Duarte-Rojo A, Altamirano JT, Feld JJ

Language: English
References: 101
Page: 426-439
PDF size: 185.77 Kb.

ABSTRACT

Noninvasive markers of fibrosis have emerged as an alternative to the staging of fibrosis by means of liver biopsy. Apart from being noninvasive and thus lacking the adverse effects of liver biopsy, they offer some advantages such as reduced risk of sampling error, objectiveness in the interpretation of the result, appropriateness for repeated measurements and lower cost. Many studies have validated different panels of blood markers and imaging/transient elastography for the estimation of fibrosis with acceptable accuracy. Clinical scenarios leading to inacurate or failed estimation must be acknowledged, as well as the fact that performance of blood markers and transient elastography, and their diagnostic cut-off values vary among specific liver diseases. The combination of two blood markers or of a blood marker and transient elastography has been shown to increase accuracy of the estimation. Further, unlike liver biopsy the noninvasive markers of fibrosis are not associated with a ceiling effect after cirrhosis is identified, but can discriminate early from advanced stages of cirrhosis. Longitudinal studies have shown their utility as predictors of complications from portal hypertension and mortality, outperforming liver biopsy. In conclusion, noninvasive markers of fibrosis provide major advantages over liver biopsy. The reported performance of some of the available tests -particularly when used in combination- make them a reliable tool, very attractive for daily clinical practice.

REFERENCES

1. Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD, American Association for the Study of Liver Diseases. Liver biopsy. Hepatology 2009; 49: 1017-44.

2. Goodman ZD. Grading and staging systems for inflammation and fibrosis in chronic liver diseases. J Hepatol 2007; 47: 598-607.

3. Cholongitas E, Senzolo M, Standish R, et al. A systematic review of the quality of liver biopsy specimens. Am J Clin Pathol 2006; 125: 710-21.

4. Colloredo G, Guido M, Sonzogni 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: 239-44.

5. Garcia-Tsao G, Friedman S, Iredale J, Pinzani M. Now there are many (stages) where before there was one: In search of a pathophysiological classification of cirrhosis. Hepatology 2010; 51: 1445-9.

6. Germani G, Hytiroglou P, Fotiadu A, Burroughs AK, Dhillon AP. Assessment of fibrosis and cirrhosis in liver biopsies: an update. Semin Liver Dis 2011; 31: 82-90.

7. Calčs P, Oberti F, Michalak S, et al. A novel panel of blood markers to assess the degree of liver fibrosis. Hepatology 2005; 42: 1373-81.

8. Mallet V, Dhalluin-Venier V, Roussin C, et al. The accuracy of the FIB-4 index for the diagnosis of mild fibrosis in chronic hepatitis B. Aliment Pharmacol Ther 2009; 29: 409-15.

9. Idobe Y, Murawaki Y, Ikuta Y, Koda M, Kawasaki H. Post-prandial serum hyaluronan concentration in patients with chronic liver disease. Intern Med 1998; 37: 568-75.

10. Lin ZH, Xin YN, Dong QJ, et al. Performance of the aspartate aminotransferase-to-platelet ratio index for the staging of hepatitis C-related fibrosis: an updated meta-analysis. Hepatology 2011; 53: 726-36.

11. Stibbe KJ, Verveer C, Francke J, et al. Comparison of noninvasive assessment to diagnose liver fibrosis in chronic hepatitis B and C patients. Scand J Gastroenterol 2011; 46: 962-72.

12. Sterling RK, Lissen E, Clumeck N, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology 2006; 43: 1317-25.

13. Vallet-Pichard A, Mallet V, Nalpas B, et al. FIB-4: an inexpensive and accurate marker of fibrosis in HCV infection. Comparison with liver biopsy and fibrotest. Hepatology 2007; 46: 32-6.

14. Kim BK, Kim DY, Park JY, et al. Validation of FIB-4 and comparison with other simple noninvasive indices for predicting liver fibrosis and cirrhosis in hepatitis B virus-infected patients. Liver Int 2010; 30: 546-53.

15. Koda M, Matunaga Y, Kawakami M, Kishimoto Y, Suou T, Murawaki Y. FibroIndex, a practical index for predicting significant fibrosis in patients with chronic hepatitis C. Hepatology 2007; 45: 297-306.

16. Forns X, Ampurdančs S, Llovet JM, et al. Identification of chronic hepatitis C patients without hepatic fibrosis by a simple predictive model. Hepatology 2002; 36: 986-92.

17. Siagris D, Christofidou M, Theocharis GJ, et al. Serum lipid pattern in chronic hepatitis C: histological and virological correlations. J Viral Hepat 2006; 13: 56-61.

18. Kim BK, Kim SA, Park YN, et al. Noninvasive models to predict liver cirrhosis in patients with chronic hepatitis B. Liver Int 2007; 27: 969-76.

19. Rosenberg WM, Voelker M, Thiel R, et al. Serum markers detect the presence of liver fibrosis: a cohort study. Gastroenterology 2004; 127: 1704-13.

20. Parkes J, Guha IN, Roderick P, et al. Enhanced Liver Fibrosis (ELF) test accurately identifies liver fibrosis in patients with chronic hepatitis C. J Viral Hepat 2011; 18: 23-31.

21. Kawser CA, Iredale JP, Winwood PJ, Arthur MJ. Rat hepatic stellate cell expression of alpha2-macroglobulin is a feature of cellular activation: implications for matrix remodelling in hepatic fibrosis. Clin Sci (Lond) 1998; 95: 179-86.

22. Patel K, Gordon SC, Jacobson I, et al. Evaluation of a panel of non-invasive serum markers to differentiate mild from moderate-to-advanced liver fibrosis in chronic hepatitis C patients. J Hepatol 2004; 41: 935-42.

23. Patel K, Nelson DR, Rockey DC, et al. Correlation of FIBROSpect II with histologic and morphometric evaluation of liver fibrosis in chronic hepatitis C. Clin Gastroenterol Hepatol 2008; 6: 242-7.

24. Adams LA, Bulsara M, Rossi E, et al. Hepascore: an accurate validated predictor of liver fibrosis in chronic hepatitis C infection. Clin Chem 2005; 51: 1867-73.

25. Degos F, Perez P, Roche B, et al. Diagnostic accuracy of FibroScan and comparison to liver fibrosis biomarkers in chronic viral hepatitis: a multicenter prospective study (the FIBROSTIC study). J Hepatol 2010; 53: 1013-21.

26. Poynard T, de Ledinghen V, Zarski JP, et al. FibroTest(®) and Fibroscan(®) performances revisited in patients with chronic hepatitis C. Impact of the spectrum effect and the applicability rate. Clin Res Hepatol Gastroenterol 2011 [epub ahead of print].

27. Halfon P, Munteanu M, Poynard T. FibroTest-ActiTest as a non-invasive marker of liver fibrosis. Gastroenterol Clin Biol 2008; 32: 22-39.

28. Leroy V, Halfon P, Bacq Y, et al. Diagnostic accuracy, reproducibility and robustness of fibrosis blood tests in chronic hepatitis C: a meta-analysis with individual data. Clin Biochem 2008; 41: 1368-76.

29. Poynard T, Ngo Y, Munteanu M, Thabut D, Ratziu V. Noninvasive Markers of Hepatic Fibrosis in Chronic Hepatitis B. Curr Hepat Rep 2011; 10: 87-97.

30. Guha IN, Myers RP, Patel K, Talwalkar JA. Biomarkers of liver fibrosis: What lies beneath the receiver operating characteristic curve? Hepatology 2011; 54: 1454-62.

31. Zarski JP, Sturm N, Guechot J, et al. Comparison of nine blood tests and transient elastography for liver fibrosis in chronic hepatitis C: The ANRS HCEP-23 study. J Hepatol 2011 [epub ahead of print].

32. Bataller R, Rombouts K, Altamirano J, Marra F. Fibrosis in alcoholic and nonalcoholic steatohepatitis. Best Pract Res Clin Gastroenterol 2011; 25: 231-44.

33. Poynard T, Aubert A, Bedossa P, et al. A simple biological index for detection of alcoholic liver disease in drinkers. Gastroenterology 1991; 100: 1397-402.

34. Naveau S, Poynard T, Benattar C, Bedossa P, Chaput JC. Alpha-2-macroglobulin and hepatic fibrosis. Diagnostic interest. Dig Dis Sci 1994; 39: 2426-32.

35. Naveau S, Gaudé G, Asnacios A, et al. Diagnostic and prognostic values of noninvasive biomarkers of fibrosis in patients with alcoholic liver disease. Hepatology 2009; 49: 97-105.

36. Janssens F, de Suray N, Piessevaux H, Horsmans Y, de Timary P, Stärkel P. Can transient elastography replace liver histology for determination of advanced fibrosis in alcoholic patients: a real-life study. J Clin Gastroenterol 2010; 44: 575-82.

37. Naveau S, Raynard B, Ratziu V, et al. Biomarkers for the prediction of liver fibrosis in patients with chronic alcoholic liver disease. Clin Gastroenterol Hepatol 2005; 3: 167-74.

38. Lavallard VJ, Bonnafous S, Patouraux S, et al. Serum markers of hepatocyte death and apoptosis are non invasive biomarkers of severe fibrosis in patients with alcoholic liver disease. PLoS One 2011; 6: 17599.

39. Angulo P, Hui JM, Marchesini G, et al. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology 2007; 45: 846-54.

40. Harrison SA, Oliver D, Arnold HL, Gogia S, Neuschwander- Tetri BA. Development and validation of a simple NAFLD clinical scoring system for identifying patients without advanced disease. Gut 2008; 57: 1441-7.

41. Ratziu V, Massard J, Charlotte F, et al. Diagnostic value of biochemical markers (FibroTest-FibroSURE) for the prediction of liver fibrosis in patients with non-alcoholic fatty liver disease. BMC Gastroenterol 2006; 6: 6.

42. Calčs P, Lainé F, Boursier J, et al. Comparison of blood tests for liver fibrosis specific or not to NAFLD. J Hepatol 2009; 50: 165-73.

43. Guha IN, Parkes J, Roderick P, et al. Noninvasive markers of fibrosis in nonalcoholic fatty liver disease: Validating the European Liver Fibrosis Panel and exploring simple markers. Hepatology 2008; 47: 455-60.

44. Shah AG, Lydecker A, Murray K, et al. Comparison of noninvasive markers of fibrosis in patients with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 2009; 7: 1104-12.

45. Adams LA, George J, Bugianesi E, et al. Complex non-invasive fibrosis models are more accurate than simple models in non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2011; 26: 1536-43.

46. Loaeza-del-Castillo A, Paz-Pineda F, Oviedo-Cardenas E, et al. AST to platelet ratio index (APRI) for the noninvasive evaluation of liver fibrosis. Ann Hepatol 2008; 7: 350-7.

47. Floreani A, Cazzagon N, Martines D, Cavalletto L, Baldo V, Chemello L. Performance and utility of transient elastography and noninvasive markers of liver fibrosis in primary biliary cirrhosis. Dig Liver Dis 2011; 43: 887-92.

48. Friedrich-Rust M, Müller C, Winckler A, et al. Assessment of liver fibrosis and steatosis in PBC with FibroScan, MRI, MR-spectroscopy, and serum markers. J Clin Gastroenterol 2010; 44: 58-65.

49. Castera L, Forns X, Alberti A. Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol 2008; 48: 835-47.

50. 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: 968-73.

51. Lucidarme D, Foucher J, Le Bail B, et al. Factors of accuracy of transient elastography (fibroscan) for the diagnosis of liver fibrosis in chronic hepatitis C. Hepatology 2009; 49: 1083-9.

52. Castéra L, Foucher J, Bernard PH, et al. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology 2010; 51: 828-35.

53. Myers RP, Pomier-Layrargues G, Kirsch R, et al. Feasibility and diagnostic performance of the fibroscan xl probe for liver stiffness measurement in overweight and obese patients. Hepatology 2012; 54: 199-208.

54. Myers RP, Pomier-Layrargues G, Kirsch R, et al. Discordance in fibrosis staging between liver biopsy and transient elastography using the fibroscan XL probe. J Hepatol 2012 [epub ahead of print].

55. Tsochatzis EA, Gurusamy KS, Ntaoula S, Cholongitas E, Davidson BR, Burroughs AK. Elastography for the diagnosis of severity of fibrosis in chronic liver disease: a meta-analysis of diagnostic accuracy. J Hepatol 2011; 54: 650-9.

56. Castéra L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterol 2005; 128: 343-50.

57. Ziol M, Handra-Luca A, Kettaneh A, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology 2005; 41: 48-54.

58. Marcellin P, Ziol M, Bedossa P, et al. Non-invasive assessment of liver fibrosis by stiffness measurement in patients with chronic hepatitis B. Liver Int 2009; 29: 242-7.

59. Coco B, Oliveri F, Maina AM, et al. Transient elastography: a new surrogate marker of liver fibrosis influenced by major changes of transaminases. J Viral Hepat 2007; 14: 360-9.

60. Arena U, Vizzutti F, Corti G, et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology 2008; 47: 380-4.

61. Kim SU, Kim do Y, Park JY, et al. How can we enhance the performance of liver stiffness measurement using FibroScan in diagnosing liver cirrhosis in patients with chronic hepatitis B? J Clin Gastroenterol 2010; 44: 66-71.

62. Chan HL, Wong GL, Choi PC, et al. Alanine aminotransferase- based algorithms of liver stiffness measurement by transient elastography (Fibroscan) for liver fibrosis in chronic hepatitis B. J Viral Hepat 2009; 16: 36-44.

63. Lupsor M, Badea R, Stefănescu H, et al. Analysis of histopathological changes that influence liver stiffness in chronic hepatitis C. Results from a cohort of 324 patients. J Gastrointestin Liver Dis 2008; 17: 155-63.

64. Wong VW, Vergniol J, Wong GL, et al. Diagnosis of fibrosis and cirrhosis using liver stiffness measurement in nonalcoholic fatty liver disease. Hepatology 2010; 51: 454-62.

65. Nguyen-Khac E, Chatelain D, Tramier B, et al. Assessment of asymptomatic liver fibrosis in alcoholic patients using fibroscan: prospective comparison with seven non-invasive laboratory tests. Aliment Pharmacol Ther 2008; 28: 1188-98.

66. Nahon P, Kettaneh A, Tengher-Barna I, et al. Assessment of liver fibrosis using transient elastography in patients with alcoholic liver disease. J Hepatol 2008; 49: 1062-8.

67. Yoneda M, Mawatari H, Fujita K, et al. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with nonalcoholic fatty liver disease (NAFLD). Dig Liver Dis 2008; 40: 371-8.

68. Mueller S, Millonig G, Sarovska L, et al. Increased liver stiffness in alcoholic liver disease: differentiating fibrosis from steatohepatitis. World J Gastroenterol 2010; 16: 966-72.

69. Corpechot C, El Naggar A, Poujol-Robert A, et al. Assessment of biliary fibrosis by transient elastography in patients with PBC and PSC. Hepatology 2006; 43: 1118-24.

70. Yin M, Talwalkar JA, Glaser KJ, et al. Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 2007; 5: 1207-13.

71. Huwart L, Sempoux C, Vicaut E, et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 2008; 135: 32-40.

72. Wang Y, Ganger DR, Levitsky J, et al. Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. AJR Am J Roentgenol 2011; 196: 553-61.

73. Friedrich-Rust M, Romen D, Vermehren J, et al. Acoustic radiation force impulse-imaging and transient elastography for non-invasive assessment of liver fibrosis and steatosis in NAFLD. Eur J Radiol 2011 [in press].

74. Friedrich-Rust M, Wunder K, Friener S, et al. Liver fibrosis in viral hepatitis: noninvasive assessment with acoustic radiation force impulse imaging versus transient elastography. Radiology 2009; 252: 595-604.

75. Ebinuma H, Saito H, Komuta M, et al. Evaluation of liver fibrosis by transient elastography using acoustic radiation force impulse: comparison with Fibroscan(®). J Gastroenterol 2011; 46: 1238-48.

76. Palmeri ML, Wang MH, Rouze NC, et al. Noninvasive evaluation of hepatic fibrosis using acoustic radiation forcebased shear stiffness in patients with nonalcoholic fatty liver disease. J Hepatol 2011; 55: 666-72.

77. Rizzo L, Calvaruso V, Cacopardo B, et al. Comparison of transient elastography and acoustic radiation force impulse for non-invasive staging of liver fibrosis in patients with chronic hepatitis c. Am J Gastroenterol 2011; 106: 2112-20.

78. Bourličre M, Pénaranda G, Adhoute X, Oules V, Castellani P. Combining non-invasive methods for assessment of liver fibrosis. Gastroenterol Clin Biol 2008; 32: 73-9.

79. Castéra L, Sebastiani G, Le Bail B, de Lédinghen V, Couzigou P, Alberti A. Prospective comparison of two algorithms combining non-invasive methods for staging liver fibrosis in chronic hepatitis C. J Hepatol 2010; 52: 191-8.

80. Boursier J, de Ledinghen V, Zarski JP, et al. Comparison of eight diagnostic algorithms for liver fibrosis in hepatitis C: new algorithms are more precise and entirely noninvasive. Hepatology 2011; 55: 58-67.

81. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of hepatitis C virus infection. J Hepatol 2011s; 55: 245-64.

82. Poynard T, Imbert-Bismut F, Ratziu V, et al. Biochemical markers of liver fibrosis in patients infected by hepatitis C virus: longitudinal validation in a randomized trial. J Viral Hepat 2002; 9: 128-33.

83. Patel K, Benhamou Y, Yoshida EM, et al. An independent and prospective comparison of two commercial fibrosis marker panels (HCV FibroSURE and FIBROSpect II) during albinterferon alfa-2b combination therapy for chronic hepatitis C. J Viral Hepat 2009; 16: 178-86.

84. Vergniol J, Foucher J, Castéra L, et al. Changes of non-invasive markers and FibroScan values during HCV treatment. J Viral Hepat 2009; 16: 132-40.

85. Martinez SM, Fernández-Varo G, González P, et al. Assessment of liver fibrosis before and after antiviral therapy by different serum marker panels in patients with chronic hepatitis C. Aliment Pharmacol Ther 2011; 33: 138-48.

86. Poynard T, Munteanu M, Colombo M, et al. FibroTest is an independent predictor of virologic response in chronic hepatitis C patients retreated with pegylated interferon alfa-2b and ribavirin in the EPIC3 program. J Hepatol 2011; 54: 227-35.

87. Hézode C, Castéra L, Roudot-Thoraval F, et al. Liver stiffness diminishes with antiviral response in chronic hepatitis C. Aliment Pharmacol Ther 2011; 34: 656-63.

88. Ogawa E, Furusyo N, Toyoda K, Takeoka H, Maeda S, Hayashi J. The longitudinal quantitative assessment by transient elastography of chronic hepatitis C patients treated with pegylated interferon alpha-2b and ribavirin. Antiviral Res 2009; 83: 127-34.

89. van der Meer, Veldt BJ, Feld JJ, et al. Improved platelet count and smaller spleen size long after sustained virological response in chronic hepatitis c patients with advanced fibrosis. Hepatology 2011; 54(Suppl.): 820A.

90. Enomoto M, Mori M, Ogawa T, et al. Usefulness of transient elastography for assessment of liver fibrosis in chronic hepatitis B: Regression of liver stiffness during entecavir therapy. Hepatol Res 2010; 40: 853-61.

91. Bureau C, Metivier S, Peron JM, et al. Transient elastography accurately predicts presence of significant portal hypertension in patients with chronic liver disease. Aliment Pharmacol Ther 2008; 27: 1261-8.

92. Robic MA, Procopet B, Métivier S, et al. Liver stiffness accurately predicts portal hypertension related complications in patients with chronic liver disease: A prospective study. J Hepatol 2011; 55: 1017-25.

93. Hirooka M, Ochi H, Koizumi Y, et al. Splenic elasticity measured with real-time tissue elastography is a marker of portal hypertension. Radiology 2011; 261: 960-8.

94. Talwalkar JA, Yin M, Venkatesh S, et al. Feasibility of in vivo MR elastographic splenic stiffness measurements in the assessment of portal hypertension. AJR Am J Roentgenol 2009; 193: 122-7.

95. Stefanescu H, Grigorescu M, Lupsor M, Procopet B, Maniu A, Badea R. Spleen stiffness measurement using fibroscan for the noninvasive assessment of esophageal varices in liver cirrhosis patients. J Gastroenterol Hepatol 2011; 26: 164-70.

96. Fung J, Lai CL, Seto WK, Wong DK, Yuen MF. Prognostic significance of liver stiffness for hepatocellular carcinoma and mortality in HBeAg-negative chronic hepatitis B. J Viral Hepat 2011; 18: 738-44.

97. Thabut D, Imbert-Bismut F, Cazals-Hatem D, et al. Relationship between the Fibrotest and portal hypertension in patients with liver disease. Aliment Pharmacol Ther 2007; 26: 359-68.

98. Ngo Y, Munteanu M, Messous D, et al. A prospective analysis of the prognostic value of biomarkers (FibroTest) in patients with chronic hepatitis C. Clin Chem 2006; 52: 1887-96.

99. Ngo Y, Benhamou Y, Thibault V, et al. An accurate definition of the status of inactive hepatitis B virus carrier by a combination of biomarkers (FibroTest-ActiTest) and viral load. PLoS One 2008; 3: 2573.

100. 100.Mayo MJ, Parkes J, Adams-Huet B, et al. Prediction of clinical outcomes in primary biliary cirrhosis by serum enhanced liver fibrosis assay. Hepatology 2008; 48: 1549-57.

101. 101.Vergniol J, Foucher J, Terrebonne E, et al. Noninvasive tests for fibrosis and liver stiffness predict 5-year outcomes of patients with chronic hepatitis C.