Gastroenterology
Volume 127, Issue 6 , Pages 1704-1713 , December 2004

Serum markers detect the presence of liver fibrosis: A cohort study

  • William M.C. Rosenberg

      Affiliations

    • Liver Group, Division of Infection, Inflammation and Repair, University of Southampton, Southampton, England
    • Corresponding Author InformationAddress requests for reprints to: William M. C. Rosenberg, DPhil, FRCP, Liver Group, Division of Infection, Inflammation and Repair, University of Southampton, Mailpoint 811, Level D South Block, Southampton General Hospital, Tremona Road, Southampton, Hampshire, England, SO16 6YD; fax: (44) 023-8079-6968
  • ,
  • Michael Voelker

      Affiliations

    • Bayer HealthCare AG, Leverkusen, Germany
  • ,
  • Robert Thiel

      Affiliations

    • Thiel Statistical Consultants, Oxford, Connecticut
  • ,
  • Michael Becka

      Affiliations

    • Bayer HealthCare AG, Leverkusen, Germany
  • ,
  • Alastair Burt

      Affiliations

    • School of Clinical and Laboratory Sciences, University of Newcastle Upon Tyne, Newcastle Upon Tyne, England
  • ,
  • Detlef Schuppan

      Affiliations

    • Department of Medicine, University of Erlangen, Erlangen, Germany
  • ,
  • Stefan Hubscher

      Affiliations

    • Department of Pathology, University of Birmingham, Birmingham, England
  • ,
  • Tania Roskams

      Affiliations

    • Department of Pathology, University of Leuven, Leuven, Belgium
  • ,
  • Massimo Pinzani

      Affiliations

    • Department of Medicine, University of Florence, Florence, Italy
  • ,
  • Michael J.P. Arthur

      Affiliations

    • Liver Group, Division of Infection, Inflammation and Repair, University of Southampton, Southampton, England
  • ,
  • European Liver Fibrosis Group

Received 15 December 2003 ,Accepted 19 August 2004.

References 

  1. World Health Organization Mortality Statistics 1999. http://www3.who.int/whosis.
  2. Desmet V , Fevery J . Liver biopsy . Baillieres Clin Gastroenterol . 1995;9:811–828
  3. Scheuer PJ . Chronic hepatitis (what is activity and how should it be assessed?) . Histopathology . 1997;30:103–105
  4. Pasha T , Gabriel S , Therneau T , Dickson ER , Lindor KD . Cost-effectiveness of ultrasound-guided liver biopsy . Hepatology . 1998;27:1220–1226
  5. Gilmore IT , Burroughs A , Murray-Lyon IM , Williams R , Jenkins D , Hopkins A . Indications, methods, and outcomes of percutaneous liver biopsy in England and Wales (an audit by the British Society of Gastroenterology and the Royal College of Physicians of London) . Gut . 1995;36:437–441
  6. McGill DB , Rakela J , Zinsmeister AR , Ott BJ . A 21-year experience with major hemorrhage after percutaneous liver biopsy . Gastroenterology . 1990;99:1396–1400
  7. Sherlock S , Dooley J . Diseases of the liver and biliary system . 10th ed. London: Blackwell Scientific; 1997;
  8. 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
  9. Bedossa P , Dagere D , Paradis V . Sampling variability of liver fibrosis in chronic hepatitis C . Hepatology . 2003;38:1449–1457
  10. Colloredo G , Guido M , Sonozogni A , Leandro G . Impact of liver biopsy size on histological evaluation of chronic viral hepatitis (the smaller the sample, the milder the disease) . J Hepatol . 2003;39:239–244
  11. Theodossi A, Skene AM, Portmann B, Knill-Jones RP, Patrick RS, Tate RA, et al. Observer variation in assessment of liver biopsies including analysis by kappa statistics . Gastroenterology . 1980;79:232–241
  12. Scheuer PJ , Lefkowitch JH . Liver biopsy interpretation . 6th ed. London: WB Saunders; 2002;
  13. Yamauchi M , Mizuhara Y , Maezawa Y , Toda G . Serum tenascin levels in chronic liver disease . Liver . 1994;14:148–153
  14. McHutchison JG, Blatt LM, de Medina M, Craig JR, Conrad A, Schiff ER, et al. Measurement of serum hyaluronic acid in patients with chronic hepatitis C and its relationship to liver histology. Consensus Interferon Study Group . J Gastroenterol Hepatol . 2000;15:945–951
  15. Hayasaka A , Schuppan D , Ohnishi K , Okuda K , Hahn EG . Serum concentrations of the carboxyterminal cross-linking domain of procollagen type IV (NC1) and the aminoterminal propeptide of procollagen type III (PIIIP) in chronic liver disease . J Hepatol . 1990;10:17–22
  16. Schuppan D, Cantaluppi MC, Becker J, Veit A, Bunte T, Troyer D, et al. Undulin, an extracellular matrix glycoprotein associated with collagen fibrils . J Biol Chem . 1990;265:8823–8832
  17. Murawaki Y , Ikuta Y , Koda M , Kawasaki H . Serum type III procollagen peptide, type IV collagen 7S domain, central triple-helix of type IV collagen and tissue inhibitor of metalloproteinases in patients with chronic viral liver disease (relationship to liver histology) . Hepatology . 1994;20:780–787
  18. Kasahara A, Hayashi N, Mochizuki K, Oshita M, Katayama K, Kato M, et al. Circulating matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-1 as serum markers of fibrosis in patients with chronic hepatitis C. Relationship to interferon response . J Hepatol . 1997;26:574–583
  19. Murawaki Y , Ikuta Y , Okamoto K , Koda M , Kawasaki H . Serum matrix metalloproteinase-3 (stromelysin-1) concentration in patients with chronic liver disease . J Hepatol . 1999;31:474–481
  20. Trinchet JC . Clinical use of serum markers of fibrosis in chronic hepatitis . J Hepatol . 1995;22:89–95
  21. 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
  22. Castera L, Hartmann DJ, Chapel F, Guettier C, Mall F, Lons T, et al. Serum laminin and type IV collagen are accurate markers of histologically severe alcoholic hepatitis in patients with cirrhosis . J Hepatol . 2000;32:412–418
  23. Pilette C, Rousselet MC, Bedossa P, Chappard D, Oberti F, Rifflet H, et al. Histopathological evaluation of liver fibrosis: quantitative image analysis vs semi-quantitative scores. Comparison with serum markers . J Hepatol . 1998;28:439–446
  24. Guechot J , Laudat A , Loria A , Serfaty L , Poupon R , Giboudeau J . Diagnostic accuracy of hyaluronan and type III procollagen amino-terminal peptide serum assays as markers of liver fibrosis in chronic viral hepatitis C evaluated by ROC curve analysis . Clin Chem . 1996;42:558–563
  25. Murawaki Y , Ikuta Y , Koda M , Nishimura Y , Kawasaki H . Clinical significance of serum hyaluronan in patients with chronic viral liver disease . J Gastroenterol Hepatol . 1996;11:459–465
  26. Johansen JS, Christoffersen P, Moller S, Price PA, Henriksen JH, Garbarsch C, et al. Serum YKL-40 is increased in patients with hepatic fibrosis . J Hepatol . 2000;32:911–920
  27. Nojgaard C , Johansen JS , Christensen E , Skovgaard LT , Price PA , Becker U  The EMALD Group . Serum levels of YKL-40 and PIIINP as prognostic markers in patients with alcoholic liver disease . J Hepatol . 2003;39:179–186
  28. Nojgaard C , Johansen JS , Krarup HB , Holten-Andersen M , Moller A , Bendtsen F  Danish Viral Hepatitis Study Group . Effect of antiviral therapy on markers of fibrogenesis in patients with chronic hepatitis C . Scand J Gastroenterol . 2003;38:659–665
  29. Patel K, Lajoie A, Heaton S, Pianko S, Behling CA, Bylund D, et al. Clinical use of hyaluronic acid as a predictor of fibrosis change in hepatitis C . J Gastroenterol Hepatol . 2003;18:253–257
  30. Myers RP, Benhamou Y, Imbert-Bismut F, Thibault V, Bochet M, Charlotte F, et al. Serum biochemical markers accurately predict liver fibrosis in HIV and hepatitis C virus co-infected patients . AIDS . 2003;17:721–725
  31. Myers RP, Tainturier MH, Ratziu V, Piton A, Thibault V, Imbert-Bismut F, et al. Prediction of liver histological lesions with biochemical markers in patients with chronic hepatitis B . J Hepatol . 2003;39:222–230
  32. Forns X, Ampurdanes S, Llovet JM, Aponte J, Quinto L, Martinez-Bauer E, et al. Identification of chronic hepatitis C patients without hepatic fibrosis by a simple predictive model . Hepatology . 2002;36:986–992
  33. 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
  34. Scheuer PJ . Classification of chronic viral hepatitis (a need for reassessment) . J Hepatol . 1991;13:372–374
  35. Ishak K, Baptista A, Bianchi L, Callea F, De Groote J, Gudat F, et al  Histological grading and staging of chronic hepatitis . J Hepatol . 1995;22:696–699
  36. Arthur MJ . Reversibility of liver fibrosis and cirrhosis following treatment for hepatitis C . Gastroenterology . 2002;122:1525–1528
  37. Rosenberg WM . Rating fibrosis progression in chronic liver diseases . J Hepatol . 2003;38:357–360
  38. Scheuer PJ . Liver biopsy size matters in chronic hepatitis (bigger is better) . Hepatology . 2003;38:1356–1358
  39. Teli MR , James OF , Burt AD , Bennett MK , Day CP . The natural history of nonalcoholic fatty liver (a follow-up study) . Hepatology . 1995;22:1714–1719
  40. Rossi E, Adams L, Prins A, Bulsara M, de Boer B, Garas G, et al. Validation of the FibroTest biochemical markers score in assessing liver fibrosis in hepatitis C patients . Clin Chem . 2003;49:450–454
  41. Lichtinghagen R, Huegel O, Seifert T, Haberkorn CI, Michels D, Flemming P, et al. Expression of matrix metalloproteinase-2 and -9 and their inhibitors in peripheral blood cells of patients with chronic hepatitis C . Clin Chem . 2000;46:183–192
  42. Tran A, Benzaken S, Saint-Paul MC, Guzman-Granier E, Hastier P, Pradier C, et al. Chondrex (YKL-40), a potential new serum fibrosis marker in patients with alcoholic liver disease . Eur J Gastroenterol Hepatol . 2000;12:989–993
  43. Callewaert N , Vlierberghe HV , Hecke AV , Laroy W , Delanghe J , Contreras R . Noninvasive diagnosis of liver cirrhosis using DNA sequencer-based total serum protein glycomics . Nat Med . 2004;10:429–434
  44. Guyader D, Jacquelinet C, Moirand R, Turlin B, Mendler MH, Chaperon J, et al. Noninvasive prediction of fibrosis in C282Y homozygous hemochromatosis . Gastroenterology . 1998;115:929–936
  45. Beaton M , Guyader D , Deugnier Y , Moirand R , Chakrabarti S , Adams P . Noninvasive prediction of cirrhosis in C282Y-linked hemochromatosis . Hepatology . 2002;36:673–678

 Supported by Bayer Healthcare AG (Leverkusen, Germany). This study is an investigator-initiated study funded by Bayer AG. M.B. and M.V. are employees of Bayer HealthCare AG. R.T. is an independent statistical analyst engaged by Bayer HealthCare AG. A.B., S.H., and T.R. received grant support from Bayer AG.

PII: S0016-5085(04)01553-7

doi: 10.1053/j.gastro.2004.08.052

Gastroenterology
Volume 127, Issue 6 , Pages 1704-1713 , December 2004