Download PDF
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)

    Permissions and Reprints

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.

KEYWORDS

Ultrasonography - computed tomography - magnetic resonance imaging - percutaneous biopsy

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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 3 Lencioni R, Cioni D, Crocetti L et al.. Magnetic resonance imaging of liver tumors.  J Hepatol. 2004;  40 162-171
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    Thieme ConnectPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 34 Baron R L, Brancatelli G. Computed tomographic imaging of hepatocellular carcinoma.  Gastroenterology. 2004;  127(5 suppl 1) S133-S143
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 41 Keogan M T, Edelman R R. Technologic advances in abdominal MR imaging.  Radiology. 2001;  220 310-320
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 43 Bartolozzi C, Cioni D, Donati F, Lencioni R. Focal liver lesions: MR imaging-pathologic correlation.  Eur Radiol. 2001;  11 1374-1388
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    Search in Google Scholar
  • 49 Taouli B, Losada M, Holland A, Krinsky G. Magnetic resonance imaging of hepatocellular carcinoma.  Gastroenterology. 2004;  127 S144-S152
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    PubMedSearch in Google Scholar
  • 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
    CrossrefPubMedSearch in Google Scholar

 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