Role of Liver Biopsy in the Era of Direct-Acting Antivirals

An accurate assessment of the degree of fibrosis or presence of cirrhosis is critical both for the appropriate management of, and to provide prognosis for, patients with chronic hepatitis C infection. In the new era of direct acting antivirals, large numbers of patients may enter therapy, and although liver biopsy remains the gold standard, it is not practical in all settings. In recent years, a variety of noninvasive methods have been developed that may obviate the need for liver biopsy in most settings. Indirect laboratory formulas, tests, panels of biomarkers and imaging modalities may accurately stage the degree of fibrosis in hepatitis C monoinfection, hepatitis C/HIV coinfection, and post-transplant recurrent hepatitis C.

[1]  Josh Levitsky,et al.  Magnetic Resonance Elastography and Biomarkers to Assess Fibrosis From Recurrent Hepatitis C in Liver Transplant Recipients , 2011, Transplantation.

[2]  F. Carrat,et al.  Comparison of non-invasive liver fibrosis biomarkers in HIV/HCV co-infected patients: the fibrovic study--ANRS HC02. , 2008, Journal of hepatology.

[3]  F. Carrat,et al.  Comparison of liver fibrosis blood tests developed for HCV with new specific tests in HIV/HCV co-infection. , 2010, Journal of hepatology.

[4]  G. Casazza,et al.  Etiology-related determinants of liver stiffness values in chronic viral hepatitis B or C. , 2011, Journal of hepatology.

[5]  M. Shiffman,et al.  Peginterferon alfa-2a in patients with chronic hepatitis C and cirrhosis. , 2000, The New England journal of medicine.

[6]  D. Thabut,et al.  Overview of the diagnostic value of biochemical markers of liver fibrosis (FibroTest, HCV FibroSure) and necrosis (ActiTest) in patients with chronic hepatitis C , 2004, Comparative hepatology.

[7]  Neil Kaplowitz,et al.  Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis , 1981, Hepatology.

[8]  M. Ghany,et al.  Diagnosis, management, and treatment of hepatitis C: An update , 2009, Hepatology.

[9]  P. Bedossa,et al.  Diagnostic accuracy of FibroScan and comparison to liver fibrosis biomarkers in chronic viral hepatitis: a multicenter prospective study (the FIBROSTIC study). , 2010, Journal of hepatology.

[10]  E. Schiff,et al.  Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection , 2002, American Journal of Gastroenterology.

[11]  J. Montaner,et al.  Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection , 2006, Hepatology.

[12]  V. Mazzaferro,et al.  Prevention of recurrent hepatitis C after liver transplantation with early interferon and ribavirin treatment. , 2001, Transplantation proceedings.

[13]  I. Chiang,et al.  Effects of patient factors on noninvasive liver stiffness measurement using acoustic radiation force impulse elastography in patients with chronic hepatitis C , 2012, BMC Gastroenterology.

[14]  B. Bacon,et al.  Levels of alanine aminotransferase confound use of transient elastography to diagnose fibrosis in patients with chronic hepatitis C virus infection. , 2012, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[15]  Y. Baruch,et al.  Prevalence and Characteristics of Pain Induced by Percutaneous Liver Biopsy , 2003, Anesthesia and analgesia.

[16]  Llorenç Quintó,et al.  Identification of chronic hepatitis C patients without hepatic fibrosis by a simple predictive model , 2002, Hepatology.

[17]  Laurent Castera,et al.  How to assess liver fibrosis in chronic hepatitis C: serum markers or transient elastography vs. liver biopsy? , 2011, Liver international : official journal of the International Association for the Study of the Liver.

[18]  N. Afdhal,et al.  Editorial: Staging Liver Fibrosis in Hepatitis C: A Challenge for This Decade , 2011, The American Journal of Gastroenterology.

[19]  Edward A Belongia,et al.  National Institutes of Health Consensus Development Conference Statement: management of hepatitis B. , 2009, Annals of internal medicine.

[20]  Valeer J Desmet,et al.  Knodell RG, Ishak KG, Black WC, Chen TS, Craig R, Kaplowitz N, Kiernan TW, Wollman J. Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis [Hepatology 1981;1:431-435]. , 2003, Journal of hepatology.

[21]  S. Ahn,et al.  Normal liver elasticity values using acoustic radiation force impulse imaging: A prospective study in healthy living liver and kidney donors , 2012, Journal of gastroenterology and hepatology.

[22]  A. Act Noninvasive tests for liver disease, fibrosis, and cirrhosis: Is liver biopsy obsolete? , 2010 .

[23]  N. Afdhal Noninvasive Markers of Liver Fibrosis. , 2006, Gastroenterology & hepatology.

[24]  M. Attanasio,et al.  Comparison of Transient Elastography and Acoustic Radiation Force Impulse for Non-Invasive Staging of Liver Fibrosis in Patients With Chronic Hepatitis C , 2011, The American Journal of Gastroenterology.

[25]  C. Renou,et al.  External validation of FibroIndex , 2007, Hepatology.

[26]  R. Myers,et al.  Diagnostic accuracy of the aspartate aminotransferase‐to‐platelet ratio index for the prediction of hepatitis C–related fibrosis: A systematic review , 2007, Hepatology.

[27]  Gunda Millonig,et al.  Extrahepatic cholestasis increases liver stiffness (FibroScan) irrespective of fibrosis , 2008, Hepatology.

[28]  Ying Sun,et al.  Performance of the aspartate aminotransferase‐to‐platelet ratio index for the staging of hepatitis C‐related fibrosis: An updated meta‐analysis , 2011, Hepatology.

[29]  A. Manduca,et al.  Assessment of hepatic fibrosis with magnetic resonance elastography. , 2007, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[30]  R. Myers,et al.  FibroTest and FibroScan for the Prediction of Hepatitis C-Related Fibrosis: A Systematic Review of Diagnostic Test Accuracy , 2007, The American Journal of Gastroenterology.

[31]  E. Collisson,et al.  A 10-Year Experience of Liver Transplantation for Hepatitis C: Analysis of Factors Determining Outcome in Over 500 Patients , 2001, Annals of surgery.

[32]  V. de Lédinghen,et al.  Pitfalls of liver stiffness measurement: A 5‐year prospective study of 13,369 examinations , 2010, Hepatology.

[33]  U. Neumann,et al.  Chances and limitations of non‐invasive tests in the assessment of liver fibrosis in liver transplant patients , 2010, Clinical transplantation.

[34]  G. Hunault,et al.  FibroMeters: a family of blood tests for liver fibrosis. , 2008, Gastroenterologie clinique et biologique.

[35]  M. Makuuchi,et al.  Preemptive Therapy for Hepatitis C Virus after Living-Donor Liver Transplantation , 2004, Transplantation.

[36]  P. Bedossa,et al.  Intraobserver and Interobserver Variations in Liver Biopsy Interpretation in Patients with Chronic Hepatitis C , 1994 .

[37]  C. Katlama,et al.  Serum biochemical markers accurately predict liver fibrosis in HIV and hepatitis C virus co-infected patients , 2003, AIDS.

[38]  S. Zeuzem,et al.  Chronic hepatitis C in patients with persistently normal alanine transaminase levels. , 2006, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[39]  Enrico Rossi,et al.  Validation of the FibroTest biochemical markers score in assessing liver fibrosis in hepatitis C patients. , 2003, Clinical chemistry.

[40]  J. Kench,et al.  Hepascore: an accurate validated predictor of liver fibrosis in chronic hepatitis C infection. , 2005, Clinical chemistry.

[41]  T. Poynard,et al.  Biochemical markers of liver fibrosis in patients with hepatitis C virus infection: a prospective study , 2001, The Lancet.

[42]  J. Borovička,et al.  HCV‐related advanced fibrosis/cirrhosis: randomized controlled trial of pegylated interferon α‐2a and ribavirin , 2006, Journal of viral hepatitis.

[43]  U. Neumann,et al.  Long-term outcome of liver transplants for chronic hepatitis C: a 10-year follow-up , 2004, Transplantation.

[44]  A. Duarte-Rojo,et al.   Noninvasive markers of fibrosis: key concepts for improving accuracy in daily clinical practice. , 2012, Annals of hepatology.

[45]  G. Gerken,et al.  Assessment of Allograft Fibrosis by Transient Elastography and Noninvasive Biomarker Scoring Systems in Liver Transplant Patients , 2010, Transplantation.

[46]  D. Gretch,et al.  Use of the AST to platelet ratio index in HCV/HIV co‐infected patients , 2011, Alimentary pharmacology & therapeutics.

[47]  C. Dietrich,et al.  13C‐methacetin breath test as liver function test in patients with chronic hepatitis C virus infection , 2005, Alimentary pharmacology & therapeutics.

[48]  F. Roudot-thoraval,et al.  Guidelines for the diagnosis of uncomplicated cirrhosis. , 2007, Gastroenterologie clinique et biologique.

[49]  M. Ghany,et al.  An Update on Treatment of Genotype 1 Chronic Hepatitis C Virus Infection: 2011 Practice Guideline by the American Association for the Study of Liver Diseases , 2011, Hepatology.

[50]  C. Avellini,et al.  Role of AST to platelet ratio index in the detection of liver fibrosis in patients with recurrent hepatitis C after liver transplantation , 2007, Journal of gastroenterology and hepatology.

[51]  O. Pappo,et al.  A continuous 13C methacetin breath test for noninvasive assessment of intrahepatic inflammation and fibrosis in patients with chronic HCV infection and normal ALT , 2008, Journal of viral hepatitis.

[52]  J. Kalbfleisch,et al.  A simple noninvasive index can predict both significant fibrosis and cirrhosis in patients with chronic hepatitis C , 2003, Hepatology.

[53]  S. Pol,et al.  FIB‐4: An inexpensive and accurate marker of fibrosis in HCV infection. comparison with liver biopsy and fibrotest , 2007, Hepatology.

[54]  A. Sanyal,et al.  A prospective evaluation of fibrosis progression in patients with recurrent hepatitis C virus following liver transplantation , 2007, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[55]  M. Yaran,et al.  Validation of Hepascore as a Predictor of Liver Fibrosis in Patients with Chronic Hepatitis C Infection , 2011, Hepatitis research and treatment.

[56]  Patrice Faure,et al.  Prospective comparison of six non-invasive scores for the diagnosis of liver fibrosis in chronic hepatitis C. , 2007, Journal of hepatology.

[57]  K. Ishak,et al.  Histological grading and staging of chronic hepatitis. , 1995 .

[58]  C. Féray Fibrosis progression after liver transplantation in patients with recurrent hepatitis C. , 2004, Journal of hepatology.

[59]  Richard D Moore,et al.  Assessment of liver fibrosis by transient elastography in persons with hepatitis C virus infection or HIV-hepatitis C virus coinfection. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[60]  Hirokazu Takahashi,et al.  Evaluation of acoustic radiation force impulse elastography for fibrosis staging of chronic liver disease: a pilot study , 2010, Liver international : official journal of the International Association for the Study of the Liver.

[61]  G. Menghini One-second needle biopsy of the liver. , 1958, Gastroenterology.

[62]  A. Burroughs,et al.  Noninvasive tests for evaluation of fibrosis in HCV recurrence after liver transplantation: a systematic review , 2010, Transplant international : official journal of the European Society for Organ Transplantation.

[63]  Eva Herrmann,et al.  Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. , 2008, Gastroenterology.

[64]  Ralph Sinkus,et al.  Magnetic resonance elastography for the noninvasive staging of liver fibrosis. , 2008, Gastroenterology.

[65]  W. Kim,et al.  Ultrasound‐based transient elastography for the detection of hepatic fibrosis in patients with recurrent hepatitis C virus after liver transplantation: A systematic review and meta‐analysis , 2012, Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society.

[66]  M. Manns,et al.  Clinical feasibility of liver elastography by acoustic radiation force impulse imaging (ARFI). , 2011, Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver.

[67]  A. Baranova,et al.  Non-Invasive markers for hepatic fibrosis , 2011, BMC gastroenterology.

[68]  G. Verset,et al.  The predictive value of FIB‐4 versus FibroTest, APRI, FibroIndex and Forns index to noninvasively estimate fibrosis in hepatitis C and nonhepatitis C liver diseases , 2008, Hepatology.

[69]  Yukihiro Kishimoto,et al.  Fibroindex, a practical index for predicting significant fibrosis in patients with chronic hepatitis C , 2007, Hepatology.

[70]  R. Nelson,et al.  Liver biopsy , 2009, Hepatology.

[71]  R. Sterling,et al.  Comparison of FIB-4 and APRI in HIV–HCV Coinfected Patients with Normal and Elevated ALT , 2011, Digestive Diseases and Sciences.

[72]  M. El-Raziky,et al.  Can aspartate aminotransferase to platelet ratio index replace liver biopsy in chronic hepatitis C? , 2011, Tropical gastroenterology : official journal of the Digestive Diseases Foundation.

[73]  N. Afdhal,et al.  Validation of hepascore, compared with simple indices of fibrosis, in patients with chronic hepatitis C virus infection in United States. , 2009, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.