Journal of Hepatology
Volume 52, Issue 2 , Pages 191-198 , February 2010

Prospective comparison of two algorithms combining non-invasive methods for staging liver fibrosis in chronic hepatitis C

  • Laurent Castéra

      Affiliations

    • Service d’Hépato-Gastroentérologie, Hôpital Haut-Lévêque, Centre Hospitalier Universitaire (C.H.U.) de Bordeaux, France
    • Service d’Hépato-Gastroentérologie, Hôpital Saint-André, C.H.U. de Bordeaux, France
    • Corresponding Author InformationCorresponding author. Address: Service d’Hépato-Gastroentérologie, Hôpital Haut-Lévêque, C.H.U. Bordeaux, Avenue Magellan, 33604 Pessac, France. Tel.: +33 5 57 65 64 39; fax: +33 5 57 65 64 45.
  • ,
  • Giada Sebastiani

      Affiliations

    • Venetian Institute of Molecular Medicine, Padova, Italy
  • ,
  • Brigitte Le Bail

      Affiliations

    • Service d’Anatomo-Pathologie, Hôpital Pellegrin, C.H.U. de Bordeaux, France
  • ,
  • Victor de Lédinghen

      Affiliations

    • Service d’Hépato-Gastroentérologie, Hôpital Haut-Lévêque, Centre Hospitalier Universitaire (C.H.U.) de Bordeaux, France
  • ,
  • Patrice Couzigou

      Affiliations

    • Service d’Hépato-Gastroentérologie, Hôpital Haut-Lévêque, Centre Hospitalier Universitaire (C.H.U.) de Bordeaux, France
  • ,
  • Alfredo Alberti

      Affiliations

    • Venetian Institute of Molecular Medicine, Padova, Italy

Received 29 May 2009 ,Revised 6 August 2009 ,Accepted 1 September 2009.

References 

  1. EASL International Consensus Conference on hepatitis C. Paris, 26–27 February 1999. Consensus statement. J Hepatol 1999;31(Suppl. 1):3–8.
  2. NIH Consensus Statement on Management of Hepatitis C: 2002. Hepatology 2002;36:S3–S20.
  3. Ghany MG, Strader DB, Thomas DL, Seeff LB. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology. 2008;49:1335–1374
  4. Cadranel JF, Rufat P, Degos F. Practices of liver biopsy in France: results of a prospective nationwide survey. For the Group of Epidemiology of the French Association for the Study of the Liver (AFEF). Hepatology. 2000;32:477–481
  5. Castera L, Negre I, Samii K, Buffet C. Pain experienced during percutaneous liver biopsy. Hepatology. 1999;30:1529–1530
  6. Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344:495–500
  7. Bedossa P, Dargère D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology. 2003;38:1449–1457
  8. Maharaj B, Maharaj RJ, Leary WP, Cooppan RM, Naran AD, Pirie D, et al. Sampling variability and its influence on the diagnostic yield of percutaneous needle biopsy of the liver. Lancet. 1986;1:523–525
  9. Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol. 2002;97:2614–2618
  10. Rousselet MC, Michalak S, Dupre F, Croue A, Bedossa P, Saint-Andre JP, et al. Sources of variability in histological scoring of chronic viral hepatitis. Hepatology. 2005;41:257–264
  11. Rockey DC, Bissell DM. Noninvasive measures of liver fibrosis. Hepatology. 2006;43(2 Suppl. 1):S113–S120
  12. Manning DS, Afdhal NH. Diagnosis and quantitation of fibrosis. Gastroenterology. 2008;134:1670–1681
  13. Pinzani M, Vizzutti F, Arena U, Marra F. Technology Insight: noninvasive assessment of liver fibrosis by biochemical scores and elastography. Nat Clin Pract Gastroenterol Hepatol. 2008;5:95–106
  14. Castera L. Transient elastography and other noninvasive tests to assess hepatic fibrosis in patients with viral hepatitis. J Viral Hepat. 2009;16:300–314
  15. Wai CT, Greenson JK, Fontana RJ, Kalbfleisch JD, Marrero JA, Conjeevaram HS, et al. A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C. Hepatology. 2003;38:518–526
  16. Imbert-Bismut F, Ratziu V, Pieroni L, Charlotte F, Benhamou Y, Poynard T. Biochemical markers of liver fibrosis in patients with hepatitis C virus infection: a prospective study. Lancet. 2001;357:1069–1075
  17. Castera L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128:343–350
  18. Ziol M, Handra-Luca A, Kettaneh A, Christidis C, Mal F, Kazemi F, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology. 2005;41:48–54
  19. Castera L, Denis J, Babany G, Roudot-Thoraval F. Evolving practices of non-invasive markers of liver fibrosis in patients with chronic hepatitis C in France. Time for new guidelines?. J Hepatol. 2007;46:528–529
  20. Friedrich-Rust M, Ong MF, Martens S, Sarrazin C, Bojunga J, Zeuzem S, et al. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology. 2008;134:960–974
  21. Halfon P, Munteanu M, Poynard T. FibroTest-ActiTest as a non-invasive marker of liver fibrosis. Gastroenterol Clin Biol. 2008;32(6 Suppl. 1):22–39
  22. Shaheen AA, Myers RP. Diagnostic accuracy of the aspartate aminotransferase-to-platelet ratio index for the prediction of hepatitis C-related fibrosis: a systematic review. Hepatology. 2007;46:912–921
  23. Non invasive methods for the evaluation of hepatic fibrosis/cirrhosis. Available from www.has-sante.fr; 2006.
  24. Sebastiani G, Vario A, Guido M, Noventa F, Plebani M, Pistis R, et al. Stepwise combination algorithms of non-invasive markers to diagnose significant fibrosis in chronic hepatitis C. J Hepatol. 2006;44:686–693
  25. Sebastiani G, Halfon P, Castera L, Pol S, Thomas DL, Mangia A, et al. SAFE biopsy: a validated method for large-scale staging of liver fibrosis in chronic hepatitis C. Hepatology. 2009;49:1821–1827
  26. Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29:1705–1713
  27. Castera L, Forns X, Alberti A. Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol. 2008;48:835–847
  28. Poynard T, Munteanu M, Imbert-Bismut F, Charlotte F, Thabut D, Le Calvez S, et al. Prospective Analysis of Discordant Results between Biochemical Markers and Biopsy in Patients with Chronic Hepatitis C. Clin Chem. 2004;10:10
  29. Intraobserver and interobserver variations in liver biopsy interpretation in patients with chronic hepatitis C. The French METAVIR Cooperative Study Group. Hepatology 1994;20:15–20.
  30. Poynard T, Halfon P, Castera L, Munteanu M, Imbert-Bismut F, Ratziu V, et al. Standardization of ROC curve areas for diagnostic evaluation of liver fibrosis markers based on prevalences of fibrosis stages. Clin Chem. 2007;53:1615–1622
  31. Hanley JA, McNeil BJ. A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology. 1983;148:839–843
  32. Sebastiani G, Alberti A. Non invasive fibrosis biomarkers reduce but not substitute the need for liver biopsy. World J Gastroenterol. 2006;12:3682–3694
  33. Leroy V, Hilleret MN, Sturm N, Trocme C, Renversez JC, Faure P, et al. Prospective comparison of six non-invasive scores for the diagnosis of liver fibrosis in chronic hepatitis C. J Hepatol. 2007;46:775–782
  34. Parkes J, Guha IN, Roderick P, Rosenberg W. Performance of serum marker panels for liver fibrosis in chronic hepatitis C. J Hepatol. 2006;44:462–474
  35. Bedossa P, Carrat F. Liver biopsy: the best, not the gold standard. J Hepatol. 2009;50:1–3
  36. Guido M, Rugge M. Liver biopsy sampling in chronic viral hepatitis. Semin Liver Dis. 2004;24:89–97
  37. Zeuzem S. Interferon-based therapy for chronic hepatitis C: current and future perspectives. Nat Clin Pract Gastroenterol Hepatol. 2008;5:610–622
  38. Sebastiani G, Vario A, Guido M, Alberti A. Performance of noninvasive markers for liver fibrosis is reduced in chronic hepatitis C with normal transaminases. J Viral Hepat. 2008;15:212–218
  39. Poynard T, Ingiliz P, Elkrief L, Munteanu M, Lebray P, Morra R, et al. Concordance in a world without a gold standard: a new non-invasive methodology for improving accuracy of fibrosis markers. PLoS ONE. 2008;3:e3857
  40. Fraquelli M, Rigamonti C, Casazza G, Conte D, Donato MF, Ronchi G, et al. Reproducibility of transient elastography in the evaluation of liver fibrosis in patients with chronic liver disease. Gut. 2007;56:968–973
  41. Imbert-Bismut F, Messous D, Thibaut V, Myers RB, Piton A, Thabut D, et al. Intra-laboratory analytical variability of biochemical markers of fibrosis (Fibrotest) and activity (Actitest) and reference ranges in healthy blood donors. Clin Chem Lab Med. 2004;42:323–333
  42. Piton A, Poynard T, Imbert-Bismut F, Khalil L, Delattre J, Pelissier E, et al. Factors associated with serum alanine transaminase activity in healthy subjects: consequences for the definition of normal values, for selection of blood donors, and for patients with chronic hepatitis C. MULTIVIRC Group. Hepatology. 1998;27:1213–1219
  43. Ngo Y, Munteanu M, Messous D, Charlotte F, Imbert-Bismut F, Thabut D, et al. A prospective analysis of the prognostic value of biomarkers (FibroTest) in patients with chronic hepatitis C. Clin Chem. 2006;52:1887–1896
  44. Foucher J, Chanteloup E, Vergniol J, Castera L, Le Bail B, Adhoute X, et al. Diagnosis of cirrhosis by transient elastography (FibroScan): a prospective study. Gut. 2006;55:403–408
  45. Carrion JA, Navasa M, Bosch J, Bruguera M, Gilabert R, Forns X. Transient elastography for diagnosis of advanced fibrosis and portal hypertension in patients with hepatitis C recurrence after liver transplantation. Liver Transpl. 2006;12:1791–1798
  46. Vizzutti F, Arena U, Romanelli RG, Rega L, Foschi M, Colagrande S, et al. Liver stiffness measurement predicts severe portal hypertension in patients with HCV-related cirrhosis. Hepatology. 2007;45:1290–1297
  47. Kazemi F, Kettaneh A, N’Kontchou G, Pinto E, Ganne-Carrie N, Trinchet JC, et al. Liver stiffness measurement selects patients with cirrhosis at risk of bearing large oesophageal varices. J Hepatol. 2006;45:230–235
  48. Castera L, Le Bail B, Roudot-Thoraval F, Bernard PH, Foucher J, Merrouche W, et al. Early detection in routine clinical practice of cirrhosis and oesophageal varices in chronic hepatitis C: comparison of transient elastography (FibroScan) with standard laboratory tests and non-invasive scores. J Hepatol. 2009;50:59–68
  49. Masuzaki R, Tateishi R, Yoshida H, Goto E, Sato T, Ohki T, et al. Prospective risk assessment for hepatocellular carcinoma development in patients with chronic hepatitis C by transient elastography. Hepatology. 2009;49:1954–1961
  50. Castera L. Liver stiffness and hepatocellular carcinoma: liaisons dangereuses?. Hepatology. 2009;49:1793–1794
  51. Arena U, Vizzutti F, Corti G, Ambu S, Stasi C, Bresci S, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology. 2008;47:380–384
  52. Coco B, Oliveri F, Maina AM, Ciccorossi P, Sacco R, Colombatto P, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat. 2007;14:360–369
  53. Sagir A, Erhardt A, Schmitt M, Haussinger D. Transient elastography is unreliable for detection of cirrhosis in patients with acute liver damage. Hepatology. 2007;47:592–595
  54. Foucher J, Castera L, Bernard PH, Adhoute X, Laharie D, Bertet J, et al. Prevalence and factors associated with failure of liver stiffness measurement using FibroScan in a prospective study of 2114 examinations. Eur J Gastroenterol Hepatol. 2006;18:411–412
  55. Bourliere M, Penaranda G, Renou C, Botta-Fridlund D, Tran A, Portal I, et al. Validation and comparison of indexes for fibrosis and cirrhosis prediction in chronic hepatitis C patients: proposal for a pragmatic approach classification without liver biopsies. J Viral Hepat. 2006;13:659–670
  56. Bourliere M, Penaranda G, Ouzan D, Renou C, Botta-Fridlund D, Tran A, et al. Optimized stepwise combination algorithms of non-invasive liver fibrosis scores including Hepascore in hepatitis C virus patients. Aliment Pharmacol Ther. 2008;28:458–467
  57. Sebastiani G, Alberti A. Implementing non-invasive markers for liver fibrosis in clinical practice. J Hepatol. 2008;48:880–881
  58. Sebastiani G, Halfon P, Castera L, Mangia A, Di Marco V, Pirisi M, et al. Large-scale multicenter comparison of three algorithms combining serum non-invasive markers for liver fibrosis in chronic hepatitis C (abstract). J Hepatol. 2008;48(Suppl. 2):S282

 Part of this work has been presented as oral presentation at the 58th Annual Meeting of the American Association for the Study of Liver Diseases (AASLD), Boston (USA), November 2–6, 2007.

PII: S0168-8278(09)00734-X

doi: 10.1016/j.jhep.2009.11.008

Journal of Hepatology
Volume 52, Issue 2 , Pages 191-198 , February 2010