Clinical Radiology
Volume 64, Issue 11 , Pages 1056-1066 , November 2009

Non-invasive evaluation of liver cirrhosis using ultrasound

  • N. Goyal

      Affiliations

    • Department of Radiology, University Hospital of Wales, Cardiff, UK
    • Corresponding Author InformationGuarantor and correspondent: N. Goyal, Department of Radiology, University Hospital of Wales, Cardiff CF14 4XW, UK. Tel: +44 29 2074 3030; fax: +44 29 2074 3029.
  • ,
  • N. Jain

      Affiliations

    • Department of Radiology, University Hospital of Wales, Cardiff, UK
  • ,
  • V. Rachapalli

      Affiliations

    • Department of Radiology, University Hospital of Wales, Cardiff, UK
  • ,
  • D.L. Cochlin

      Affiliations

    • Department of Radiology, University Hospital of Wales, Cardiff, UK
  • ,
  • M. Robinson

      Affiliations

    • Department of Radiology, Royal Gwent Hospital, Newport, Wales, UK

Received 2 March 2009 ,Revised 26 May 2009 ,Accepted 27 May 2009.

References 

  1. Anthony PP, Ishak KG, Nayak NC, et al. The morphology of cirrhosis. Recommendations on definition, nomenclature, and classification by a working group sponsored by the World Health Organization. J Clin Pathol. 1978;31:395–414
  2. Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med. 2001;344:495–500
  3. Cadranel JF, Rufat P, Degos F. Practices of liver biopsy in France: results of a prospective nationwide survey. For the Group of Epidemiology of the French Association for the Study of the Liver (AFEF). Hepatology. 2000;32:477–481
  4. Saadeh S, Cammell G, Carey WD, et al. The role of liver biopsy in chronic hepatitis C. Hepatology. 2001;33:196–200
  5. Poynard T, Ratziu V, Bedossa P. Appropriateness of liver biopsy. Can J Gastroenterol. 2000;14:543–548
  6. Colli A, Fraquelli M, Andreoletti M, et al. Severe liver fibrosis or cirrhosis: accuracy of US for detection—analysis of 300 cases. Radiology. 2003;227:89–94
  7. Fontana RJ, Lok AS. Noninvasive monitoring of patients with chronic hepatitis C. Hepatology. 2002;36:S57–S64
  8. Ono E, Shiratori Y, Okudaira T, et al. Platelet count reflects stage of chronic hepatitis C. Hepatol Res. 1999;15:192–200
  9. Luo JC, Hwang SJ, Chang FY, et al. Simple blood tests can predict compensated liver cirrhosis in patients with chronic hepatitis C. Hepatogastroenterology. 2002;49:478–481
  10. Pohl A, Behling C, Oliver D, et al. Serum aminotransferase levels and platelet counts as predictors of degree of fibrosis in chronic hepatitis C virus infection. Am J Gastroenterol. 2001;96:3142–3146
  11. Guechot J, Laudat A, Loria A, et al. 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
  12. Dohmen K, Shirahama M, Onohara S, et al. Differences in survival based on the type of follow-up for the detection of hepatocellular carcinoma: an analysis of 547 patients. Hepatol Res. 2000;18:110–121
  13. Dohmen K, Shigematsu H, Irie K, et al. Trends in clinical characteristics, treatment and prognosis of hepatocellular carcinoma. Hepatogastroenterology. 2003;50:1872–1877
  14. Celle G, Savarino V, Picciotto A, et al. Is hepatic ultrasonography a valid alternative tool to liver biopsy? Report on 507 cases studied with both techniques. Dig Dis Sci. 1988;33:467–471
  15. Gaiani S, Gramantieri L, Venturoli N, et al. What is the criterion for differentiating chronic hepatitis from compensated cirrhosis? A prospective study comparing ultrasonography and percutaneous liver biopsy. J Hepatol. 1997;27:979–985
  16. Tuney D, Aribal ME, Ertem D, et al. Diagnosis of liver cirrhosis in children based on colour Doppler ultrasonography with histopathological correlation. Pediatr Radiol. 1998;28:859–864
  17. Khan KN, Yamasaki M, Yamasaki K, et al. Proposed abdominal sonographic staging to predict severity of liver diseases: analysis with peritoneoscopy and histology. Dig Dis Sci. 2000;45:554–564
  18. Nicolau C, Bianchi L, Vilana R. Gray-scale ultrasound in hepatic cirrhosis and chronic hepatitis: diagnosis, screening, and intervention. Semin Ultrasound CT MRI. 2002;23:3–18
  19. Kutcher R, Smith GS, Sen F, et al. Comparison of sonograms and liver histologic findings in patients with chronic hepatitis C virus infection. J Ultrasound Med. 1998;17:321–325
  20. Di Lelio A, Cestari C, Lomazzi A, et al. Cirrhosis: diagnosis with sonographic study of the liver surface. Radiology. 1989;172:389–392
  21. Ferral H, Male R, Cardiel M, et al. Cirrhosis: diagnosis by liver surface analysis with high-frequency ultrasound. Gastrointest Radiol. 1992;17:74–78
  22. Simonovsky V. The diagnosis of cirrhosis by high resolution ultrasound of the liver surface. Br J Radiol. 1999;72:29–34
  23. Ong TZ, Tan HJ. Ultrasonography is not reliable in diagnosing liver cirrhosis in clinical practice. Singapore Med J. 2003;44:293–295
  24. Hofer M. Ultrasound teaching manual. 2nd ed.. New York: Thieme; 1997;
  25. Afdhal NH, Nunes D. Evaluation of liver fibrosis: a concise review. Am J Gastroenterol. 2004;99:1160–1174
  26. Harbin WP, Robert NJ, Ferrucci JT. Diagnosis of cirrhosis based on regional changes in hepatic morphology: a radiological and pathological analysis. Radiology. 1980;135:273–283
  27. Niazi MFK, Khan MU, Ghaffar A, et al. Accuracy of ultrasonography in detection of severe liver fibrosis/cirrhosis in chronic liver disease. Medical Forum Monthly. 2007;18:2–6
  28. Sharatchandra SL, Jain AP, Pathak S. Ultrasonography in the diagnosis of decompensated liver cirrhosis. JMS Journal of Medical Society. 2003;17:87–90
  29. Hess CF, Schmiedl U, Koelbel G, et al. Diagnosis of liver cirrhosis with US: receiver-operating characteristic analysis of multidimensional caudate lobe indexes. Radiology. 1989;171:349–351
  30. Cioni G, Tincani E, D'Alimonte P, et al. Relevance of reduced portal flow velocity, low platelet count and enlarged spleen diameter in the non-invasive diagnosis of compensated liver cirrhosis. Eur J Med. 1993;2:408–410
  31. Macias Rodriguez MA, Rendon Unceta P, Navas Relinque C, et al. Ultrasonography in patients with chronic liver disease: its usefulness in the diagnosis of cirrhosis. Rev Esp Enferm Dig. 2003;95:258–264251–7
  32. Schneider AR, Teuber G, Kriener S, et al. Noninvasive assessment of liver steatosis, fibrosis and inflammation in chronic hepatitis C virus infection. Liver Int. 2005;25:1150–1155
  33. Brogna A, Bucceri AM, Catalano F, et al. Ultrasound demonstration of gallbladder wall thickening as a method to differentiate cirrhotic ascites from other ascites. Invest Radiol. 1996;31:80–83
  34. Huang YS, Lee SD, Wu JC, et al. Utility of sonographic gallbladder wall patterns in differentiating malignant from cirrhotic ascites. J Clin Ultrasound. 1989;17:187–192
  35. Colli A, Cocciolo M, Buccino G, et al. Thickening of the gallbladder wall in ascites. J Clin Ultrasound. 1991;19:357–359
  36. Wang TF, Hwang SJ, Lee EY, et al. Gall-bladder wall thickening in patients with liver cirrhosis. J Gastroenterol Hepatol. 1997;12:445–449
  37. Sezgin O, Bahar K, Uzunalimoglu O. Gallbladder wall thickening and emptying function in liver cirrhosis. Turk J Gastroenterol. 1997;8:397–401
  38. Arroyo V, Colmenero J. Ascites and hepatorenal syndrome in cirrhosis: pathophysiological basis of therapy and current management. J Hepatol. 2003;38(Suppl 1):S69–S89
  39. Arroyo V, Gines P, Gerbes AL, et al. Definition and diagnostic criteria of refractory ascites and hepatorenal syndrome in cirrhosis. International Ascites Club. Hepatology. 1996;23:164–176
  40. Kumar R, Ahmed R, Rathi SK, et al. Frequency of hepatorenal syndrome among cirrhotics. J Coll Physicians Surg Pak. 2005;15:590–593
  41. Fiorinia F, Barozzib L. The role of ultrasonography in the study of medical nephropathy. J Ultrasound. 2007;10:161–167
  42. Gotzberger M, Kaiser C, Landauer N, et al. Intrarenal resistance index for the assessment of early renal function impairment in patients with liver cirrhosis. Eur J Med Res. 2008;13:383–387
  43. Platt JF, Rubin JM, Ellis JH. Acute renal failure: possible role of duplex Doppler US in distinction between acute prerenal failure and acute tubular necrosis. Radiology. 1991;179:419–423
  44. Pompili M, Rapaccini GL, De Luca F, et al. Doppler ultrasonographic evaluation of the early changes in renal resistive index in cirrhotic patients undergoing liver transplantation. J Ultrasound Med. 1999;18:497–502
  45. Platt JF, Ellis JH, Rubin JM, et al. Renal duplex Doppler ultrasonography: a noninvasive predictor of kidney dysfunction and hepatorenal failure in liver disease. Hepatology. 1994;20:362–369
  46. Maroto A, Gines A, Salo J, et al. Diagnosis of functional kidney failure of cirrhosis with Doppler sonography: prognostic value of resistive index. Hepatology. 1994;20:839–844
  47. Iwao T, Toyonaga A, Oho K, et al. Value of Doppler ultrasound parameters of portal vein and hepatic artery in the diagnosis of cirrhosis and portal hypertension. Am J Gastroenterol. 1997;92:1012–1017
  48. Vassiliades VG, Ostrow TD, Chezmar JL, et al. Hepatic arterial resistive indices: correlation with the severity of cirrhosis. Abdom Imaging. 1993;18:61–65
  49. Bolondi L, Li Bassi S, Gaiani S, et al. Liver cirrhosis: changes of Doppler waveform of hepatic veins. Radiology. 1991;178:513–516
  50. Gorka W, Kagalwalla A, McParland BJ, et al. Diagnostic value of Doppler ultrasound in the assessment of liver cirrhosis in children: histopathological correlation. J Clin Ultrasound. 1996;24:287–295
  51. Zironi G, Gaiani S, Fenyves D, et al. Value of measurement of mean portal flow velocity by Doppler flowmetry in the diagnosis of portal hypertension. J Hepatol. 1992;16:298–303
  52. Taylor KJ, Burns PN. Duplex Doppler scanning in the pelvis and abdomen. Ultrasound Med Biol. 1985;11:643–658
  53. Pierce ME, Sewell R. Identification of hepatic cirrhosis by duplex Doppler ultrasound value of the hepatic artery resistive index. Australas Radiol. 1990;34:331–333
  54. Sacerdoti D, Merkel C, Bolognesi M, et al. Hepatic arterial resistance in cirrhosis with and without portal vein thrombosis: relationships with portal hemodynamics. Gastroenterology. 1995;108:1152–1158
  55. Koslin DB, Berland LL. Duplex Doppler examination of the liver and portal venous system. J Clin Ultrasound. 1987;15:675–686
  56. Kok T, Haagsma EB, Klompmaker IJ, et al. Doppler ultrasound of the hepatic artery and vein performed daily in the first two weeks after orthotopic liver transplantation. Useful for the diagnosis of acute rejection?. Invest Radiol. 1996;31:173–179
  57. Colli A, Cocciolo M, Riva C, et al. Abnormalities of Doppler waveform of the hepatic veins in patients with chronic liver disease: correlation with histologic findings. AJR Am J Roentgenol. 1994;162:833–837
  58. Ohta M, Hashizume M, Tomikawa M, et al. Analysis of hepatic vein waveform by Doppler ultrasonography in 100 patients with portal hypertension. Am J Gastroenterol. 1994;89:170–175
  59. Ohta M, Hashizume M, Kawanaka H, et al. Prognostic significance of hepatic vein waveform by Doppler ultrasonography in cirrhotic patients with portal hypertension. Am J Gastroenterol. 1995;90:1853–1857
  60. Hosoki T, Kuroda C, Tokunaga K, et al. Hepatic venous outflow obstruction: evaluation with pulsed duplex sonography. Radiology. 1989;170:733–737
  61. Bolondi L, Gaiani S, Li Bassi S, et al. Diagnosis of Budd–Chiari syndrome by pulsed Doppler ultrasound. Gastroenterology. 1991;100:1324–1331
  62. Ralls PW, Johnson MB, Radin DR, et al. Budd–Chiari syndrome: detection with color Doppler sonography. AJR Am J Roentgenol. 1992;159:113–116
  63. Lim AK, Patel N, Eckersley RJ, et al. Can Doppler sonography grade the severity of hepatitis C-related liver disease?. AJR Am J Roentgenol. 2005;184:1848–1853
  64. O'Donohue J, Ng C, Catnach S, et al. Diagnostic value of Doppler assessment of the hepatic and portal vessels and ultrasound of the spleen in liver disease. Eur J Gastroenterol Hepatol. 2004;16:147–155
  65. Plestina S, Pulanic R, Kralik M, et al. Color Doppler ultrasonography is reliable in assessing the risk of esophageal variceal bleeding in patients with liver cirrhosis. Wien Klin Wochenschr. 2005;117:711–717
  66. Kishimoto R, Chen M, Ogawa H, et al. Esophageal varices: evaluation with transabdominal US. Radiology. 1998;206:647–650
  67. de Vries PJ, van Hattum J, Hoekstra JB, et al. Duplex Doppler measurements of portal venous flow in normal subjects. Inter- and intra-observer variability. J Hepatol. 1991;13:358–363
  68. Bolondi L, Gaiani S, Barbara L. Accuracy and reproducibility of portal flow measurement by Doppler US. J Hepatol. 1991;13:269–273
  69. Sabba C, Weltin GG, Cicchetti DV, et al. Observer variability in echo-Doppler measurements of portal flow in cirrhotic patients and normal volunteers. Gastroenterology. 1990;98:1603–1611
  70. Smith HJ, Grottum P, Simonsen S. Ultrasonic assessment of abdominal venous return. I. Effect of cardiac action and respiration on mean velocity pattern, cross-sectional area and flow in the inferior vena cava and portal vein. Acta Radiol Diagn (Stockh). 1985;26:581–588
  71. Ohnishi K, Saito M, Nakayama T, et al. Portal venous hemodynamics in chronic liver disease: effects of posture change and exercise. Radiology. 1985;155:757–761
  72. Bolondi L, Gandolfi L, Arienti V, et al. Ultrasonography in the diagnosis of portal hypertension: diminished response of portal vessels to respiration. Radiology. 1982;142:167–172
  73. Moriyasu F, Nishida O, Ban N, et al. “Congestion index” of the portal vein. AJR Am J Roentgenol. 1986;146:735–739
  74. Doi T, Kasai C, Oohara E, et al. Studies on portal blood flow using an ultrasonic pulsed Doppler system and correlation between portal blood flow and cardiac output. [in Japanese] Rinsho Byori. 1986;34:977–980
  75. Fogteloo AJ, Smid WM, Kok T, et al. Successful treatment of veno-occlusive disease of the liver with urokinase in a patient with non-Hodgkin's lymphoma. Leukemia. 1993;7:760–763
  76. Bezzi M, Mitchell DG, Needleman L, et al. Iatrogenic aneurysmal portal–hepatic venous fistula. Diagnosis by color Doppler imaging. J Ultrasound Med. 1988;7:457–461
  77. Grant EG, Tessler FN, Gomes AS, et al. Color Doppler imaging of portosystemic shunts. AJR Am J Roentgenol. 1990;154:393–397
  78. Leeuwen M. Doppler ultrasound in the evaluation of portal hypertension. Edinburgh: Churchill Livingstone; 1990;
  79. Broide E, Farrant P, Reid F, et al. Hepatic artery resistance index can predict early death in children with biliary atresia. Liver Transpl Surg. 1997;3:604–610
  80. D'Onofrio M, Faccioli N, Zamboni G, et al. Focal liver lesions in cirrhosis: value of contrast-enhanced ultrasonography compared with Doppler ultrasound and alpha-fetoprotein levels. Radiol Med. 2008;113:978–991
  81. Quaia E, Stacul F, Gaiani S, et al. Comparison of diagnostic performance of unenhanced vs SonoVue—enhanced ultrasonography in focal liver lesions characterization. The experience of three Italian centers. Radiol Med. 2004;108:71–81
  82. Quaia E, Calliada F, Bertolotto M, et al. Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: diagnostic performance and confidence. Radiology. 2004;232:420–430
  83. Jang HJ, Kim TK, Wilson SR. Small nodules (1–2cm) in liver cirrhosis: characterization with contrast-enhanced ultrasound. Eur J Radiol. 2008;[available online 1 October 2008]
  84. Dai Y, Chen MH, Fan ZH, et al. Diagnosis of small hepatic nodules detected by surveillance ultrasound in patients with cirrhosis: comparison between contrast-enhanced ultrasound and contrast-enhanced helical computed tomography. Hepatol Res. 2008;38:281–290
  85. Forner A, Vilana R, Ayuso C, et al. Diagnosis of hepatic nodules 20mm or smaller in cirrhosis: prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology. 2008;47:97–104
  86. Lim AK, Taylor-Robinson SD, Patel N, et al. Hepatic vein transit times using a microbubble agent can predict disease severity non-invasively in patients with hepatitis C. Gut. 2005;54:128–133
  87. Blomley MJ, Lim AK, Harvey CJ, et al. Liver microbubble transit time compared with histology and Child–Pugh score in diffuse liver disease: a cross-sectional study. Gut. 2003;52:1188–1193
  88. Abbattista T, Ridolfi F, Ciabattoni E, et al. Diagnosis of liver cirrhosis by transit-time analysis at contrast-enhanced ultrasonography. Radiol Med. 2008;113:860–874
  89. Searle J, Mendelson R, Zelesco M, et al. Non-invasive prediction of the degree of liver fibrosis in patients with hepatitis C using an ultrasound contrast agent. A pilot study. J Med Imaging Radiat Oncol. 2008;52:130–133
  90. Staub F, Tournoux-Facon C, Roumy J, et al. Liver fibrosis staging with contrast-enhanced ultrasonography: prospective multicenter study compared with METAVIR scoring. Eur Radiol. 2009;
  91. Tamano M, Yoneda M, Kojima K, et al. Evaluation of esophageal varices using contrast-enhanced coded harmonic ultrasonography. J Gastroenterol Hepatol. 2004;19:572–575
  92. Sato T, Yamazaki K, Toyota J, et al. Evaluation of arterial blood flow in esophageal varices via endoscopic color Doppler ultrasonography with a galactose-based contrast agent. J Gastroenterol. 2005;40:64–69
  93. 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
  94. Sandrin L, Fourquet B, Hasquenoph JM, et al. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29:1705–1713
  95. Castera L, Forns X, Alberti A. Non-invasive evaluation of liver fibrosis using transient elastography. J Hepatol. 2008;48:835–847
  96. 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;56:968–973
  97. Kettaneh A, Marcellin P, Douvin C, et al. Features associated with success rate and performance of fibroscan measurements for the diagnosis of cirrhosis in HCV patients: a prospective study of 935 patients. J Hepatol. 2007;46:628–634
  98. Foucher J, Chanteloup E, Vergniol J, et al. Diagnosis of cirrhosis by transient elastography (fibroscan): a prospective study. Gut. 2006;55:403–408
  99. Huwart L, Sempoux C, Salameh N, et al. Liver fibrosis: noninvasive assessment with MR elastography versus aspartate aminotransferase-to-platelet ratio index. Radiology. 2007;245:458–466
  100. Friedrich-Rust M, Ong MF, Herrmann E, et al. Real-time elastography for noninvasive assessment of liver fibrosis in chronic viral hepatitis. AJR Am J Roentgenol. 2007;188:758–764
  101. Lewin M, Poujol-Robert A, Boelle PY, et al. Diffusion-weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C. Hepatology. 2007;46:658–665
  102. Frey H. Realtime elastography. A new ultrasound procedure for the reconstruction of tissue elasticity. [in German] Radiologe. 2003;43:850–855
  103. Srinivasan S, Kallel F, Ophir J. The effects of digitization on the elastographic signal-to-noise ratio. Ultrasound Med Biol. 2002;28:1521–1534
  104. Srinivasan S, Kallel F, Souchon R, et al. Analysis of an adaptive strain estimation technique in elastography. Ultrason Imaging. 2002;24:109–118
  105. Maurice RL, Bertrand M. Lagrangian speckle model and tissue-motion estimation—theory. IEEE Trans Med Imaging. 1999;18:593–603
  106. Nitta N, Yamakawa M, Shiina T. Tissue elasticity imaging based on combined autocorrelation method and 3D tissue model. Proc IEEE Ultrason Symp. 1996;2:1611–1614
  107. Yamakawa M, Shiina T. Tissue elasticity reconstruction based on 3-dimensional finite element model. Jpn J Appl Phys. 1999;38:3393–3398
  108. Yamakawa M, Shiina T. Strain estimation using the extended combined autocorrelation method. Jpn J Appl Phys. 2001;40:3872–3876
  109. Giuseppetti GM, Martegani A, Di Cioccio B, et al. Elastosonography in the diagnosis of the nodular breast lesions: preliminary report. Radiol Med. 2005;110:69–76
  110. Konig K, Scheipers U, Pesavento A, et al. Initial experiences with real-time elastography guided biopsies of the prostate. J Urol. 2005;174:115–117
  111. Lyshchik A, Higashi T, Asato R, et al. Thyroid gland tumor diagnosis at US elastography. Radiology. 2005;237:202–211
  112. Farrell RJ, Smiddy PF, Pilkington RM, et al. Guided versus blind liver biopsy for chronic hepatitis C: clinical benefits and costs. J Hepatol. 1999;30:580–587
  113. Sporea I, Sirli R, Popescu A, et al. The quality of the fragment obtained by liver biopsy for staging chronic hepatitis. J Gastrointestin Liver Dis. 2007;16:263–266
  114. Pasha T, Gabriel S, Therneau T, et al. Cost-effectiveness of ultrasound-guided liver biopsy. Hepatology. 1998;27:1220–1226
  115. Papini E, Pacella CM, Rossi Z, et al. A randomized trial of ultrasound-guided anterior subcostal liver biopsy versus the conventional Menghini technique. J Hepatol. 1991;13:291–297
  116. Lindor KD, Bru C, Jorgensen RA, et al. The role of ultrasonography and automatic-needle biopsy in outpatient percutaneous liver biopsy. Hepatology. 1996;23:1079–1083
  117. Smith JM, Cox LA, Long BW. Ultrasound evaluation of TIPS placement. Radiol Technol. 2000;71:321–325
  118. Ferral H, Foshager MC, Bjarnason H, et al. Early sonographic evaluation of the transjugular intrahepatic portosystemic shunt (TIPS). Cardiovasc Intervent Radiol. 1993;16:275–279
  119. Costa JF, Graca B, Costa A, et al. Doppler evaluation of portal hypertension: a pictorial review. Lisbon: ESGAR; 2007;

PII: S0009-9260(09)00235-9

doi: 10.1016/j.crad.2009.05.010

Clinical Radiology
Volume 64, Issue 11 , Pages 1056-1066 , November 2009