Hepatocellular carcinoma: Diagnostic criteria by imaging techniques

Best Practice and Research: Clinical Gastroenterology

Volumn 28, Issue 5, 2014, Pages 795-812

  Ronot, Maxime ^a,b,c   Vilgrain, Valérie ^a,b,c  

^a ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CENTRE DE RECHERCHE BIOMÉDICALE BICHAT BEAUJON CRB3   (France)

Author keywords

Computed tomography; Contrast enhanced ultrasound; Hepatobiliary; Hepatocellular carcinoma; Hypervascularity; Magnetic resonance imaging; Washout

Indexed keywords

CONTRAST MEDIUM; EXTRACELLULAR CONTRAST AGENT; HEPATOBILIARY CONTRAST AGENT; IRON; UNCLASSIFIED DRUG;

BILE DUCT CARCINOMA; CLASSIFICATION ALGORITHM; COMPUTER ASSISTED TOMOGRAPHY; CONTRAST ENHANCED ULTRASOUND; CONTRAST ENHANCEMENT; DIAGNOSTIC IMAGING; DIAGNOSTIC VALUE; DIFFUSION WEIGHTED IMAGING; DISEASE CLASSIFICATION; ELASTOGRAPHY; FAT CONTENT; FIBROSIS; HIGH RISK PATIENT; HUMAN; KUPFFER CELL; LIVER BIOPSY; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER METASTASIS; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PRACTICE GUIDELINE; REVIEW; SCINTIGRAPHY; CARCINOMA, HEPATOCELLULAR; DIFFERENTIAL DIAGNOSIS; ECHOGRAPHY; LIVER NEOPLASMS; PROCEDURES; REPRODUCIBILITY;

CARCINOMA, HEPATOCELLULAR; CONTRAST MEDIA; DIAGNOSIS, DIFFERENTIAL; DIAGNOSTIC IMAGING; HUMANS; LIVER NEOPLASMS; MAGNETIC RESONANCE IMAGING; REPRODUCIBILITY OF RESULTS; TOMOGRAPHY, X-RAY COMPUTED; ULTRASONOGRAPHY;

EID: 84921733535     PISSN: 15216918     EISSN: 15321916     Source Type: Journal    
DOI: 10.1016/j.bpg.2014.08.005     Document Type: Review

References (79)

1. EASL-EORTC clinical practice guidelines: Management of hepatocellular carcinoma. J Hepatol 2012; 56: 908-43.
2. Bruix J, Sherman M. Management of hepatocellular carcinoma: An update. Hepatology 2011; 53: 1020-2.
3. Omata M, Lesmana LA, Tateishi R, Chen PJ, Lin SM, Yoshida H, et al. Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma. Hepatol Int 2010; 4: 439-74.
4. Kudo M, Izumi N, Kokudo N, Matsui O, Sakamoto M, Nakashima O, et al. Management of hepatocellular carcinoma in Japan: Consensus-Based Clinical Practice Guidelines proposed by the Japan Society of Hepatology (JSH) 2010 updated version. Dig Dis 2011; 29: 339-64.
5. Kudo M. Real practice of hepatocellular carcinoma in Japan: Conclusions of the Japan Society of Hepatology 2009 Kobe Congress. Oncology 2010; 78 (Suppl. 1) : 180-8.
6. Carlos RC, Kim HM, Hussain HK, Francis IR, Nghiem HV, Fendrick AM. Developing a prediction rule to assess hepatic malignancy in patients with cirrhosis. AJR Am J Roentgenol 2003; 180: 893-900.
7. Forner A, Vilana R, Ayuso C, Bianchi L, Sole M, Ayuso JR, et al. Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 2008; 47: 97-104.
8. Luca A, Caruso S, Milazzo M, Mamone G, Marrone G, Miraglia R, et al. Multidetector-row computed tomography (MDCT) for the diagnosis of hepatocellular carcinoma in cirrhotic candidates for liver transplantation: Prevalence of radiological vascular patterns and histological correlation with liver explants. Eur Radiol 2010; 20: 898-907.
9. Marrero JA, Hussain HK, Nghiem HV, Umar R, Fontana RJ, Lok AS. Improving the prediction of hepatocellular carcinoma in cirrhotic patients with an arterially-enhancing liver mass. Liver Transpl 2005; 11: 281-9.
10. Rimola J, Forner A, Tremosini S, Reig M, Vilana R, Bianchi L, et al. Non-invasive diagnosis of hepatocellular carcinoma /=2 cm in cirrhosis. Diagnostic accuracy assessing fat, capsule and signal intensity at dynamic MRI. J Hepatol 2012; 56: 1317-23.
11. Serste T, Barrau V, Ozenne V, Vullierme MP, Bedossa P, Farges O, et al. Accuracy and disagreement of computed tomography and magnetic resonance imaging for the diagnosis of small hepatocellular carcinoma and dysplastic nodules: Role of biopsy. Hepatology 2012; 55: 800-6.
12. Liu YI, Shin LK, Jeffrey RB, Kamaya A. Quantitatively defining washout in hepatocellular carcinoma. AJR Am J Roentgenol 2013; 200: 84-9.
13. Lim JH, Choi D, Kim SH, Lee SJ, Lee WJ, Lim HK, et al. Detection of hepatocellular carcinoma: Value of adding delayed phase imaging to dual-phase helical CT. AJR Am J Roentgenol 2002; 179: 67-73.
14. Monzawa S, Ichikawa T, Nakajima H, Kitanaka Y, Omata K, Araki T. Dynamic CT for detecting small hepatocellular carcinoma: Usefulness of delayed phase imaging. AJR Am J Roentgenol 2007; 188: 147-53.
15. Yu JS, Lee JH, Chung JJ, Kim JH, Kim KW. Small hypervascular hepatocellular carcinoma: Limited value of portal and delayed phases on dynamic magnetic resonance imaging. Acta Radiol 2008; 49: 735-43.
16. Lv P, Lin XZ, Chen K, Gao J. Spectral CT in patients with small HCC: Investigation of image quality and diagnostic accuracy. Eur Radiol 2012; 22: 2117-24.
17. Marchiano A, Spreafico C, Lanocita R, Frigerio L, Di Tolla G, Patelli G, et al. Does iodine concentration affect the diagnostic efficacy of biphasic spiral CT in patients with hepatocellular carcinoma? Abdom Imaging 2005; 30: 274-80.
18. Earls JP, Rofsky NM, DeCorato DR, Krinsky GA, Weinreb JC. Hepatic arterial-phase dynamic gadolinium-enhanced MR imaging: Optimization with a test examination and a power injector. Radiology 1997; 202: 268-73.
19. Kitao A, Matsui O, Yoneda N, Kozaka K, Shinmura R, KodaW, et al. The uptake transporter OATP8 expression decreases during multistep hepatocarcinogenesis: Correlation with gadoxetic acid enhanced MR imaging. Eur Radiol 2011; 21: 2056-66.
20. Kitao A, Zen Y, Matsui O, Gabata T, Kobayashi S, KodaW, et al. Hepatocellular carcinoma: Signal intensity at gadoxetic acidenhanced MR imagingecorrelation with molecular transporters and histopathologic features. Radiology 2010; 256: 817-26.
21. Bashir MR, Breault SR, Braun R, Do RK, Nelson RC, Reeder SB. Optimal timing and diagnostic adequacy of hepatocyte phase imaging with gadoxetate-enhanced liver MRI. Acad Radiol 2014; 21: 726-32.
22. Nakamura Y, Toyota N, Date S, Oda S, Namimoto T, Yamashita Y, et al. Clinical significance of the transitional phase at gadoxetate disodium-enhanced hepatic MRI for the diagnosis of hepatocellular carcinoma: Preliminary results. J Comput Assist Tomogr 2011; 35: 723-7.
23. Claudon M, Dietrich CF, Choi BI, Cosgrove DO, Kudo M, Nolsoe CP, et al. Guidelines and good clinical practice recommendations for Contrast Enhanced Ultrasound (CEUS) in the liver - update 2012: A WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultrasound Med Biol 2013; 39: 187-210.
24. Roskams T, Kojiro M. Pathology of early hepatocellular carcinoma: Conventional and molecular diagnosis. Semin Liver Dis 2010; 30: 17-25.
25. Grazioli L, Olivetti L, Fugazzola C, Benetti A, Stanga C, Dettori E, et al. The pseudocapsule in hepatocellular carcinoma: Correlation between dynamic MR imaging and pathology. Eur Radiol 1999; 9: 62-7.
26. Ishigami K, Yoshimitsu K, Nishihara Y, Irie H, Asayama Y, Tajima T, et al. Hepatocellular carcinoma with a pseudocapsule on gadolinium-enhanced MR images: Correlation with histopathologic findings. Radiology 2009; 250: 435-43.
27. Lim JH, Choi D, Park CK, Lee WJ, Lim HK. Encapsulated hepatocellular carcinoma: CT-pathologic correlations. Eur Radiol 2006; 16: 2326-33.
28. Takayasu K, Furukawa H, Wakao F, Muramatsu Y, Abe H, Terauchi T, et al. CT diagnosis of early hepatocellular carcinoma: Sensitivity, findings, and CT-pathologic correlation. AJR Am J Roentgenol 1995; 164: 885-90.
29. Kim MJ. Current limitations and potential breakthroughs for the early diagnosis of hepatocellular carcinoma. Gut Liver 2011; 5: 15-21.
30. Rosenkrantz AB, Lee L, Matza BW, Kim S. Infiltrative hepatocellular carcinoma: Comparison of MRI sequences for lesion conspicuity. Clin Radiol 2012; 67: E105-11.
31. Kanematsu M, Semelka RC, Leonardou P, Mastropasqua M, Lee JK. Hepatocellular carcinoma of diffuse type: MR imaging findings and clinical manifestations. J Magn Reson Imaging 2003; 18: 189-95.
32. Khan AS, Hussain HK, Johnson TD, Weadock WJ, Pelletier SJ, Marrero JA. Value of delayed hypointensity and delayed enhancing rim in magnetic resonance imaging diagnosis of small hepatocellular carcinoma in the cirrhotic liver. J Magn Reson Imaging 2010; 32: 360-6.
33. Sano K, Ichikawa T, Motosugi U, Sou H, Muhi AM, Matsuda M, et al. Imaging study of early hepatocellular carcinoma: Usefulness of gadoxetic acid-enhanced MR imaging. Radiology 2011; 261: 834-44.
34. Choi JW, Lee JM, Kim SJ, Yoon JH, Baek JH, Han JK, et al. Hepatocellular carcinoma: Imaging patterns on gadoxetic acidenhanced MR images and their value as an imaging biomarker. Radiology 2013; 267: 776-86.
35. Kim MJ, Lee M, Choi JY, Park YN. Imaging features of small hepatocellular carcinomas with microvascular invasion on gadoxetic acid-enhanced MR imaging. Eur J Radiol 2012; 81: 2507-12.
36. Lee MH, Kim SH, Park MJ, Park CK, Rhim H. Gadoxetic acid-enhanced hepatobiliary phase MRI and high-b-value diffusionweighted imaging to distinguish well-differentiated hepatocellular carcinomas from benign nodules in patients with chronic liver disease. AJR Am J Roentgenol 2011; 197: W868-75.
37. Hyodo T, Murakami T, Imai Y, Okada M, Hori M, Kagawa Y, et al. Hypovascular nodules in patients with chronic liver disease: Risk factors for development of hypervascular hepatocellular carcinoma. Radiology 2013; 266: 480-90.
38. Motosugi U, Ichikawa T, Sano K, Sou H, Onohara K, Muhi A, et al. Outcome of hypovascular hepatic nodules revealing no gadoxetic acid uptake in patients with chronic liver disease. J Magn Reson Imaging 2011; 34: 88-94.
39. Akai H, Matsuda I, Kiryu S, Tajima T, Takao H, Watanabe Y, et al. Fate of hypointense lesions on Gd-EOB-DTPA-enhanced magnetic resonance imaging. Eur J Radiol 2012; 81: 2973-7.
40. Leoni S, Piscaglia F, Golfieri R, Camaggi V, Vidili G, Pini P, et al. The impact of vascular and nonvascular findings on the noninvasive diagnosis of small hepatocellular carcinoma based on the EASL and AASLD criteria. Am J Gastroenterol 2010; 105: 599-609.
41. Arita J, Hasegawa K, Takahashi M, Hata S, Shindoh J, Sugawara Y, et al. Correlation between contrast-enhanced intraoperative ultrasound using Sonazoid and histologic grade of resected hepatocellular carcinoma. AJR Am J Roentgenol 2011; 196: 1314-21.
42. Pupulim LF, Felce-Dachez M, Paradis V, Vullierme MP, Zappa M, Bedossa P, et al. Algorithm for immediate cytologic diagnosis of hepatic tumors. AJR Am J Roentgenol 2008; 190: W208-212.
43. Young AL, Lodge JP. Needle-track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: A systematic review and meta-analysis. Gut 2009; 58: 887-8.
44. Rode A, Bancel B, Douek P, Chevallier M, Vilgrain V, Picaud G, et al. Small nodule detection in cirrhotic livers: Evaluation with US, spiral CT, and MRI and correlation with pathologic examination of explanted liver. J Comput Assist Tomogr 2001; 25: 327-36.
45. Kim YK, Kim CS, Chung GH, Han YM, Lee SY, Chon SB, et al. Comparison of gadobenate dimeglumine-enhanced dynamic MRI and 16-MDCT for the detection of hepatocellular carcinoma. AJR Am J Roentgenol 2006; 186: 149-57.
46. Ahn SS, Kim MJ, Lim JS, Hong HS, Chung YE, Choi JY. Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 2010; 255: 459-66.
47. Golfieri R, Renzulli M, Lucidi V, Corcioni B, Trevisani F, Bolondi L. Contribution of the hepatobiliary phase of Gd-EOB-DTPAenhanced MRI to dynamic MRI in the detection of hypovascular small (
48. Marin D, Di Martino M, Guerrisi A, De Filippis G, Rossi M, Ginanni Corradini S, et al. Hepatocellular carcinoma in patients with cirrhosis: Qualitative comparison of gadobenate dimeglumine-enhanced MR imaging and multiphasic 64-section CT. Radiology 2009; 251: 85-95.
49. Boozari B, Soudah B, Rifai K, Schneidewind S, Vogel A, Hecker H, et al. Grading of hypervascular hepatocellular carcinoma using late phase of contrast enhanced sonography - A prospective study. Dig Liver Dis 2011; 43: 484-90.
50. Chen MH, Dai Y, Yan K, Fan ZH, Yin SS, Yang W, et al. The role of contrast-enhanced ultrasound on the diagnosis of small hepatocellular carcinoma (/=3 cm) in patients with cirrhosis Hepatol Res 2006 35 281-288
51. Vilana R, Forner A, Bianchi L, Garcia-Criado A, Rimola J, de Lope CR, et al. Intrahepatic peripheral cholangiocarcinoma in cirrhosis patients may display a vascular pattern similar to hepatocellular carcinoma on contrast-enhanced ultrasound. Hepatology 2010; 51: 2020-9.
52. Ho CL, Chen S, Yeung DW, Cheng TK. Dual-tracer PET/CT imaging in evaluation of metastatic hepatocellular carcinoma. J Nucl Med 2007; 48: 902-9.
53. Hennedige T, Venkatesh SK. Imaging of hepatocellular carcinoma: Diagnosis, staging and treatment monitoring. Cancer Imaging 2013; 12: 530-47.
54. Taouli B, Johnson RS, Hajdu CH, Oei MT, Merad M, Yee H, et al. Hepatocellular carcinoma: Perfusion quantification with dynamic contrast-enhanced MRI. AJR Am J Roentgenol 2013; 201: 795-800.
55. Ippolito D, Sironi S, Pozzi M, Antolini L, Ratti L, Meloni F, et al. Perfusion computed tomographic assessment of early hepatocellular carcinoma in cirrhotic liver disease: Initial observations. J Comput Assist Tomogr 2008; 32: 855-8.
56. Ippolito D, Sironi S, Pozzi M, Antolini L, Ratti L, Alberzoni C, et al. Hepatocellular carcinoma in cirrhotic liver disease: Functional computed tomography with perfusion imaging in the assessment of tumor vascularization. Acad Radiol 2008; 15: 919-27.
57. Takahashi N, Yoshioka H, Yamaguchi M, Saida Y, Itai Y. Accelerated dynamic MR imaging with a parallel imaging technique for hypervascular hepatocellular carcinomas: Usefulness of a test bolus in examination and subtraction imaging. J Magn Reson Imaging 2003; 18: 80-9.
58. Alicioglu B, Guler O, Bulakbasi N, Akpinar S, Tosun O, Comunoglu C. Utility of semiquantitative parameters to differentiate benign and malignant focal hepatic lesions. Clin Imaging 2013; 37: 692-6.
59. Sahani DV, Holalkere N-S, Mueller PR, Zhu AX. Advanced hepatocellular carcinoma: CT perfusion of liver and tumor tissueeinitial experience. Radiology 2007; 243: 736-43.
60. Wu LM, Xu JR, Lu Q, Hua J, Chen J, Hu J. A pooled analysis of diffusion-weighted imaging in the diagnosis of hepatocellular carcinoma in chronic liver diseases. J Gastroenterol Hepatol 2013; 28: 227-34.
61. Vandecaveye V, De Keyzer F, Verslype C, Op de Beeck K, Komuta M, Topal B, et al. Diffusion-weighted MRI provides additional value to conventional dynamic contrast-enhanced MRI for detection of hepatocellular carcinoma. Eur Radiol 2009; 19: 2456-66.
62. Piana G, Trinquart L, Meskine N, Barrau V, Beers BV, Vilgrain V. New MR imaging criteria with a diffusion-weighted sequence for the diagnosis of hepatocellular carcinoma in chronic liver diseases. J Hepatol 2011; 55: 126-32.
63. Park MS, Kim S, Patel J, Hajdu CH, Do RK, Mannelli L, et al. Hepatocellular carcinoma: Detection with diffusion-weighted versus contrast-enhanced magnetic resonance imaging in pretransplant patients. Hepatology 2012; 56: 140-8.
64. Nakanishi M, Chuma M, Hige S, Omatsu T, Yokoo H, Nakanishi K, et al. Relationship between diffusion-weighted magnetic resonance imaging and histological tumor grading of hepatocellular carcinoma. Ann Surg Oncol 2012; 19: 1302-9.
65. Catalano OA, Choy G, Zhu A, Hahn PF, Sahani DV. Differentiation of malignant thrombus from bland thrombus of the portal vein in patients with hepatocellular carcinoma: Application of diffusion-weighted MR imaging. Radiology 2010; 254: 154-62.
66. Morii K, Nakamura S, Yamamoto T, Okushin H. Steatotic regenerative nodules mimicking hepatocellular carcinoma. Liver Int 2013 Jun 19. http://dx.doi.org/10.1111/liv.12256 [Epub ahead of print].
67. Siripongsakun S, Lee JK, Raman SS, Tong MJ, Sayre J, Lu DS. MRI detection of intratumoral fat in hepatocellular carcinoma: Potential biomarker for a more favorable prognosis. AJR Am J Roentgenol 2012; 199: 1018-25.
68. Kadoya M, Matsui O, Takashima T, Nonomura A. Hepatocellular carcinoma: Correlation of MR imaging and histopathologic findings. Radiology 1992; 183: 819-25.
69. Ebara M, Fukuda H, Kojima Y, Morimoto N, Yoshikawa M, Sugiura N, et al. Small hepatocellular carcinoma: Relationship of signal intensity to histopathologic findings and metal content of the tumor and surrounding hepatic parenchyma. Radiology 1999; 210: 81-8.
70. Lee KH, O'Malley ME, Haider MA, Hanbidge A. Triple-phase MDCT of hepatocellular carcinoma. AJR Am J Roentgenol 2004; 182: 643-9.
71. Kita R, Sakamoto A, Nagata Y, Nishijima N, Ikeda A, Matsuo H, et al. Visualization of blood drainage area from hypervascular hepatocellular carcinoma on ultrasonographic images during hepatic arteriogram: Comparison with depiction of drainage area on contrast-enhanced ultrasound. Hepatol Res 2012; 42: 999-1007.
72. Nishie A, Yoshimitsu K, Asayama Y, Irie H, Tajima T, Hirakawa M, et al. Radiologic detectability of minute portal venous invasion in hepatocellular carcinoma. AJR Am J Roentgenol 2008; 190: 81-7.
73. Miyata R, Tanimoto A, Wakabayashi G, Shimazu M, Nakatsuka S, Mukai M, et al. Accuracy of preoperative prediction of microinvasion of portal vein in hepatocellular carcinoma using superparamagnetic iron oxide-enhanced magnetic resonance imaging and computed tomography during hepatic angiography. J Gastroenterol 2006; 41: 987-95.
74. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001; 35: 421-30.
75. Greten TF, Malek NP, Schmidt S, Arends J, Bartenstein P, Bechstein W, et al. Diagnosis of and therapy for hepatocellular carcinoma. Z fur Gastroenterol 2013; 51: 1269-326.
76. Yu NC, Chaudhari V, Raman SS, Lassman C, Tong MJ, Busuttil RW, et al. CT and MRI improve detection of hepatocellular carcinoma, compared with ultrasound alone, in patients with cirrhosis. Clin Gastroenterol Hepatol 2011; 9: 161-7.
77. Radiology ACo. Liver imaging reporting and data system version v 2013.1; May 12 2014. Available from: Http://www.acr.org/Quality-Safety/Resources/LIRADS/.
78. Bota S, Piscaglia F, Marinelli S, Pecorelli A, Terzi E, Bolondi L. Comparison of international guidelines for noninvasive diagnosis of hepatocellular carcinoma. Liver Cancer 2012; 1: 190-200.
79. Davenport MS, Khalatbari S, Liu PS, Maturen KE, Kaza RK,Wasnik AP, et al. Repeatability of diagnostic features and scoring systems for hepatocellular carcinoma by using MR imaging. Radiology 2014; 272: 132-42.