Semin Liver Dis 2005; 25(2): 162-170
DOI: 10.1055/s-2005-871196
Copyright © 2005 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Imaging Diagnosis

Riccardo Lencioni1 , 2 , Dania Cioni2 , Clotilde Della Pina2 , Laura Crocetti2 , Carlo Bartolozzi2
  • 1Professor, Division of Diagnostic and Interventional Radiology, Department of Oncology, Transplants and Advanced Technologies in Medicine, University of Pisa, Pisa, Italy
  • 2Division of Diagnostic and Interventional Radiology, Department of Oncology, Transplants and Advanced Technologies in Medicine, University of Pisa, Pisa, Italy
Further Information

Publication History

Publication Date:
25 May 2005 (online)

ABSTRACT

The diagnosis of hepatocellular carcinoma (HCC) is based on imaging examinations in combination with clinical and laboratory findings. Despite technological advances, imaging cirrhotic patients remains a challenging issue because nonmalignant hepatocellular lesions, such as dysplastic nodules, mimic a small HCC. One of the key pathologic factors for differential diagnosis that is reflected in imaging appearances is the vascular supply to the lesion. It is accepted that imaging techniques may establish the diagnosis of HCC in nodules larger than 2 cm showing characteristic arterial hypervascularization. In lesions ranging from 1 to 2 cm, biopsy is still recommended, although a negative response can never be used to rule out malignancy completely. Although ultrasonography is widely accepted for HCC surveillance, spiral computed tomography (CT) or dynamic magnetic resonance imaging is required for diagnostic confirmation and intrahepatic tumor staging. These examinations have replaced invasive procedures, such as lipiodol CT, but remain relatively insensitive for the detection of tiny HCC lesions and tumor vascular invasion into peripheral portal vein branches.

REFERENCES

  • 1 Bruix J, Sherman M, Llovet J M 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;  35 421-430
  • 2 Tajima T, Honda H, Taguchi K et al.. Sequential hemodynamic change in hepatocellular carcinoma and dysplastic nodules: CT angiography and pathologic correlation.  AJR Am J Roentgenol. 2002;  178 885-897
  • 3 Lencioni R, Cioni D, Crocetti L et al.. Magnetic resonance imaging of liver tumors.  J Hepatol. 2004;  40 162-171
  • 4 Dodd III G D, Miller W J, Baron R L et al.. Detection of malignant tumors in end-stage cirrhotic livers: efficacy of sonography as a screening technique.  AJR Am J Roentgenol. 1992;  159 727-733
  • 5 Shapiro R S, Katz R, Mendelson D S et al.. Detection of hepatocellular carcinoma in cirrhotic patients: sensitivity of CT and ultrasonography.  J Ultrasound Med. 1996;  15 497-502
  • 6 Kim C K, Lim J H, Lee W J. Detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic liver: accuracy of ultrasonography in transplant patients.  J Ultrasound Med. 2001;  20 99-104
  • 7 Rode A, Bancel B, Douek P 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;  25 327-336
  • 8 Bennett G L, Krinsky G A, Abitbol R J et al.. Sonographic detection of hepatocellular carcinoma and dysplastic nodules in cirrhosis: correlation of pretransplantation sonography and liver explant pathology in 200 patients.  AJR Am J Roentgenol. 2002;  179 75-80
  • 9 Liu W C, Lim J H, Park C K et al.. Poor sensitivity of sonography in detection of hepatocellular carcinoma in advanced liver cirrhosis: accuracy of pretransplantation sonography in 118 patients.  Eur Radiol. 2003;  13 1693-1698
  • 10 Teefey S A, Hildeboldt C C, Dehdashti F et al.. Detection of primary hepatic malignancy in liver transplant candidates: prospective comparison of CT, MR imaging, US, and PET.  Radiology. 2003;  226 533-542
  • 11 Caturelli E, Pompili M, Bartolucci F et al.. Hemangioma-like lesions in chronic liver disease: diagnostic evaluation in patients.  Radiology. 2001;  220 337-342
  • 12 Lencioni R, Pinto F, Armillotta N, Bartolozzi C. Assessment of tumor vascularity in hepatocellular carcinoma: comparison of power Doppler US and color Doppler US.  Radiology. 1996;  201 353-358
  • 13 Lencioni R, Cioni D, Bartolozzi C. Tissue harmonic and contrast-specific imaging: back to gray scale in ultrasound.  Eur Radiol. 2002;  12 151-165
  • 14 Fracanzani A L, Burdick L, Borzio M et al.. Contrast-enhanced Doppler ultrasonography in the diagnosis of hepatocellular carcinoma and premalignant lesions in patients with cirrhosis.  Hepatology. 2001;  34 1109-1112
  • 15 Lencioni R, Cioni D, Crocetti L et al.. Ultrasound imaging of focal liver lesions with a second-generation contrast agent.  Acad Radiol. 2002;  9(suppl 2) S371-S374
  • 16 Wen Y L, Kudo M, Zheng R Q et al.. Characterization of hepatic tumors: value of contrast-enhanced coded phase-inversion harmonic angio.  AJR Am J Roentgenol. 2004;  182 1019-1026
  • 17 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
  • 18 Albrecht T, Blomley M, Bolondi L et al.. Guidelines for the use of contrast agents in ultrasound. January 2004.  Ultraschall Med. 2004;  25 249-256
  • 19 Nicolau C, Catala V, Vilana R et al.. Evaluation of hepatocellular carcinoma using SonoVue, a second generation ultrasound contrast agent: correlation with cellular differentiation.  Eur Radiol. 2004;  14 1092-1099
  • 20 Gaiani S, Celli N, Piscaglia F et al.. Usefulness of contrast-enhanced perfusional sonography in the assessment of hepatocellular carcinoma hypervascular at spiral computed tomography.  J Hepatol. 2004;  41 421-426
  • 21 Kim T, Murakami T, Hori M et al.. Small hypervascular hepatocellular carcinoma revealed by double arterial phase CT performed with single breath-hold scanning and automatic bolus tracking.  AJR Am J Roentgenol. 2002;  178 899-904
  • 22 Kawata S, Murakami T, Kim T et al.. Multidetector CT: diagnostic impact of slice thickness on detection of hypervascular hepatocellular carcinoma.  AJR Am J Roentgenol. 2002;  179 61-66
  • 23 Murakami T, Kim T, Takamura M et al.. Hypervascular hepatocellular carcinoma: detection with double arterial phase multi-detector row helical CT.  Radiology. 2001;  218 763-767
  • 24 Ichikawa T, Kitamura T, Nakajima H et al.. Hypervascular hepatocellular carcinoma: can double arterial phase imaging with multidetector CT improve tumor depiction in the cirrhotic liver?.  AJR Am J Roentgenol. 2002;  179 751-758
  • 25 Kim S K, Lim J H, Lee W J et al.. Detection of hepatocellular carcinoma: comparison of dynamic three-phase computed tomography images and four-phase computed tomography images using multidetector row helical computed tomography.  J Comput Assist Tomogr. 2002;  26 691-698
  • 26 Laghi A, Iannaccone R, Rossi P et al.. Hepatocellular carcinoma: detection with triple-phase multi-detector row helical CT in patients with chronic hepatitis.  Radiology. 2003;  226 543-549
  • 27 Francis I R, Cohan R H, McNulty N J et al.. Multidetector CT of the liver and hepatic neoplasms: effect of multiphasic imaging on tumor conspicuity and vascular enhancement.  AJR Am J Roentgenol. 2003;  180 1217-1224
  • 28 Murakami T, Kim T, Kawata S et al.. Evaluation of optimal timing of arterial phase imaging for the detection of hypervascular hepatocellular carcinoma by using triple arterial phase imaging with multidetector-row helical computed tomography.  Invest Radiol. 2003;  38 497-503
  • 29 Lim J H, Kim C K, Lee W J et al.. Detection of hepatocellular carcinomas and dysplastic nodules in cirrhotic livers: accuracy of helical CT in transplant patients.  AJR Am J Roentgenol. 2000;  175 693-698
  • 30 de Lédinghen V, Laharie D, Lecesne R et al.. Detection of nodules in liver cirrhosis: spiral computed tomography or magnetic resonance imaging? A prospective study of 88 nodules in 34 patients.  Eur J Gastroenterol Hepatol. 2002;  14 159-165
  • 31 Burrel M, Llovet J M, Ayuso C et al.. MRI angiography is superior to helical CT for detection of HCC prior to liver transplantation: an explant correlation.  Hepatology. 2003;  38 1034-1042
  • 32 Valls C, Cos M, Figueras J et al.. Pretransplantation diagnosis and staging of hepatocellular carcinoma in patients with cirrhosis: value of dual-phase helical CT.  AJR Am J Roentgenol. 2004;  182 1011-1017
  • 33 Hayashi M, Matsui O, Ueda K et al.. Progression to hypervascular hepatocellular carcinoma: correlation with intranodular blood supply evaluated with CT during intraarterial injection of contrast material.  Radiology. 2002;  225 143-149
  • 34 Baron R L, Brancatelli G. Computed tomographic imaging of hepatocellular carcinoma.  Gastroenterology. 2004;  127(5 suppl 1) S133-S143
  • 35 Freeny P C, Grossholz M, Kaakaji K, Schmiedl U P. Significance of hyperattenuating and contrast-enhancing hepatic nodules detected in the cirrhotic liver during arterial phase helical CT in pre-liver transplant patients: radiologic-histopathologic correlation of explanted livers.  Abdom Imaging. 2003;  28 333-346
  • 36 Brancatelli G, Baron R L, Peterson M S, Marsh W. Helical CT screening for hepatocellular carcinoma in patients with cirrhosis: frequency and causes of false-positive interpretation.  AJR Am J Roentgenol. 2003;  180 1007-1014
  • 37 Kim T, Federle M P, Baron R L et al.. Discrimination of small hepatic hemangiomas from hypervascular malignant tumors smaller than 3 cm with three-phase helical CT.  Radiology. 2001;  219 699-706
  • 38 Colagrande S, Fargnoli R, Dal Pozzo F et al.. Value of hepatic arterial phase CT versus lipiodol ultrafluid CT in the detection of hepatocellular carcinoma.  J Comput Assist Tomogr. 2000;  24 878-883
  • 39 Iannaccone R, Laghi A, Catalano C et al.. Hepatocellular carcinoma: role of unenhanced and delayed phase multi-detector row helical CT in patients with cirrhosis.  Radiology. 2005;  234 460-467
  • 40 Tsai T J, Chau G Y, Lui W Y et al.. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma.  Surgery. 2000;  127 603-608
  • 41 Keogan M T, Edelman R R. Technologic advances in abdominal MR imaging.  Radiology. 2001;  220 310-320
  • 42 Sugihara E, Murakami T, Kim T et al.. Detection of hypervascular hepatocellular carcinoma with dynamic magnetic resonance imaging with simultaneously obtained in-phase and opposed-phase echo images.  J Comput Assist Tomogr. 2003;  27 110-116
  • 43 Bartolozzi C, Cioni D, Donati F, Lencioni R. Focal liver lesions: MR imaging-pathologic correlation.  Eur Radiol. 2001;  11 1374-1388
  • 44 Hussain H K, Syed I, Nghiem H V et al.. T2-weighted MR imaging in the assessment of cirrhotic liver.  Radiology. 2004;  230 637-644
  • 45 Lencioni R, Mascalchi M, Caramella D, Bartolozzi C. Small hepatocellular carcinoma: differentiation from adenomatous hyperplasia with color Doppler US and dynamic Gd-DTPA-enhanced MR imaging.  Abdom Imaging. 1996;  21 41-48
  • 46 Noguchi Y, Murakami T, Kim T et al.. Detection of hypervascular hepatocellular carcinoma by dynamic magnetic resonance imaging with double-echo chemical shift in-phase and opposed-phase gradient echo technique: comparison with dynamic helical computed tomography imaging with double arterial phase.  J Comput Assist Tomogr. 2002;  26 981-987
  • 47 Eubank W B, Wherry K L, Maki J H et al.. Preoperative evaluation of patients awaiting liver transplantation: comparison of multiphasic contrast-enhanced 3D magnetic resonance to helical computed tomography examinations.  J Magn Reson Imaging. 2002;  16 565-575
  • 48 Noguchi Y, Murakami T, Kim T et al.. Detection of hepatocellular carcinoma: comparison of dynamic MR imaging with dynamic double arterial phase helical CT.  AJR Am J Roentgenol. 2003;  180 455-460
  • 49 Taouli B, Losada M, Holland A, Krinsky G. Magnetic resonance imaging of hepatocellular carcinoma.  Gastroenterology. 2004;  127 S144-S152
  • 50 Hussain H K, Londy F J, Francis I R et al.. Hepatic arterial phase MR imaging with automated bolus-detection three-dimensional fast gradient-recalled-echo sequence: comparison with test-bolus method.  Radiology. 2003;  226 558-566
  • 51 Mori K, Yoshioka H, Takahashi N et al.. Triple arterial phase dynamic MRI with sensitivity encoding for hypervascular hepatocellular carcinoma: comparison of the diagnostic accuracy among the early, middle, late, and whole triple arterial phase imaging.  AJR Am J Roentgenol. 2005;  184 63-69
  • 52 Shimizu A, Ito K, Koike S et al.. Cirrhosis or chronic hepatitis: evaluation of small ( < or = 2-cm) early-enhancing hepatic lesions with serial contrast enhanced dynamic MR imaging.  Radiology. 2003;  226 550-555
  • 53 Ito K, Fujita T, Shimizu A et al.. Multiarterial phase dynamic MRI of small early enhancing hepatic lesions in cirrhosis or chronic hepatitis: differentiating between hypervascular hepatocellular carcinomas and pseudolesions.  AJR Am J Roentgenol. 2004;  183 699-705
  • 54 Krinsky G A, Lee V S, Theise N D et al.. Transplantation for hepatocellular carcinoma and cirrhosis: sensitivity of magnetic resonance imaging.  Liver Transpl. 2002;  8 1156-1164
  • 55 Bhartia B, Ward J, Guthrie J A, Robinson P J. Hepatocellular carcinoma in cirrhotic livers: double-contrast thin-section MR imaging with pathologic correlation of explanted tissue.  AJR Am J Roentgenol. 2003;  180 577-584
  • 56 Bartolozzi C, Donati F, Cioni D et al.. MnDPDP-enhanced MRI vs dual-phase spiral CT in the detection of hepatocellular carcinoma in cirrhosis.  Eur Radiol. 2000;  10 1697-1702
  • 57 Lim J H, Choi D, Cho S K et al.. Conspicuity of hepatocellular nodular lesions in cirrhotic livers at ferumoxides-enhanced MR imaging: importance of Kupffer cell number.  Radiology. 2001;  220 669-676
  • 58 Kang B K, Lim J H, Kim S H et al.. Preoperative depiction of hepatocellular carcinoma: ferumoxides-enhanced MR imaging versus triple-phase helical CT.  Radiology. 2003;  226 79-85
  • 59 Pauleit D, Textor J, Bachmann R et al.. Hepatocellular carcinoma: detection with gadolinium- and ferumoxides-enhanced MR imaging of the liver.  Radiology. 2002;  222 73-80
  • 60 Youk J H, Lee J M, Kim C S. MRI for detection of hepatocellular carcinoma: comparison of mangafodipir trisodium and gadopentetate dimeglumine contrast agents.  AJR Am J Roentgenol. 2004;  183 1049-1054
  • 61 Kwak H S, Lee J M, Kim Y K et al.. Detection of hepatocellular carcinoma: comparison of ferumoxides-enhanced and gadolinium-enhanced dynamic three-dimensional volume interpolated breath-hold MR imaging.  Eur Radiol. 2005;  15 140-147

 Prof.
Riccardo Lencioni

Division of Diagnostic and Interventional Radiology

Pisa University Hospital, Via Roma 67

I-56125 Pisa, Italy

Email: Lencioni@do.med.unipi.it

    >