Liver fibrosis, cirrhosis, and cirrhosis-related nodules: Imaging diagnosis and surveillance.

Although biological scores and elastography continue to yield the best results, imaging retains a crucial role in the diagnosis of liver fibrosis and cirrhosis. First, digestive symptoms or biological liver test abnormalities often lead the referring physician to request an abdominal ultrasound, and with an experienced operator, accuracy of ultrasound can reach 85% for the diagnosis of severe fibrosis or cirrhosis. Second, imaging could lead to discovery of nonsymptomatic fibrosis or cirrhosis, with an estimated prevalence of 0.5-2.8% in the population. After diagnosis, imaging is central in the follow-up of cirrhosis. It is used to detect worsening of portal hypertension and hepatocellular carcinoma (HCC). Because many nodules are present in a cirrhotic liver, familiarity with the features of HCC can facilitate noninvasive diagnosis and early and accurate treatment.

[1]  M. Colombo,et al.  Clinical and economical impact of 2010 AASLD guidelines for the diagnosis of hepatocellular carcinoma. , 2014, Journal of hepatology.

[2]  Fabrice Carrat,et al.  Liver biopsy: the best, not the gold standard. , 2009, Journal of hepatology.

[3]  D G Mitchell,et al.  Enlargement of hilar periportal space: A sign of early cirrhosis at MR imaging , 2000, Journal of magnetic resonance imaging : JMRI.

[4]  S. Sourbron Technical aspects of MR perfusion. , 2010, European journal of radiology.

[5]  Baojun Li,et al.  Using texture analyses of contrast enhanced CT to assess hepatic fibrosis. , 2016, European journal of radiology.

[6]  J. Bruix,et al.  Management of hepatocellular carcinoma: An update , 2011, Hepatology.

[7]  Julien Vergniol,et al.  Liver stiffness in nonalcoholic fatty liver disease: A comparison of supersonic shear imaging, FibroScan, and ARFI with liver biopsy , 2016, Hepatology.

[8]  Steven Solga,et al.  Can imaging modalities diagnose and stage hepatic fibrosis and cirrhosis accurately? , 2009, Journal of hepatology.

[9]  T. Kim,et al.  CEUS: An essential component in a multimodality approach to small nodules in patients at high-risk for hepatocellular carcinoma. , 2015, European journal of radiology.

[10]  D. Conte,et al.  Severe liver fibrosis or cirrhosis: accuracy of US for detection--analysis of 300 cases. , 2003, Radiology.

[11]  B. Choi,et al.  Nontumorous arterioportal shunt mimicking hypervascular tumor in cirrhotic liver: two-phase spiral CT findings. , 1998, Radiology.

[12]  J. Marrero,et al.  The challenge of prognosis and staging for hepatocellular carcinoma. , 2010, The oncologist.

[13]  R. Gaba,et al.  Outcomes of transjugular intrahepatic portosystemic shunt creation for flow-enabled dissolution of spleno-mesenterico-portal venous thrombosis. , 2016, Diagnostic and interventional imaging.

[14]  W D Carey,et al.  The role of liver biopsy in chronic hepatitis C , 2001, Hepatology.

[15]  J. Babb,et al.  Technical Failure of MR Elastography Examinations of the Liver: Experience from a Large Single-Center Study. , 2017, Radiology.

[16]  D. Mitchell,et al.  Right posterior hepatic notch sign: A simple diagnostic MR finding of cirrhosis , 2003, Journal of magnetic resonance imaging : JMRI.

[17]  K. Nouso,et al.  Measurement of spleen stiffness by acoustic radiation force impulse imaging identifies cirrhotic patients with esophageal varices. , 2013, Gastroenterology.

[18]  Diagnosis of Liver Cirrhosis with US: Receiver-Operating Characteristic Analysis of Multidimensional Caudate Lobe Indexes , 1989 .

[19]  M. Ronot,et al.  Prospective comparison of spleen and liver stiffness by using shear-wave and transient elastography for detection of portal hypertension in cirrhosis. , 2015, Radiology.

[20]  G. D’Amico,et al.  Noninvasive markers of esophageal varices: Another round, not the last , 2004, Hepatology.

[21]  S. Ahn,et al.  A Novel Model to Predict Esophageal Varices in Patients with Compensated Cirrhosis Using Acoustic Radiation Force Impulse Elastography , 2015, PloS one.

[22]  K. Nouso,et al.  Portal Hypertension in Patients with Liver Cirrhosis: Diagnostic Accuracy of Spleen Stiffness. , 2016, Radiology.

[23]  Jae Young Lee,et al.  Esophageal varices in patients with cirrhosis: multidetector CT esophagography--comparison with endoscopy. , 2007, Radiology.

[24]  Christophe Aubé,et al.  Imaging modalities for the diagnosis of hepatic fibrosis and cirrhosis. , 2015, Clinics and research in hepatology and gastroenterology.

[25]  Y. Arai,et al.  Successful balloon-occluded retrograde transvenous obliteration for bleeding duodenal varices using cyanoacrylate. , 2013, World journal of gastroenterology.

[26]  H. Schulz,et al.  Sister Mary Joseph's nodule as the first sign of pregnancy-associated gastric cancer: a case report. , 2008, World journal of gastroenterology.

[27]  S. Sharma,et al.  Ultrasonic diagnosis of cirrhosis: Reference to quantitative measurements of hepatic dimensions , 2005, Gastrointestinal Radiology.

[28]  A. Luciani,et al.  Liver Cirrhosis : Intravoxel Incoherent Motion MR Imaging — Pilot Study 1 , 2008 .

[29]  C. Aubé,et al.  Coexistence d’un carcinome hépato-cellulaire et d’une métastase hépatique , 2006 .

[30]  F. Terrier,et al.  Treatment of gastrointestinal hemorrhage , 2005, Abdominal Imaging.

[31]  Eun Sun Lee,et al.  Hepatic fibrosis: prospective comparison of MR elastography and US shear-wave elastography for evaluation. , 2014, Radiology.

[32]  L. Castéra Transient elastography and other noninvasive tests to assess hepatic fibrosis in patients with viral hepatitis , 2009, Journal of viral hepatitis.

[33]  M. Zeng,et al.  MR comparative study of combined hepatocellular-cholangiocarcinoma in normal, fibrotic, and cirrhotic livers , 2016, Abdominal Radiology.

[34]  Y. Ngo,et al.  Open Access Research Article Prevalence of Liver Fibrosis and Risk Factors in a General Population Using Non-invasive Biomarkers (fibrotest) , 2022 .

[35]  Thorsten Feiweier,et al.  Diffusion-weighted imaging of the liver with multiple b values: effect of diffusion gradient polarity and breathing acquisition on image quality and intravoxel incoherent motion parameters--a pilot study. , 2013, Radiology.

[36]  Riccardo Lencioni,et al.  EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. , 2012, Journal of hepatology.

[37]  M. Kaplan,et al.  Regression of Hepatic Fibrosis in Hepatitis C with Long-Term Interferon Treatment , 1998, Digestive Diseases and Sciences.

[38]  P. Nahon,et al.  [Screening of hepatocellular carcinoma and surveillance of patients with cirrhosis: a public health issue]. , 2013, La Revue du praticien.

[39]  Carlo Catalano,et al.  Hepatocellular carcinoma in cirrhotic patients: prospective comparison of US, CT and MR imaging , 2013, European Radiology.

[40]  M. Lupsor,et al.  Performance of Acoustic Radiation Force Impulse imaging for the staging of liver fibrosis: a pooled meta‐analysis , 2012, Journal of viral hepatitis.

[41]  Richard L Ehman,et al.  MR elastography for the assessment of hepatic fibrosis in patients with chronic hepatitis B infection: does histologic necroinflammation influence the measurement of hepatic stiffness? , 2014, Radiology.

[42]  Min Ju Kim,et al.  Non-invasive assessment of liver fibrosis using acoustic structure quantification: comparison with transient elastography in chronic viral hepatitis , 2016, Abdominal Radiology.

[43]  C. Aubé,et al.  Liver fibrosis in patients with non-alcoholic fatty liver disease: diagnostic options in clinical practice. , 2012, Expert opinion on medical diagnostics.

[44]  C. Aubé,et al.  New Doppler ultrasound signs improve the non-invasive diagnosis of cirrhosis or severe liver fibrosis , 2004, European journal of gastroenterology & hepatology.

[45]  U. Schmiedl,et al.  Diagnosis of liver cirrhosis with US: receiver-operating characteristic analysis of multidimensional caudate lobe indexes. , 1989, Radiology.

[46]  Y. Ohno,et al.  CT hepatic perfusion measurement: comparison of three analytic methods. , 2012, European journal of radiology.

[47]  R. Loffroy,et al.  Transjugular intrahepatic portosystemic shunt for acute variceal gastrointestinal bleeding: Indications, techniques and outcomes. , 2015, Diagnostic and interventional imaging.

[48]  Julien Vergniol,et al.  Diagnostic accuracy and prognostic significance of blood fibrosis tests and liver stiffness measurement by FibroScan in non-alcoholic fatty liver disease. , 2016, Journal of hepatology.

[49]  D. Marin,et al.  Enhancement pattern of small hepatocellular carcinoma (HCC) at contrast-enhanced US (CEUS), MDCT, and MRI: intermodality agreement and comparison of diagnostic sensitivity between 2005 and 2010 American Association for the Study of Liver Diseases (AASLD) guidelines. , 2012, European journal of radiology.

[50]  P. Kim,et al.  Liver Imaging Reporting and Data System v2014 With Gadoxetate Disodium–Enhanced Magnetic Resonance Imaging: Validation of LI-RADS Category 4 and 5 Criteria , 2016, Investigative radiology.

[51]  D. Mitchell,et al.  Hepatic morphologic changes in cirrhosis: MR imaging findings , 2000, Abdominal Imaging.

[52]  C. Liang,et al.  Intravoxel Incoherent Motion MR Imaging for Staging of Hepatic Fibrosis , 2016, PloS one.

[53]  L. Bolondi,et al.  Value of measurement of mean portal flow velocity by Doppler flowmetry in the diagnosis of portal hypertension. , 1992, Journal of hepatology.

[54]  R. Semelka,et al.  Chronic hepatitis: Correlation of early patchy and late linear enhancement patterns on gadolinium‐enhanced MR images with histopathology initial experience , 2001, Journal of magnetic resonance imaging : JMRI.

[55]  Ming-de Lu,et al.  Assessment of liver fibrosis in chronic hepatitis B using acoustic structure quantification: quantitative morphological ultrasound , 2016, European Radiology.

[56]  I Bricault,et al.  Ultrasonographic assessment of liver fibrosis with computer-assisted analysis of liver surface irregularities. , 2015, Diagnostic and interventional imaging.

[57]  C. Aubé,et al.  Portosystemic collateral vessels in liver cirrhosis: a three-dimensional MDCT pictorial review , 2012, Abdominal Radiology.

[58]  M. Topbaş,et al.  Diagnostic performance of using effervescent powder for detection and grading of esophageal varices by multi-detector computed tomography. , 2014, European journal of radiology.

[59]  S Franchi-Abella,et al.  Ultrasound elastography: advantages, limitations and artefacts of the different techniques from a study on a phantom. , 2013, Diagnostic and interventional imaging.

[60]  S. Roman,et al.  Noninvasive diagnosis and prognosis of liver cirrhosis: a comparison of biological scores, elastometry, and metabolic liver function tests , 2010, European journal of gastroenterology & hepatology.

[61]  Julien Vergniol,et al.  Non-invasive assessment of liver fibrosis with impulse elastography: comparison of Supersonic Shear Imaging with ARFI and FibroScan®. , 2014, Journal of hepatology.

[62]  L. Bolondi,et al.  The Impact of Vascular and Nonvascular Findings on the Noninvasive Diagnosis of Small Hepatocellular Carcinoma Based on the EASL and AASLD Criteria , 2010, The American Journal of Gastroenterology.

[63]  Pierre-Yves Boëlle,et al.  Diffusion‐weighted magnetic resonance imaging for the assessment of fibrosis in chronic hepatitis C , 2007, Hepatology.

[64]  J. Dumortier,et al.  Shear wave elastography: An accurate technique to stage liver fibrosis in chronic liver diseases. , 2016, Diagnostic and interventional imaging.

[65]  C. Aubé,et al.  Screening for significant chronic liver disease by using three simple ultrasound parameters. , 2015, European journal of radiology.

[66]  J. Bruix,et al.  Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma , 2007, Hepatology.

[67]  Hepatic artery resistance in alcoholic liver disease , 1998, Hepatology.

[68]  Lu Wang,et al.  Development of a quantitative method for the diagnosis of cirrhosis , 2011, Scandinavian journal of gastroenterology.

[69]  G. Hunault,et al.  Improved fibrosis staging by elastometry and blood test in chronic hepatitis C , 2014, Liver international : official journal of the International Association for the Study of the Liver.

[70]  Shinn-Jang Hwang,et al.  Gall‐bladder wall thickening in patients with liver cirrhosis , 1997, Journal of gastroenterology and hepatology.

[71]  J. Fruit,et al.  The role of liver biopsy in chronic hepatitis C , 2002 .

[72]  Sung Ho Hwang,et al.  Nontumorous arterioportal shunts in the liver: CT and MRI findings considering mechanisms and fate , 2010, European Radiology.

[73]  G. Parisi,et al.  Clinical relevance of colonic lesions in cirrhotic patients with portal hypertension , 2006, Endoscopy.

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

[75]  N. Afdhal,et al.  Diagnosis and quantitation of fibrosis. , 2008, Gastroenterology.

[76]  R Sinkus,et al.  CONTINUING EDUCATION PROGRAM : FOCUS . . . Can we justify not doing liver perfusion imaging in 2013 ? , 2013 .

[77]  V. Vilgrain,et al.  Ultrasonographic surveillance of hepatocellular carcinoma in cirrhosis: A randomized trial comparing 3‐ and 6‐month periodicities , 2011, Hepatology.

[78]  V. Vilgrain,et al.  Cirrhosis: CT and MR imaging evaluation. , 2007, European journal of radiology.

[79]  Kemal Arda,et al.  Hepatic vein Doppler waveform changes in early stage (Child‐Pugh A) chronic parenchymal liver disease , 1997, Journal of clinical ultrasound : JCU.

[80]  Jae Young Lee,et al.  Hepatic Steatosis: Assessment with Acoustic Structure Quantification of US Imaging. , 2016, Radiology.

[81]  G. D’Amico,et al.  Natural history. Clinical-haemodynamic correlations. Prediction of the risk of bleeding. , 1997, Bailliere's clinical gastroenterology.

[82]  Shinn-Jang Hwang,et al.  Simple blood tests can predict compensated liver cirrhosis in patients with chronic hepatitis C. , 2002, Hepato-gastroenterology.

[83]  G. Baron,et al.  Liver fibrosis in chronic hepatitis C virus infection: differentiating minimal from intermediate fibrosis with perfusion CT. , 2010, Radiology.

[84]  L. Bolondi Screening for hepatocellular carcinoma in cirrhosis. , 2003, Journal of hepatology.

[85]  C. Radu,et al.  Non‐invasive ménage à trois for the prediction of high‐risk varices: stepwise algorithm using lok score, liver and spleen stiffness , 2015, Liver international : official journal of the International Association for the Study of the Liver.

[86]  Ivan Bricault,et al.  EASL and AASLD recommendations for the diagnosis of HCC to the test of daily practice , 2017, Liver international (Print).

[87]  Vincent Mallet,et al.  Chronic Liver Disease: Systemic and Splanchnic Venous Flow Mapping with Optimized Cine Phase-Contrast MR Imaging Validated in a Phantom Model and Prospectively Evaluated in Patients1 , 2011 .

[88]  S. Ko,et al.  Diffuse Gallbladder Wall Thickening on Computed Tomography in Patients With Liver Cirrhosis: Correlation With Clinical and Laboratory Variables , 2011, Journal of computer assisted tomography.

[89]  M. Tzalonikou,et al.  Cirrhosis: spectrum of findings on unenhanced and dynamic gadolinium-enhanced MR imaging , 2001 .

[90]  E. Vittinghoff,et al.  Esophageal varices on computed tomography and subsequent variceal hemorrhage , 2013, Abdominal Imaging.

[91]  Laurent Castera,et al.  Non-invasive evaluation of liver fibrosis using transient elastography. , 2008, Journal of hepatology.

[92]  S. Taylor-Robinson,et al.  Liver microbubble transit time compared with histology and Child-Pugh score in diffuse liver disease: a cross sectional study , 2003, Gut.

[93]  M. V. van Oijen,et al.  Surveillance for hepatocellular carcinoma is associated with increased survival: Results from a large cohort in the Netherlands. , 2015, Journal of hepatology.

[94]  R. Groszmann,et al.  American association for the study of liver diseases , 1992 .

[95]  Segment 4 (The Quadrate Lobe): A Barometer of Cirrhotic Liver Disease at US , 1998 .

[96]  R Sinkus,et al.  [Diffusion-weighted MR imaging of the liver]. , 2010, Journal de radiologie.

[97]  C. Aubé,et al.  Direct percutaneous approach for endoluminal glue embolization of stomal varices. , 2008, Journal of vascular and interventional radiology : JVIR.

[98]  G. Labbadia,et al.  Ultrasound evaluation of liver fibrosis: preliminary experience with acoustic structure quantification (ASQ) software , 2013, La radiologia medica.

[99]  L. Forzenigo,et al.  The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis , 2009, Gut.

[100]  D. Harnois The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis , 2010 .

[101]  Guy Cloutier,et al.  Ultrasound Elastography and MR Elastography for Assessing Liver Fibrosis: Part 1, Principles and Techniques. , 2015, AJR. American journal of roentgenology.

[102]  J. Bosch,et al.  Early use of TIPS in patients with cirrhosis and variceal bleeding , 2010, Annals of Internal Medicine.

[103]  Ramon Planas,et al.  Beta-blockers to prevent gastroesophageal varices in patients with cirrhosis. , 2005, The New England journal of medicine.

[104]  Hiroyuki Hachiya,et al.  A pilot approach for quantitative assessment of liver fibrosis using ultrasound: preliminary results in 79 cases. , 2006, Journal of hepatology.

[105]  V. Mazzaferro,et al.  EASL-EORTC Clinical Practice Guidelines: Management of hepatocellular carcinoma European Association for the Study of the Liver ⇑ , European Organisation for Research and Treatment of Cancer , 2012 .

[106]  Bin Zhang,et al.  Liver Stiffness Measurements with MR Elastography: Agreement and Repeatability across Imaging Systems, Field Strengths, and Pulse Sequences. , 2016, Radiology.

[107]  Jeong Min Lee,et al.  Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma , 2010, Hepatology international.

[108]  L. Bolondi,et al.  What is the criterion for differentiating chronic hepatitis from compensated cirrhosis? A prospective study comparing ultrasonography and percutaneous liver biopsy. , 1997, Journal of hepatology.

[109]  M. Reiser,et al.  Diffusion‐weighted MRI of the abdomen: Current value in clinical routine , 2013, Journal of magnetic resonance imaging : JMRI.

[110]  Zhao-You Tang,et al.  Randomized controlled trial of screening for hepatocellular carcinoma , 2004, Journal of Cancer Research and Clinical Oncology.

[111]  Guy Cloutier,et al.  Ultrasound Elastography and MR Elastography for Assessing Liver Fibrosis: Part 2, Diagnostic Performance, Confounders, and Future Directions. , 2015, AJR. American journal of roentgenology.

[112]  Z. Ben‐Ari,et al.  [Non-invasive assessment of liver fibrosis]. , 2015, Harefuah.

[113]  V. de Lédinghen,et al.  Liver and spleen elastography using supersonic shear imaging for the non-invasive diagnosis of cirrhosis severity and oesophageal varices. , 2015, Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver.

[114]  Armando Manduca,et al.  Hepatic MR Elastography: Clinical Performance in a Series of 1377 Consecutive Examinations. , 2016, Radiology.

[115]  Peng Zhang,et al.  Quantitative Detection of Cirrhosis: Towards the Development of Computer-Assisted Detection Method , 2014, Journal of Digital Imaging.