Gastroenterology
Volume 136, Issue 5 , Pages 1629-1638 , May 2009

A 28-Year Study of the Course of Hepatitis Δ Infection: A Risk Factor for Cirrhosis and Hepatocellular Carcinoma

  • Raffaella Romeo

      Affiliations

    • A. M. Migliavacca Center, First Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy
    • Corresponding Author InformationReprint requests Address requests for reprints to: Raffaella Romeo, MD, PhD, First Division of Gastroenterology, IRCCS Maggiore Hospital, Pad. Granelli, Via F. Sforza, 35, 20122 Milan, Italy
    • ,
  • Ersilio Del Ninno

      Affiliations

    • A. M. Migliavacca Center, First Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy
    • ,
  • Mariagrazia Rumi

      Affiliations

    • A. M. Migliavacca Center, First Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy
    • ,
  • Antonio Russo

      Affiliations

    • Unit of Epidemiology and Medical Statistics, San Carlo Borromeo Hospital of Milan, Milan, Italy
    • ,
  • Angelo Sangiovanni

      Affiliations

    • A. M. Migliavacca Center, First Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy
    • ,
  • Roberto de Franchis

      Affiliations

    • Third Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy
    • ,
  • Guido Ronchi

      Affiliations

    • A. M. Migliavacca Center, First Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy
    • ,
  • Massimo Colombo

      Affiliations

    • A. M. Migliavacca Center, First Division of Gastroenterology, IRCCS Maggiore Hospital, University of Milan, Milan, Italy

Received 29 July 2008 ,Accepted 19 January 2009.

References 

  1. Rizzetto M, Canese M, Aricò S. Immunofluorescence detection of a new antigen antibody system (Δ/anti-Δ) associated to hepatitis B virus in liver and serum of HBsAg carriers. Gut. 1977;18:997–1003
  2. Smedile A, Rizzetto M, Gerin JL. Advances in hepatitis D virus biology and disease. In:  Boyer JL,  Okner RK editor. Progress in liver disease, Vol 12. Philadelphia: WB Saunders; 1994;p. 157–175
  3. Smedile A, Niro MG, Rizzetto M. Hepatitis D virus. In:  Richmann DD,  Whitley RJ,  Hayden FG editor. Clinical virology. New York: Churchill Livingstone; 1997;p. 1237–1284
  4. Hoofnagle JH. Type D (Δ) heptitis. JAMA. 1989;262:2995–2996
  5. Gaeta GB, Stroffolini T, Chiaramonte M, et al. Chronic hepatitis D: a vanishing disease? (An Italian multicenter study). Hepatology. 2000;32:824–827
  6. Margolis HS, Alter MJ, Hadler SC. Hepatitis B: evolving epidemiology and implications for control. Semin Liver Dis. 1991;11:84–92
  7. D'Amelio R, Matricardi PM, Biselli R, et al. Changing epidemiology of hepatitis B in Italy: public health implications. Am J Epidemiol. 1992;135:1012–1018
  8. Rosina F, Conoscitore P, Cuppone R, et al. Changing pattern of chronic hepatitis D in southern Europe. Gastroenterology. 1999;117:161–166
  9. Flodgren E, Bengtsson S, Knutsson M, et al. Recent high incidence of fulminant hepatitis in Samara, Russia: molecular analysis of prevailing hepatitis B and D virus strains. J Clin Microbiol. 2000;38:3311–3316
  10. Khan A, Kurbanov F, Tanaka Y, et al. Epidemiological and clinical evaluation of hepatitis B, hepatitis C, and Δ hepatitis viruses in Tajikistan. J Med Virol. 2008;80:268–276
  11. Gaeta GB, Stroffolini T, Smedile A, et al. Hepatitis Δ in Europe: vanishing or refreshing?. Hepatology. 2007;46:1312–1313
  12. Wedemeyer H, Heindrich B, Manns MP. Hepatitis D virus infection—not a vanishing disease in Europe!. Hepatology. 2007;45:1331–1332
  13. Cross TJS, Rizzi P, Horner M, et al. The increasing prevalence of hepatitis Δ virus (HDV) infection in South London. J Med Virol. 2008;80:277–282
  14. Wu JC, Chen TZ, Huang YS, et al. Natural history of hepatitis D viral superinfection: significance of viremia detected by polymerase chain reaction. Gastroenterology. 1995;108:796–802
  15. Taylor JM. Structure and replication of hepatitis Δ virus. Semin Virol. 1990;1:135–141
  16. Yamashiro T, Nagayama K, Enomoto N, et al. Quantitation of the level of hepatitis Δ virus RNA in serum, by real-time polymerase chain reaction and its possible correlation with the clinical stage of liver disease. J Infect Dis. 2004;189:1151–1157
  17. Farci P, Roskams T, Chessa L, et al. Long-term benefit of interferon α therapy of chronic hepatitis D: regression of advanced hepatic fibrosis. Gastroenterology. 2004;126:1740–1749
  18. Yurdaydin C. Δ Hepatitis. In:  Buti M,  Esteban R editor. BC) VH Viral hepatitis. Madrid: AG Rupem S. Coop; 2008;p. 157–168
  19. Rosina F, Pintus C, Meschievitz C, et al. A randomized controlled trial of a 12-month course of recombinant human interferon-α in chronic Δ (type D) hepatitis: a multicenter study. Hepatology. 1991;13:1052–1053
  20. Farci P, Mandas A, Coiana A, et al. Treatment of chronic hepatitis D with interferon alfa-2a. N Engl J Med. 1994;330:88–94
  21. Colombo M, Cambieri R, Rumi MG, et al. Long-term Δ superinfection in hepatitis B surface antigen carriers and its relationship to the course of chronic hepatitis. Gastroenterology. 1983;85:235–239
  22. Niro GA, Smedile S, Andriulli A, et al. The predominance of hepatitis Δ virus genotype I among chronically infected Italian patients. Hepatology. 1997;25:728–734
  23. Brunetto MR, Cerenzia MT, Olivieri F, et al. Monitoring the natural course and response to therapy of chronic hepatitis B with an automated semi-quantitative assay for IgM anti-HBc. J Hepatol. 1993;19:431–436
  24. Scotto J, Hadchouel M, Hery C, et al. Detection of hepatitis B virus DNA in serum by a single spot hybridization technique: comparison with results for other viral markers. Hepatology. 1983;3:279–283
  25. The French METAVIR Cooperative Study Group. Intraobserver and interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C. Hepatology. 1994;20:15–20
  26. Fraquelli M, Rigamonti C, Casazza G, et al. Reproducibility of transient elastography in the evaluation of liver fibrosis in patients with chronic liver disease. Gut. 2007;56:968–973
  27. Pugh RN, Murray-Lyon IM, Dawson JL, et al. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg. 1973;60:646–649
  28. Colombo M, de Franchis R, Del Ninno E, et al. Hepatocellular carcinoma in Italian patients with cirrhosis. N Engl J Med. 1991;325:675–680
  29. Bruix J, Sherman M, Llovet JM, et al. Clinical management of hepatocellular carcinoma (Conclusions of the Barcelona EASL Conference). J Hepatol. 2001;35:421–430
  30. Peters RL. Pathology of hepatocellular carcinoma. In:  Okuda K,  Peters RL editor. Hepatocellular carcinoma. New York: John Wiley; 1976;p. 107–168
  31. Portal hypertension III. In:  de Franchis R editors. Proceedings of Third Baveno International Consensus Workshop on Definition, Methodology and Therapeutic Strategies. London: Blackwell Science; 2001;p. 1–247
  32. Salerno F, Angeli P, Bernardi M, et al. Clinical practice guidelines for the management of cirrhotic patients with ascites (Committee on Ascites of the Italian Association for the Study of the Liver). Ital J Gastroenterol Hepatol. 1999;7:626–634
  33. 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 patients. Hepatology. 2006;43:1303–1310
  34. Benvegnù L, Gios M, Boccato S, et al. Natural history of compensated viral cirrhosis: a prospective study on the incidence and hierarchy of major complications. Gut. 2004;53:744–749
  35. Rizzetto M, Verme G, Recchia S, et al. Chronic hepatitis in carriers of hepatitis B surface antigen, with intrahepatic expression of the Δ antigen (An active and progressive disease unresponsive to immunosuppressive treatment). Ann Intern Med. 1983;98:437–441
  36. Yang A, Papaioannou C, Hadziyannis S, et al. Base changes at position 1014 and 578 of Δ virus RNA in Greek isolates maintain base pair in rod conformation with efficient RNA editing. J Med Virol. 1995;47:113–119
  37. Fattovich G, Giustina G, Christensen E, et al. Influence of hepatitis delta virus infection on morbidity and mortality in compensated cirrhosis type B. Gut. 2000;46:420–426
  38. Hadziyannis SJ. Hepatitis Δ: an overview. In:  Rizzetto M,  Purcell RH,  Gerin JL, et al. editor. Viral hepatitis and liver disease. Torino: Minerva Medica; 1997;p. 283–289
  39. Chen CJ, Yang HI, Su J, et al. Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA. 2006;295:65–73
  40. Iloeje UH, Yang HI, Su J, et al. Predicting cirrhosis risk based on the level of circulating hepatitis B viral load. Gastroenterology. 2006;130:678–686
  41. Lau DT-Y, Doo E, Park Y, et al. Lamivudine for chronic Δ hepatitis. Hepatology. 1999;30:546–549
  42. Battegay M, Simpson LH, Hoofnagle JH, et al. Elimination of hepatitis Δ virus infection after loss of hepatitis B surface antigen in patients with chronic Δ hepatitis. J Med Virol. 1994;44:389–392
  43. Pollicino T, Squadrito G, Cerenzia G, et al. Hepatitis B virus maintains its pro-oncogenic properties in the case of occult HBV infection. Gastroenterology. 2004;126:102–110
  44. Yuen MF, Wong DK, Fung J, et al. HBsAg seroclearance in chronic hepatitis B Asian patients: replicative level and risk of hepatocellular carcinoma. Gastroenterology. 2008;135:1192–1199

 Conflicts of interest The authors disclose the following: M. Colombo is advisor and served as a speaker bureau for Roche, Schering Plough, Glaxo Smith Kline, and Gilead. The remaining authors disclose no conflicts.

 Funding Supported by a grant from University of Milan (“First Project”) and a grant from Fondazione IRCCS Maggiore Hospital Mangiagalli and Regina Elena (“Ricerca Corrente 2008”).

PII: S0016-5085(09)00154-1

doi: 10.1053/j.gastro.2009.01.052

Gastroenterology
Volume 136, Issue 5 , Pages 1629-1638 , May 2009

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