Lok AS. Management of hepatitis C persons by primary care physicians in the USA: results of a national survey. J Viral Hepatol. 2003;98:639–644
  65. Fried MW, Shiffman ML, Reddy R, et al. Peg-interferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med. 2002;347:975–982
  66. Pawlotsky JM, Chevaliez S, McHutchison JG. The hepatitis C virus life cycle as a target for new antiviral therapies. Gastroenterology. 2007;132:1979–1998
  67. Veldt BJ, Heathcote EJ, Wedemeyer H, et al. Sustained virologic response and clinical outcomes in persons with chronic hepatitis C and advanced fibrosis. Ann Intern Med. 2007;147:677–684
  68. Alter MJ, Seeff LB, Bacon BR, et al. Testing for hepatitis C infection should be routine for persons at increased risk of infection. Ann Intern Med. 2004;141:715–717

 Conflicts of interest These authors disclose the following: Dr Davis received research funding from Human Genome Science, Merck, Novartis, Roche, Schering Plough, Tibotec, and Vertex Pharmaceuticals. Dr El-Serag received research funding from Schering-Plough and Bayer. Dr Poynard has a research grant from Schering Plough and equity share in BioPredictive. The remaining authors disclose no conflicts.

 Funding Sponsored by an unrestricted grant from Vertex Pharmaceutical Inc.

PII: S0016-5085(09)01885-X

doi: 10.1053/j.gastro.2009.09.067

Gastroenterology
Volume 138, Issue 2 , Pages 513-521.e6 , February 2010