Hepatic Elastography for the Assessment of Liver Fibrosis – Present and Future

Abstract

Liver Biopsy was considered the “gold standard” for severity assessment in chronic hepatitis for a very long time. In recent years, non invasive methods were developed in order to replace it. Among them ultrasound based elastographic methods: Transient Elastography (already validated and replacing liver biopsy in some countries), Real Time Tissue Elastography and Acoustic Radiation Force Impulse Elastography (currently under evaluation) and Shear Wave Elastography (the newest one). As an alternative to liver biopsy, the development of all these non invasive methods for dynamic evaluation of liver fibrosis will decrease the need for LB, making clinical care safer and more convenient for patients with liver diseases.

Zusammenfassung

Die Leberbiopsie galt für lange Zeit als der Goldstandard in der Beurteilung des Schweregrads der chronischen Hepatitis. Um dieses diagnostische Verfahren zu ersetzen, wurden in den letzten Jahren nicht invasive Methoden entwickelt: die transiente Elastometrie (in manchen Ländern bereits als Ersatz für die Leberbiopsie bestätigt), die Real-Time-Elastografie und die Acoustic-Radiation-Force-Impulse-Elastografie (momentan unter Evaluation) sowie die neueste Methode: die Shear-Wave-Elastografie. Die Entwicklung all dieser nicht invasiven Methoden für die dynamische Beurteilung der Leberfibrose wird die Notwendigkeit der Leberbiopsien senken und die Betreuung von Patienten mit Lebererkrankungen risikofreier und günstiger machen.

Key words

Transient Elastography - Acoustic Radiation Force Impulse Elastography - Real Time Elastrography - Shear Wave Elastography - liver fibrosis

• References

• 1 Gebo KA, Herlong HF, Torbenson MS et al. Role of liver biopsy in management of chronic hepatitis C: a systematic review. Hepatology 2002; 36: S161-S172
• 2 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
• 3 Castera 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. Gastroenterology 2005; 128: 343-350
• 4 Friedman LS. Controversies in liver biopsy: who, where, when, how, why?. Curr Gastroenterol Rep 2004; 6: 30-36
• 5 Thampanitchawong P, Piratvisuth T. Liver biopsy: complications and risk factors. World J Gastroenterol 1999; 5: 301-304
• 6 Piccinino F, Sagnelli E, Pasquale G et al. Complications following percutaneous liver biopsy. A multicentre retrospective study on 68,276 biopsies. J Hepatol 1986; 2: 165-173
• 7 Afdhal N. Debate: Are non-invasive tests ready to replace liver biopsy. Favor of the use of non-invasive tests. Clinical Care Options 2006; 7-19
• 8 Regev A, Berho M, Jeffers LJ 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, Dargere D, Paradis V. Sampling variability of liver fibrosis in chronic hepatitis C. Hepatology 2003; 38: 1449-1457
• 10 Cholongitas E, Senzolo M, Standish R et al. A Systematic Review of the Quality of Liver Biopsy Specimens. Am J Clin Pathol 2006; 125: 710-721
• 11 Colloredo G, Guido M, Sonzogni A et al. 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
• 12 Yin M, Talwalkar JA, Glaser KJ et al. Assessment of hepatic fibrosis with magnetic resonance elastography. Clin Gastroenterol Hepatol 2007; 5: 1207-1213
• 13 Watanabe H, Kanematsu M, Kitagawa T et al. MR elastography of the liver at 3 T with cine-tagging and bending energy analysis: preliminary results. Eur Radiol 2010; 20: 2381-2389
• 14 Huwart L, Sempoux C, Salameh N et al. Liver fibrosis: noninvasive assessment with MR elastography versus aspartate aminotranspherase-to-platelet ratio index. Radiology 2007; 245: 458-466
• 15 Huwart L, Sempoux C, Vicaut E et al. Magnetic resonance elastography for the noninvasive staging of liver fibrosis. Gastroenterology 2008; 135: 32-40
• 16 Wang Y, Ganger DR, Levitsky J et al. Assessment of chronic hepatitis and fibrosis: comparison of MR elastography and diffusion-weighted imaging. Am J Roentgenol 2011; 196: 553-561
• 17 Chen J, Talwalkar JA, Yin M et al. Early detection of nonalcoholic steatohepatitis in patients with nonalcoholic fatty liver disease by using MR elastography. Radiology 2011; 259: 749-756
• 18 Talwalkar JA, Kurtz DM, Schoenleber SJ et al. Ultrasound-based transient elastography for the detection of hepatic fibrosis: systematic review and meta-analysis. Clin Gastroenterol Hepatol 2007; 5: 1214-1220
• 19 Oudry J, Vappou J, Choquet P et al. Ultrasound-based transient elastography compared to magnetic resonance elastography in soft tissue-mimicking gels. J Magn Reson Imaging 2009; 30: 1145-1150
• 20 Corpechot C, El Naggar A, Poujol-Robert A et al. Assessment of biliary fibrosis by transient eleastography in patients with PBC and PSC. Hepatology 2006; 43: 1118-1124
• 21 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: 242-247
• 22 Sporea I, Sirli R, Deleanu A et al. Liver stiffness measurements in patients with HBV vs. HCV chronic hepatitis: a comparative study. World J Gastroenterol 2010; 16: 4832-4837
• 23 Sporea I, Nicolita D, Sirli R et al. Assessment of noninvasive liver stiffness in inactive HBsAg carriers by transient elastography. Hepatitis Monthly 2011; 11: 182-185
• 24 Vergara S, Macias J, Rivero A et al. The use of transient elastometry for assessing liver fibrosis in patients with HIV and hepatitis C virus coinfection. Clin Infect Dis 2007; 45: 969-974
• 25 De Ledinghen V, Douvin C, Kettaneh A et al. Diagnosis of hepatic fibrosis and cirrhosis by transient elastography in HIV/hepatitic C virus-coinfected patients. J Acquir Immune Defic Syndr 2006; 41: 175-179
• 26 Yoneda M, Fujita K, Inamori M et al. Transient elastography in patients with non-alcoholic fatty liver disease (NAFLD). Gut 2007; 56: 1330-1331
• 27 Castera L, Foucher J, Bernard PH et al. Pitfalls of liver stiffness measurement: a 5-years prospective study of 13,369 examinations. Hepatology 2010; 51: 828-835
• 28 de Lédinghen V, Vergniol J, Foucher J et al. Feasibility of liver transient elastography with FibroScan using a new probe for obese patients. Liver Int 2010; 30: 1043-1048
• 29 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; 55: 199-208
• 30 de Lédinghen V, Wong VW, Vergniol J et al. Diagnosis of liver fibrosis and cirrhosis using liver stiffness measurement: Comparison between M and XL probe of FibroScan®. [Epub ahead of print] J Hepatol 13.12.2011;
• 31 Friedrich-Rust M, Ong MF, Martens S et al. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology 2008; 134: 960-974
• 32 Castera L, Le Bail B, Roudot-Thoraval F et al. Early detection in routine clinical practice of cirrhosis and esophageal varices in chronic hepatitis C: Comparison of transient elastography (FibroScan) with standard laboratory tests and non-invasive scores. J Hepatol 2009; 50: 59-68
• 33 Foucher J, Chanteloup E, Vergniol J et al. Diagnosis of cirrhosis by transient elastography (FibroScan): A prospective study. Gut 2006; 55: 403-408
• 34 Sporea I, Raţiu I, Sirli R et al. Value of transient elastography for the prediction of variceal bleeding. World J Gastroenterol 2011; 17: 2206-2210
• 35 Masuzaki R, Tateishi R, Yoshida H et al. Prospective risk assessment for hepatocellular carcinoma development in patients with chronic hepatitis C by transient elastography. Hepatology 2009; 49: 1954-1961
• 36 Sporea I, Şirli R, Deleanu A et al. Comparison of the liver stiffness measurement by transient elastography with the liver biopsy. World J Gastroenterol 2008; 14: 6513-6517
• 37 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
• 38 Sporea I, Sirli RL, Deleanu A et al. What did we learn from the first 3,459 cases of liver stiffness measurement by transient elastography (FibroScan®)?. Ultraschall in Med 2011; 32: 40-45
• 39 Sporea I, Şirli R, Popescu A et al. Is it better to use two elastographic methods for liver fibrosis assessment?. World J Gastroenterol 2011; 17: 3824-3829
• 40 European Association for the Study of the Liver. EASL Clinical Practice Guidelines: management of hepatitis C virus infection. J Hepatol 2011; 55: 245-264
• 41 Arena U, Vizzutti F, Corti G et al. Acute viral hepatitis increases liver stiffness values measured by transient elastography. Hepatology 2008; 47: 380-384
• 42 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: 360-369
• 43 Sagir A, Erhardt A, Schmitt M et al. Transient elastography is unreliable for detection of cirrhosis in patients with acute liver damage. Hepatology 2008; 47: 592-595
• 44 Millonig G, Reimann FM, Friedrich S et al. Extrahepatic cholestasis increases liver stiffness (FibroScan) irrespective of fibrosis. Hepatology 2008; 48: 1718-1723
• 45 Lebray P, Varnous S, Charlotte F et al. Liver stiffness is an unreliable marker of liver fibrosis in patients with cardiac insufficiency. Hepatology 2008; 48: 2089
• 46 Nightingale K, Soo MS, Nightingale R et al. Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 2002; 28: 227-235
• 47 Sporea I, Sirli R, Deleanu A et al. Acoustic radiation force impulse elastography as compared to transient elastography and liver biopsy in patients with chronic hepatopathies. Ultraschall in Med 2011; 32: S46-S52
• 48 Goertz RS, Zopf Y, Jugl V et al. Measurement of Liver Elasticity with Acoustic Radiation Force Impulse (ARFI) Technology: An Alternative Noninvasive Method for Staging Liver Fibrosis in Viral Hepatitis. Ultraschall in Med 2010; 31: 151-155
• 49 Bota S, Sporea I, Sirli R et al. Factors that influence the correlation of Acoustic Radiation Force Impulse (ARFI) elastography with liver fibrosis. Med Ultrason 2011; 13: 135-40
• 50 Friedrich-Rust M, Wunder K, Kriener S et al. Liver fibrosis in viral hepatitis: noninvasive assessment with acoustic radiation force im­pulse imaging versus transient elastography. Radiology 2009; 252: 595-604
• 51 Lupsor M, Badea R, Stefanescu H et al. Performance of a new elastographic method (ARFI technology) compared to unidimensional transient elastography in the noninvasive assessment of chronic hepatitis C. Preliminary results. J Gastrointestin Liver Dis 2009; 18: 303-310
• 52 Rifai K, Cornberg J, Bahr MJ et al. Akkurate und flexible Messung der Leber steifigkeit mittels Acoustic Radiation Force Impulse Imaging (ARFI). Ultraschall in Med 2010; 31: S2
• 53 Boozari B, Potthoff A, Mederacke I et al. Etablierung einer neuen Ultraschallmethode zur Messung der Lebersteifigkeit – prospektiver Vergleich mit Fibroscan und Leberhistologie. Ultraschall in Med 2010; 31: S2
• 54 Sporea I, Sirli R, Bota S et al. Is ARFI elastography reliable for predicting fibrosis severity in chronic HCV hepatitis?. World J Radiol 2011; 28: 188-193
• 55 Friedrich-Rust M, Nierhoff J, Lupsor M et al. Performance of Acoustic Radiation Force Impulse-Imaging for the staging of liver fibrosis: a pooled meta-analysis. J Viral Hepat 2012; 19: e212-e219
• 56 Sporea I, Badea R, Sirli R et al. How efficient is acoustic radiation force impulse elastography for the evaluation of liver stiffness?. Hepatitis Monthly 2011; 11: 532-538
• 57 Piscaglia F, Salvatore V, Di Donato R et al. Accuracy of VirtualTouch Acoustic Radiation Force Impulse (ARFI) Imaging for the Diagnosis of Cirrhosis during Liver Ultrasonography. Ultraschall in Med 2011; 32: 167-175
• 58 Gallotti A, D’Onofrio M, Pozzi Mucelli R. Acoustic Radiation Force Impulse (ARFI) technique in ultrasound with Virtual Touch tissue quantification of the upper abdomen. Radiol Med 2010; 115: 889-897
• 59 Goertz RS, Bernatik T, Neurath MF et al. Acoustic radiation force impulse (ARFI) Elastometrie der Schilddrüse und abdomineller Organe bei gesunden Probanden. Ultraschall in Med 2010; 31: S7
• 60 Goertz RS, Amann K, Heide R et al. An abdominal and thyroid status with Acoustic Radiation Force Impulse Elastometry – a feasibility study: Acoustic Radiation Force Impulse Elastometry of human organs. Eur J Radiol 2011; 80: e226-e230
• 61 Heide R, Strobel D, Bernatik T et al. Characterization of focal liver lesions (FLL) with acoustic radiation force impulse (ARFI) elastometry. Ultraschall in Med 2010; 31: 405-499
• 62 Grgurevic I, Cikara I, Horvat J et al. Noninvasive assessment of liver fibrosis with acoustic radiation force impulse imaging: increased liver and splenic stiffness in patients with liver fibrosis and cirrhosis. Ultraschall in Med 2011; 32: 160-166
• 63 Bota S, Sporea I, Sirli R et al. Spleen assessment by Acoustic Radiation Force Impulse Elastography (ARFI) for prediction of liver cirrhosis and portal hypertension. Med Ultrason 2010; 12: 213-217
• 64 Rifai K, Cornberg J, Bahr M et al. ARFI elastography of the spleen is inferior to liver elastography for the detection of portal hypertension. Ultraschall in Med 2011; 32: E24-E30
• 65 Sporea I, Vlad M, Bota S et al. Thyroid stiffness assessment by acoustic radiation force impulse elastography (ARFI). Ultraschall in Med 2011; 32: 281-285
• 66 Sporea I, Sirli R, Bota S et al. ARFI elastography for the evaluation of diffuse thyroid gland pathology: Preliminary results. World J Radiol 2012; 4: 174-178
• 67 Friedrich-Rust M, Romenski O, Meyer G et al. Acoustic Radiation Force Impulse-Imaging for the evaluation of the thyroid gland: a limited patient feasibility study. Ultrasonics 2012; 52: 69-74
• 68 Gu J, Du L, Bai M et al. Preliminary study on the diagnostic value of acoustic radiation force impulse technology for differentiating between benign and malignant thyroid nodules. J Ultrasound Med 2012; 31: 763-771
• 69 Friedrich-Rust M, Ong MF, Herrmann E et al. Real-time elastography for noninvasive assessment of liver fibrosis in chronic viral hepatitis. Am J Roentgenol 2007; 188: 758-764
• 70 Frey H. Real-time elastography: a new ultrasound procedure for reconstruction of tissue elasticity. Radiologe 2003; 43: 850-855
• 71 Havre RF, Elde E, Gilja OH et al. Freehand Real-time Elastography: Impact of scanning parameters on image quality and in vitro intra- and interobserver validations. Ultrasound Med Biol 2008; 34: 1638-1650
• 72 Tatsumi C, Kudo M, Ueshima K et al. Noninvasive Evaluation of Hepatic Fibrosis Using serum Fibrosis Markers, Transient Elastography (FibroScan) and Real Time Tissue Elastography. Intervirology 2008; 51: 27-33
• 73 Friedrich-Rust M, Schwarz A, Ong M et al. Real-Time Tissue Elastography Versus FibroScan for Noninvasive Assessment of Liver Fibrosis in Chronic Liver Disease. Ultraschall in Med 2009; 30: 478-484
• 74 Wang J, Guo L, Shi X et al. Real-time Elastography with a novel quantitative technology for assessment of liver fibrosis in chronic hepatitis B. Eur J Radiol 2012; 81: e31-e36
• 75 Koizumi Y, Hirooka M, Kisaka Y et al. Liver fibrosis in patients with chronic hepatitis C: noninvasive diagnosis by means of Real Time tissue Elastography-establishment of the method for measurement. Radiology 2011; 258: 610-617
• 76 Sarvazyan AP, Rudenko OV, Swanson SD et al. Shear wave elasticity imaging: A new ultrasonic technology of medical diagnostic. Ultrasound Med Biol 1998; 20: 1419-1436
• 77 Nightingale KR, McAleavey SA, Trahey GE. Shear wave generation using acoustic radiation force: In vivo and ex vivo results. Ultrasound Med Biol 2003; 29: 1715-1723
• 78 Bercoff J, Tanter M, Fink M. Supersonic shear imaging: A new technique for soft tissues elasticity mapping. IEEE Trans Ultrason Ferroelectr Freq Control 2004; 51: 396-409
• 79 Tanter M, Bercoff J, Athanasiou A et al. Quantitative Assessement Of Breast Lesion Viscoelasticity: Initial Clinical Results Using Supersonic Shear Imaging. Ultrasound Med Biol 2008; 9: 1373-1386
• 80 Bavu E, Gennisson JL, Mallet V et al. Supersonic Shear Imaging is a new potent morphlogical noninvasive technique to assess liver fibrosis. Part II: Comparison with FibroScan. J Hepatol 2010; 52: S166
• 81 Zoumpoulis PS, Theotokas I, Mastorakou E et al. Technical and Software Adjusments for a reliable Shear Wave Elastography Estimation of Fibrosis in Chronic Liver Disease. Ultrasound Med Biol 2011; 8S: S58
• 82 Zoumpoulis PS, Mastorakou E, Theotokas I et al. Shear Wave Elastography for the Evaluation of Diffuse Liver Disease: Determining Normal and Pathological Values in kPa. Ultrasound Med Biol 2011; 8S: S58
• 83 Karlas T, Troeltzschn M, Wiegand J et al. Use of Aixplorer™ for the detection of Liver Fibrosis or Cirrhosis in patients with Hepatitis C. Ultrasound Med Biol 2011; 8S: S58
• 84 Ferraioli G, Tinelli C, Dal Bello et al. Performance of Real-Time Elastography in the Assessment of Liver Fibrosis in Chronic Hepatitis. Hepatology 2011; 4: 816A, 968
• 85 Bavu E, Gennisson JL, Couarde M et al. Noninvasive in vivo liver evaluation using supersonic shear imaging: a clinical study on 113 hepatitis C virus patients. Ultrasound Med Biol 2011; 37: 1361-1373
• 86 Heide R, Waldner M, Görtz RS et al. Echtzeit-Elastometrie (RTE) der Leber bei Gesunden: Vergleich zur konventionellen Elastometrie (cARFI). Ultraschall in Med 2010; 31: S1
• 87 Castera L, Sebastiani G, Le Bail B et al. Prospective comparison of two algorithms combining non invasive tests for staging of fibrosis in chronic hepatitis C. J Hepatol 2010; 52: 191-198
• 88 Castera L, Foucher J, Bertet J et al. FibroScan and FibroTest to assess liver fibrosis in HCV with normal aminotransferases. Hepatology 2006; 43: 373-374
• 89 Colletta C, Smirne C, Fabris C et al. Value of two noninvasive methods to detect progression of fibrosis among HCV carriers with normal aminotransferases. Hepatology 2005; 42: 838-845
• 90 Castera L, Foucher J, Bernard PH et al. Transient elastography (FibroScan) and FibroTest to assess liver fibrosis in inactive hepatitis B carriers: a prospective controlled study. Hepatology 2006; 44: 489A
• 91 Non invasive methods for the evaluation of hepatic fibrosis/cirrhosis. 2006 www.has-sante.fr
• 92 Bachmann-Nielsen M, Săftoiu A. Elastography – True or False?. Ultraschall in Med 2011; 32: 5-7