Non-invasive markers for hepatic fibrosis

Ancha Baranova, Priyanka Lal, Aybike Birerdinc, Zobair M Younossi, Ancha Baranova, Priyanka Lal, Aybike Birerdinc, Zobair M Younossi

Abstract

With great advancements in the therapeutic modalities used for the treatment of chronic liver diseases, the accurate assessment of liver fibrosis is a vital need for successful individualized management of disease activity in patients. The lack of accurate, reproducible and easily applied methods for fibrosis assessment has been the major limitation in both the clinical management and for research in liver diseases. However, the problem of the development of biomarkers capable of non-invasive staging of fibrosis in the liver is difficult due to the fact that the process of fibrogenesis is a component of the normal healing response to injury, invasion by pathogens, and many other etiologic factors. Current non-invasive methods range from serum biomarker assays to advanced imaging techniques such as transient elastography and magnetic resonance imaging (MRI). Among non-invasive methods that gain strongest clinical foothold are FibroScan elastometry and serum-based APRI and FibroTest. There are many other tests that are not yet widely validated, but are none the less, promising. The rate of adoption of non-invasive diagnostic tests for liver fibrosis differs from country to country, but remains limited. At the present time, use of non-invasive procedures could be recommended as pre-screening that may allow physicians to narrow down the patients' population before definitive testing of liver fibrosis by biopsy of the liver. This review provides a systematic overview of these techniques, as well as both direct and indirect biomarkers based approaches used to stage fibrosis and covers recent developments in this rapidly advancing area.

Figures

Figure 1
Figure 1
A scheme depicting various means of liver fibrosis diagnostics. Liver biopsy is an invasive method that remains an imperfect golden standard. Proteomics based profiles are unlikely to be introduced to routine clinical care anytime soon, but are valuable from the research point of view. Imaging techniques, serum biomarkers and biomarker panels are advancing along the route to the clinic stage, but require extensive validation.
Figure 2
Figure 2
Decision tree that may help to guide the cost-effective diagnosis of liver fibrosis in large populations of prospective patients.

References

    1. Schiff ER, Lee SS, Chao YC, Kew-Yoon S, Bessone F, Wu SS, Kryczka W, Lurie Y, Gadano A, Kitis G, Beebe S, Xu D, Tang H, Iloeje U. Long-term treatment with entecavir induces reversal of advanced fibrosis or cirrhosis in patients with chronic hepatitis B. Clin Gastroenterol Hepatol. 2010. in press .
    1. Chang TT, Liaw YF, Wu SS, Schiff E, Han KH, Lai CL, Safadi R, Lee SS, Halota W, Goodman Z, Chi YC, Zhang H, Hindes R, Iloeje U, Beebe S, Kreter B. Long-term entecavir therapy results in the reversal of fibrosis/cirrhosis and continued histological improvement in patients with chronic hepatitis B. Hepatology. 2010;52(3):886–893. doi: 10.1002/hep.23785.
    1. Rygiel KA, Robertson H, Marshall HL, Pekalski M, Zhao L, Booth TA, Jones DE, Burt AD, Kirby JA. Epithelial-mesenchymal transition contributes to portal tract fibrogenesis during human chronic liver disease. Lab Invest. 2008;88:112–123. doi: 10.1038/labinvest.3700704.
    1. Brenner DA. Molecular pathogenesis of liver fibrosis. Transactions of the American Clinical and Climatological Association. 2009;120:361–368.
    1. Malhi H, Guicciardi ME, Gregory J, Gores GJ. Hepatocyte death: a clear and present danger. Physiol Rev. 2010;90:1165–1194. doi: 10.1152/physrev.00061.2009.
    1. Roberts RA, Ganey PE, Ju C, Kamendulis LM, Rusyn I, Klaunig JE. Role of the Kupffer Cell in Mediating Hepatic Toxicity and Carcinogenesis. Toxicological Sciences. 2006;96(1):2–7. doi: 10.1093/toxsci/kfl173. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev. 2008, 88(1): 125-172.
    1. Jiao J, Friedman SL, Aloman C. Hepatic fibrosis. Curr Opin Gastroenterol. 2009;25(3):223–229. doi: 10.1097/MOG.0b013e3283279668.
    1. Bataller R, Brenner DA. Liver Fibrosis. The Journal of Clinical Investigation. 2005;115(2):209–218.
    1. Fontana L, Jerez D, Rojas-Valencia L, Solis-Herruzo JA, Greenwel P, Rojkind M. Ethanol induces the expression of alpha1(I) procollagen mRNA in a co-culture system containing a liver stellate cell-line and freshly isolated hepatocytes. Biochim Biophys Acta. 1997;1362:135–144.
    1. Purohit V, Brenner DA. Mechanisms of Alcohol-Induced Hepatic Fibrosis: A Summary of the Ron Thurman Symposium. Hepatology. 2006;43(4):872–878. doi: 10.1002/hep.21107.
    1. Bertolani C, Marra F. The role of adipokines in liver fibrosis. Pathophysiology. 2008;15:91–101. doi: 10.1016/j.pathophys.2008.05.001.
    1. Diehl AM. Nonalcoholic steatosis and steatohepatitis, Nonalcoholic fatty liver disease abnormalities in macrophage function and cytokines. Am J Physiol Gastrointest Liver Physiol. 2002;282:G1–G5.
    1. Rahmouni K, Haynes WG. Endothelial effects of leptin: implications in health and diseases. Curr Diab Rep. 2005;5:260–266. doi: 10.1007/s11892-005-0020-5.
    1. Bertolani C, Sancho-Bru P, Failli P, Bataller R, Aleffi S, DeFranco R, Mazzinghi B, Romagnani P, Milani S, Gines P, Colmenero J, Parola M, Gelmini S, Tarquini R, Laffi G, Pinzani M, Marra F. Resistin as an intrahepatic cytokine: overexpression during chronic injury and induction of proinflammatory actions in hepatic stellate cells. Am J Pathol. 2006;169:2042–2053. doi: 10.2353/ajpath.2006.060081.
    1. Glaser SS, Gaudio E, Miller T, Alvaro D, Alpini G. Cholangiocyte proliferation and liver fibrosis. Expert Rev Mol Med. 2009;25; 11:e7.
    1. Bataller R, Yang L, Brenner DA. A dual reporter gene transgenic mouse demonstrates heterogeneity in hepatic fibrogenic cell populations. Hepatology. 2004;40:1151–1159. doi: 10.1002/hep.20427.
    1. Martin-Vílchez S, Sanz-Cameno P, Rodriguez-Munoz Y, Majano PL, Molina-Jimenez F, Lopez-Cabrera M, Moreno-Otero R, Lara-Pezzi E. The hepatitis B virus X protein induces paracrine activation of human hepatic stellate cells. Hepatology. 2008;47(6):1872–1883. doi: 10.1002/hep.22265.
    1. Lin W, Wu G, Li S, Weinberg EM, Kumthip K, Peng LF, Mendez-Navarro J, Chen WC, Jilg N, Zhao H, Goto K, Zhang L, Brockman MA, Schuppan D, Chung RT. HIV and HCV cooperatively promote hepatic fibrogenesis via induction of reactive oxygen species and NF{kappa}B. J Biol Chem. 2010. in press .
    1. Sebastiani G, Alberti A. Non invasive fibrosis biomarkers reduce but not substitute the need for liver biopsy. World J Gastroenterol. 2006;12(23):3682–3694.
    1. West J, Card TR. Reduced mortality rates following elective percutaneous liver biopsies. Gastroenterology. 2010;139(4):1230–7. doi: 10.1053/j.gastro.2010.06.015. Epub 2010 Jun 12.
    1. Terjung B, Lemnitzer I, Dumoulin FL, Effenberger W, Brackmann HH, Sauerbruch T, Spengler U. Bleeding complications after percutaneous liver biopsy. An analysis of risk factors. Digestion. 2003;67(3):138–45.
    1. 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. doi: 10.1002/hep.1840010511.
    1. Standish RA, Cholongitas E, Dhillon A, Burroughs AK, Dhillon AP. An appraisal of the histopathological assessment of liver fibrosis. Gut. 2006;55:569–578. doi: 10.1136/gut.2005.084475.
    1. Scheuer PJ. Classification of chronic viral hepatitis: a need for reassessment. Journal of Hepatology. 1991;13:372–4. doi: 10.1016/0168-8278(91)90084-O.
    1. Desmet V J, Gerber M, Hoofnagle JH. et al.Classification of chronic hepatitis: Diagnosis, grading and staging. Hepatology. 1994;19:1513–20. doi: 10.1002/hep.1840190629.
    1. Ratnakar KS, Sudha S. Image analysis in the evaluation of chronic hepatitis. Bahrain Medical Bulletin. 2001.
    1. Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996;24(2):289–293.
    1. Poynard T, Hepatitis B, Hepatitis C. A Martin Dunitz Book. 1. Taylor & Francis, United Kingdom; 2002. management and treatment.
    1. Franciscus A. HCV Diagnostic tools: Grading and staging a liver biopsy. HCSP; 2010. Version 2.4.
    1. Poynard T, Ratziu V, Benmanov Y, Martino VD, Bedossa P, Opolon P. Fibrosis in patients with hepatitis C: Detection and significance. Semin Liver Dis. 2000;20(1):0047–0056. doi: 10.1055/s-2000-9258.
    1. Bedossa P, Carrat F. Liver fibrosis: screening is not staging. J Hepatol. 2009;50(6):1268–1269. doi: 10.1016/j.jhep.2009.02.011.
    1. Bondini S, Kleiner DE, Goodman ZD, Gramlich T, Younossi ZM. Pathologic assessment of non-alcoholic fatty liver disease. Clin Liver Dis. 2007;11(1):17–23. doi: 10.1016/j.cld.2007.02.002. vii.
    1. Poynard T, Halfon P, Castera L, Munteanu M, Imbert-Bismut F, Ratziu V, Benhamou Y, Bourlière M, de Ledinghen V. FibroPaca Group. Standardization of ROC curve areas for diagnostic evaluation of liver fibrosis markers based on prevalences of fibrosis stages. Clin Chem. 2007;53(9):1615–22. doi: 10.1373/clinchem.2007.085795.
    1. Bedossa P, Dargère D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology. 2003;38(6):1449–57.
    1. Ziol M, Handra-Luca A, Kettaneh A, Christidis C, Mal F, Kazemi F, de Lédinghen V, Marcellin P, Dhumeaux D, Trinchet JC, Beaugrand M. Noninvasive assessment of liver fibrosis by measurement of stiffness in patients with chronic hepatitis C. Hepatology. 2005;41(1):48–54. doi: 10.1002/hep.20506.
    1. Friedrich-Rust M, Ong MF, Martens S, Sarrazin C, Bojunga J, Zeuzem S, Herrmann E. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology. 2008;134(4):960–74. doi: 10.1053/j.gastro.2008.01.034.
    1. Degos F, Perez P, Roche B, Mahmoudi A, Asselineau J, Voitot H, Bedossa P. FIBROSTIC study group. 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(6):1013–21. doi: 10.1016/j.jhep.2010.05.035.
    1. Fraquelli M, Rigamonti C, Casazza G, Donato MF, Ronchi G, Conte D, Rumi M, Lampertico P, Colombo M. Etiology-related determinants of liver stiffness values in chronic viral hepatitis B or C. J Hepatol. 2011;54(4):621–8. doi: 10.1016/j.jhep.2010.07.017.
    1. Castéra L, Vergniol J, Foucher J, Le Bail B, Chanteloup E, Haaser M, Darriet M, Couzigou P, De Lédinghen V. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology. 2005;128(2):343–50. doi: 10.1053/j.gastro.2004.11.018.
    1. Castéra L, Foucher J, Bernard PH, Carvalho F, Allaix D, Merrouche W, Couzigou P, de Lédinghen V. Pitfalls of liver stiffness measurement: a 5-year prospective study of 13,369 examinations. Hepatology. 2010;51(3):828–35.
    1. Manning DS, Afdhal NH. Diagnosis and quantitation of fibrosis. Gastroenterology 2008, 134. Gastroenterology. 2008;134(6):1670–1681. doi: 10.1053/j.gastro.2008.03.001.
    1. Talwalkar JA. Antifibrotic therapies--emerging biomarkers as treatment end points. Nat Rev Gastroenterol Hepatol. 2010;7(1):59–61. doi: 10.1038/nrgastro.2009.197.
    1. Takahashi H, Ono N, Eguchi Y, Eguchi T, Kitajima Y, Kawaguchi Y, Nakashita S, Ozaki I, Mizuta T, Toda S, Kudo S, Miyoshi A, Miyazaki K, Fujimoto K. Evaluation of acoustic radiation force impulse elastography for fibrosis staging of chronic liver disease: a pilot study. Liver Int. 2010;30(4):538–45. doi: 10.1111/j.1478-3231.2009.02130.x.
    1. Yoneda M, Suzuki K, Kato S, Fujita K, Nozaki Y, Hosono K, Saito S, Nakajima A. Nonalcoholic fatty liver disease: US-based acoustic radiation force impulse lastography. Radiology. 2010;256(2):640–7. doi: 10.1148/radiol.10091662.
    1. Rifai K, Cornberg J, Mederacke I, Bahr MJ, Wedemeyer H, Malinski P, Bantel H, Boozari B, Potthoff A, Manns MP, Gebel M. Clinical feasibility of liver elastography by acoustic radiation force impulse imaging (ARFI) Dig Liver Dis. 2011.
    1. Kuroda H, Kakisaka K, Tatemichi Y, Sawara K, Miyamoto Y, Oikawa K, Miyasaka A, Takikawa Y, Masuda T, Suzuki K. Non-invasive evaluation of liver fibrosis using acoustic radiation force impulse imaging in chronic hepatitis patients with hepatitis C virus infection. Hepatogastroenterology. 2010;57(102-103):1203–7.
    1. Taouli B, Ehman RL, Reeder SB. Advanced MRI methods for assessment of chronic liver disease. AJR. 2009;193:14–27. doi: 10.2214/AJR.09.2601.
    1. Rouviere O, Yin M, Dresner MA, Rossman PJ, Burgart LJ, Fidler JL, Ehman RL. MR elastography of the liver: preliminary results. Radiology. 2006;240(2):440–448. doi: 10.1148/radiol.2402050606.
    1. Yin M, Talwalkar JA, Glaser KJ, Manduca A, Grimm RC, Rossman PJ, Fidler JL, Ehman RL, Yin, M. Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol. 2007;5:1207–1213. doi: 10.1016/j.cgh.2007.06.012.
    1. Huwart L, Sempoux C, Vicaut E, Salameh N, Annet L, Danse E, Peeters F, ter Beek LC, Rahier J, Sinkus R, Horsmans Y, Van Beers BE. Magnetic resonance elastography for the non invasive staging of liver fibrosis. Gastroenterology. 2008;135(1):32–40. doi: 10.1053/j.gastro.2008.03.076.
    1. Zhou K, Lu LG. Assessment of fibrosis in chronic liver diseases. Journal of Digestive Diseases. 2009;10(1):7–14. doi: 10.1111/j.1751-2980.2008.00356.x.
    1. Park SH, Kim CH, Kim DJ, Suk KT, Cheong JY, Cho SW, Hwang SG, Lee YJ, Cho M, Yang JM, Kim YB. Usefulness of multiple biomarkers for the prediction of significant fibrosis in chronic hepatitis B. J Clin Gastroenterol. 2011;45(4):361–5. doi: 10.1097/MCG.0b013e31820d3458.
    1. Grigorescu M. Noninvasive Biochemical Markers of Liver Fibrosis. J Gastrointestin Liver Dis. 2006;15(2):149–159.
    1. Gressner OA, Weiskirchen R, Gressner AM. Biomarkers of liver fibrosis: clinical translation of molecular pathogenesis or based on liver dependent malfunction tests. Clin Chim Acta. 2007;381:107–113. doi: 10.1016/j.cca.2007.02.038.
    1. Veidal SS, Vassiliadis E, Bay-Jensen AC, Tougas G, Vainer B, Karsdal MA. Procollagen type I N-terminal propeptide (PINP) is a marker for fibrogenesis in bile duct ligation-induced fibrosis in rats. Fibrogenesis Tissue Repair. 2010;3(1):5. doi: 10.1186/1755-1536-3-5.
    1. Lieber CS, Weiss DG, Paronetto F. Veterans Affairs Cooperative Study 391 Group. Value of fibrosis markers for staging liver fibrosis in patients with precirrhotic alcoholic liver disease. Alcohol Clin Exp Res. 2008;32(6):1031–9. doi: 10.1111/j.1530-0277.2008.00664.x.
    1. Jarcuska P, Janicko M, Veseliny E, Jarcuska P, Skladany L. Circulating markers of liver fibrosis progression. Clinica Chimica Acta. 2010;411(15-16):1009–1017. doi: 10.1016/j.cca.2010.04.009.
    1. Sun J. Matrix metalloproteinases and tissue inhibitor of metalloproteinases are essential for the inflammatory response in cancer cells. Journal of Signal Transduction. 2010;2010:1–7.
    1. Takahara T, Furui K, Yata Y, Jin B, Zhang LP, Nambu S, Sato H, Seiki M, Watanabe A. Dual expression of matrix protease -2 and membrane type I-matrix proteinase in fibrotic human livers. Hepatology. 1997;26:1521–1529. doi: 10.1002/hep.510260620.
    1. Walsh KM, Timms P, Campbell S, MacSween RN, Morris AJ. Plasma levels of matrix metalloproteinase-2 (MMP-2) and tissue inhibitors of metalloproteinases-1 and -2 (TIMP-1 and TIMP-2) as non invasive markers of liver disease inchronic hepatitis C: comparison using ROC analysis. Dig Dis Sci. 1999;44:624–630. doi: 10.1023/A:1026630129025.
    1. Murawaki Y, Ikuta Y, Idobe Y, Kawasaki H. Serum matrix metalloproteinase-1 in patients with chronic viral hepatitis. J Gastroenterol Hepatol. 1999;14:138–145.
    1. Hayasaka A, Suzuki N, Fujimoto N. et al.Elevated plasma levels of matrix metalloproteinase-9 (92-kd type IV collagenase/gelatinase B) in hepatocellular carcinoma. Hepatology. 1996;24:1058–1062. doi: 10.1002/hep.510240513.
    1. Badra G, Lotfy M, El-Refaie A, Obada M, Abdelmonem E, Kandeel S, Fathy A. Significance of serum matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in chronic hepatitis C patients. Acta Microbiol Immunol Hung. 2010;57(1):29–42. doi: 10.1556/AMicr.57.2010.1.3.
    1. Kanzler S, Baumann M, Schirmacher P, Dries V, Bayer E, Gerken G, Dienes HP, Lohse AW. Prediction of progressive liver fibrosis in hepatitis C infection by serum and tissue levels of transforming growth factor-beta. J Viral Hepat. 2001;8(6):430–7. doi: 10.1046/j.1365-2893.2001.00314.x.
    1. Lydatakis H, Hager IP, Kostadelou E, Mpousmpoulas S, Pappas S, Diamantis I. Non-invasive markers to predict the liver fibrosis in non alcoholic fatty liver disease. Liver Int. 2006;26:864–871. doi: 10.1111/j.1478-3231.2006.01312.x.
    1. Tran A, Benzaken S, Saint-Paul MC, Guzman-Granier E, Hastier P, Pradier C, Barjoan EM, Demuth N, Longo F, Rampal P. Chondrex (YKL-40), a potential new serum fibrosis marker in patients with alcoholic liver disease. Eur J Gastroenterol Hepatol. 2000;12(9):989–993. doi: 10.1097/00042737-200012090-00004.
    1. Berres ML, Papen S, Pauels K, Schmitz P, Zaldivar MM, Hellerbrand C, Mueller T, Berg T, Weiskirchen R, Trautwein C, Wasmuth HE. A functional variation in CHI3L1 is associated with severity of liver fibrosis and YKL-40 serum levels in chronic hepatitis C infection. J Hepatol. 2009;50(2):370–6. doi: 10.1016/j.jhep.2008.09.016.
    1. Kropf J, Gressner AM, Negwer A. Efficacy of serum laminin measurement for diagnosis of fibrotic liver diseases. Clinical Chemistry. 1988;34:2026–2030.
    1. Korner T, Kropf J, Gressner AM. Serum laminin and hyaluronan in liver cirrhosis: markers of progression with high prognostic value. J Hepatol. 1996;25:684–688. doi: 10.1016/S0168-8278(96)80239-X.
    1. Gressner OA, Gressner AM. Connective tissue growth factor: a fibrogenic master switch in fibrotic liver diseases. Liver Int. 2008;28:1065–1079. doi: 10.1111/j.1478-3231.2008.01826.x.
    1. Camps J, Marsillach J, Joven J. Measurement of serum paraoxonase-1 activity in the evaluation of liver function. World J Gastroenterol. 2009;15(16):1929–1933. doi: 10.3748/wjg.15.1929.
    1. Ferre N, Camps J, Prats E, Vilella E, Paul A, Figuera L, Joven J. Serum paraoxonase activity: a new additional test for the improved evaluation of chronic liver damage. Clin Chem. 2002;48(2):261–268.
    1. Molleken C, Sitek B, Henkel C, Poschmann G, Sipos B, Wiese S, Warscheid B, Broelsch C, Reiser M, Friedman SL, Tornoe I, Schlosser A, Kloppel G, Schmiegel W, Meyer HE, Holmskov U, Stühler K. Detection of novel biomarkers of liver cirrhosis by proteomic analysis. Hepatology. 2009;49(4):1257–1266. doi: 10.1002/hep.22764.
    1. Haukeland JW, Schreiner LT, Lorgen I, Frigstad SO, Bang C, Raknerud N, Konopski Z. AST/ALT ratio provides prognostic information independently of Child-Pugh class, gender and age in non-alcoholic cirrhosis. Scand J Gastroenterol. 2008;43(10):1241–1248. doi: 10.1080/00365520802158614.
    1. Giboney PT. Mildly elevated liver transaminase levels in the asymptomatic patient. Am Fam Physician. 2005;71(6):1105–1110.
    1. Nguyen-Khac E, Chatelain D, Tramier B, Decrombecque C, Robert B, Joly JP, Brevet M, Grignon P, Lion S, Le Page L, Dupas JL. Assessment of asymptomatic liver fibrosis in alcoholic patients using FibroScan: prospective comparison with seven non-invasive laboratory tests. Aliment Pharmacol Ther. 2008;28(10):1188–98. doi: 10.1111/j.1365-2036.2008.03831.x.
    1. Lu LG, Zeng MD, Mao YM, Li JQ, Qiu DK, Fang JY, Cao AP, Wan MB, Li CZ, Ye J, Cai X, Chen CW, Wang JY, Wu SM, Zhu JS, Zhou XQ. Relationship between clinical and pathologic findings in patients with chronic liver diseases. World J Gastroenterol. 2003;9(12):2796–2800.
    1. DallaPiazza M, Amorosa VK, Localio R, Kostman JR, Lo Re V. Prevalence and risk factors for significant liver fibrosis among HIV-monoinfected patients. BMC Infect Dis. 2010;10:116. doi: 10.1186/1471-2334-10-116.
    1. Lin ZH, Xin YN, Dong QJ, Wang Q, Jiang XJ, Zhan SH, Sun Y, Xuan SY. Performance of the aspartate aminotransferase-to-platelet ratio index for the staging of hepatitis C-related fibrosis: an updated meta-analysis. Hepatology. 2011;53(3):726–36. doi: 10.1002/hep.24105.
    1. Rossi E, Adams LA, Bulsara M, Jeffrey GP. Assessing liver fibrosis with serum marker models. Clin Biochem Rev. 2007;28(1):3–10.
    1. Guechot J, Lasnier E, Sturm N, Paris A, Zarski JP. ANRS HC EP 23 Fibrostar study group. Automation of the Hepascore and validation as a biochemical index of liver fibrosis in patients with chronic hepatitis C from the ANRS HC EP 23 Fibrostar cohort. Clin Chim Acta. 2010;411(1-2):86–91. doi: 10.1016/j.cca.2009.10.011.
    1. Sterling RK, Lissen E, Clumeck N, Sola R, Correa MC, Montaner J, S Sulkowski M, Torriani FJ, Dieterich DT, Thomas DL, Messinger D, Nelson M. APRICOT Clinical Investigators. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology. 2006;43:1317–1325. doi: 10.1002/hep.21178.
    1. Vallet-Pichard A, Mallet V, Nalpas B, Verkarre V, Nalpas A, Dhalluin-Venier V, Fontaine H, Pol S. FIB-4: An inexpensive and accurate marker of fibrosis in HCV infection. comparison with liver biopsy and fibrotest. Hepatology. 2007;46(1):32–36. doi: 10.1002/hep.21669.
    1. Kelleher TB, Mehta SH, Bhaskar R, Sulkowski M, Astemborski J, Thomas DL, Moore RE, Afdhal NH. Prediction of hepatic fibrosis in HIV/HCV co-infected patients using serum fibrosis markers: The SHASTA index. J Hepatology. 2005;43(1):78–84. doi: 10.1016/j.jhep.2005.02.025.
    1. Braden B, Faust D, Sarrazin U, Zeuzem S, Dietrich CF, Caspary WF, Sarrazin C. 13C-methacetin breath test as liver function test in patients with chronic hepatitis C virus infection. Aliment Pharmacol Ther. 2005;21(2):179–85. doi: 10.1111/j.1365-2036.2005.02317.x.
    1. Lalazar G, Pappo O, Hershcovici T, Hadjaj T, Shubi M, Ohana H, Hemed N, Ilan Y. A continuous 13C methacetin breath test for noninvasive assessment of intrahepatic inflammation and fibrosis in patients with chronic HCV infection and normal ALT. J Viral Hepat. 2008;15(10):716–728. doi: 10.1111/j.1365-2893.2008.01007.x.
    1. Patel K, Gordon SC, Jacobson I, Hezode C, Oh E, Smith KM, Pawlotsky JM, McHutchison JG. Evaluation of a panel of non-invasive serum markers to differentiate mild from moderateto- advanced liver fibrosis in chronc hepatitis C patients. J Hepatol. 2004;41:935–942. doi: 10.1016/j.jhep.2004.08.008.
    1. Patel K, Nelson DR, Rockey DC, Afdhal NH, Smith KM, Oh E, Hettinger K, Vallee M, Dev A, Smith-Riggs M, McHutchison JG. Correlation of FIBROSpect II with histologic and morphometric evaluation of liver fibrosis in chronic hepatitis C. Clin Gastroenterol Hepatol. 2008;6(2):242–247. doi: 10.1016/j.cgh.2007.11.009.
    1. Rossi E, Adams L, Prins A, Bulsara M, de Boer B, Garas G, MacQuillan G, Speers D, Jeffrey G. FibroTest biochemical markers score in assessing liver fibrosis in hepatitis C patients. Validation of the Clin Chem. 2003;49(3):450–454.
    1. Imbert-Bismut F, Messous D, Thibault V, Myers RB, Piton A, Thabut D, Devers L, Hainque B, Mercadier A, Poynard T. 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(3):323–333. doi: 10.1515/CCLM.2004.058.
    1. Friedrich-Rust M, Rosenberg W, Parkes J, Herrmann E, Zeuzem S, Sarrazin C. Comparison of ELF, FibroTest and FibroScan for the non-invasive assessment of liver fibrosis. BMC Gastroenterology. 2010;10:103. doi: 10.1186/1471-230X-10-103.
    1. 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. doi: 10.1002/hep.21520.
    1. 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(3):212–218.
    1. 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. doi: 10.1016/S0168-8278(98)80318-8.
    1. Cales P, Boursier J, Oberti F, Hubert I, Gallois Y, Rousselet MC, Dib N, Moal V, Macchi L, Chevailler A, Michalak S, Hunault G, Chaigneau J, Sawadogo A, Lunel F. FibroMeters: a family of blood tests for liver fibrosis. Gastroenterol Clin Biol. 2008;32(6 Suppl 1):40–51.
    1. Angulo P, Hui JM, Marchesini G, Bugianesi E, George J, Farrell GC, Enders F, Saksena S, Burt AD, Bida JP, Lindor K, Sanderson SO, Lenzi M, Adams LA, Kench J, Therneau TM, Day CP. The NAFLD fibrosis score: a noninvasive system that identifies liver fibrosis in patients with NAFLD. Hepatology. 2007;45:846–854. doi: 10.1002/hep.21496.
    1. Rosenberg WM, Voelker M, Thiel R, Becka M, Burt A, Schuppan D, Hubscher S, Roskams T, Pinzani M, Arthur MJ. European Liver Fibrosis Group. Serum markers detect the presence of liver fibrosis: a cohort study. Gastroenterology. 2004;127:1704–1713. doi: 10.1053/j.gastro.2004.08.052.
    1. Guha IN, Parkes J, Roderick P, Chattopadhyay D, Cross R, Harris S, Kaye P, Burt AD, Ryder SD, Aithal GP, Day CP, Rosenberg WM. Non-invasive markers of fibrosis in non-alcoholic fatty liver disease: validating the European Liver Fibrosis panel and exploring simple markers. Hepatology. 2008;47(2):455–460.
    1. Callewaert N, Vlierberghe HV, Hecke AV, Laroy W, Delanghe J, Contreras R. Non invasive diagnosis of liver cirrhosis using DNA sequencer-based total serum protein glycomics. Nature Medicine. 2004;10:429–434. doi: 10.1038/nm1006.
    1. Blomme B, Van Steenkiste C, Callewaert N, Van Vlierberghe H. Alteration of protein glycosylation in liver diseases. J Hepatol. 2009;50(3):592–603. doi: 10.1016/j.jhep.2008.12.010.
    1. Younossi ZM, Baranova A, Stepanova M, Page S, Calvert VS, Afendy A, Goodman Z, Chandhoke V, Liotta L, Petricoin E. Phosphoproteomic biomarkers predicting histologic nonalcoholic steatohepatitis and fibrosis. J Proteome Res. 2010;9(6):3218–24. doi: 10.1021/pr100069e.
    1. Sebastiani G, Vario A, Guido M, Noventa F, Plebani M, Pistis R, Ferrari A, Alberti A. Stepwise combination algorithms of non-invasive markers to diagnose significant fibrosis in chronic hepatitis C. J Hepatol. 2006;44(4):686–93. doi: 10.1016/j.jhep.2006.01.007.
    1. Sebastiani G, Halfon P, Castera L, Pol S, Thomas DL, Mangia A, Di Marco V, Pirisi M, Voiculescu M, Guido M, Bourliere M, Noventa F, Alberti A. SAFE biopsy: a validated method for large-scale staging of liver fibrosis in chronic hepatitis C. Hepatology. 2009;49(6):1821–7. doi: 10.1002/hep.22859.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj