Abdominal Imaging

, Volume 37, Issue 2, pp 215–230 | Cite as

Imaging of HCC

  • Carmen Ayuso
  • Jordi Rimola
  • Ángeles García-Criado


Imaging techniques play a crucial role in the management of patients with liver cirrhosis in whom a nodular hepatic lesion is detected. The most severe complication of patients with liver cirrhosis is the development of a hepatocellular carcinoma (HCC), and the prognosis of the disease depends on the tumoral stage. Surveillance programs based on ultrasonography (US) are recommended in cirrhotic patients with possibility to be treated if an HCC is detected, in order to improve the patient’s survival. Nevertheless, early detection and diagnostic confirmation of HCC remains a challenge despite technological advances. The non-invasive criteria to characterize small HCCs in patients with cirrhosis are based on the evaluation of the vascular profile of the lesion. Dynamic multidetector computed tomography (MDCT) and dynamic magnetic resonance imaging (MRI) are the suitable techniques for this purpose. When diagnosis is not achieved, fine US-guided fine needle biopsy (FNB) is indicated. Cellular-MRI contrast agents may have a role in lesions with atypical vascular pattern in which FNB is not feasible. The assessment of the disease extent is another important goal for imaging techniques. Again, dynamic MDCT and dynamic MRI may be used for staging purposes. Although MRI is more accurate in the detection of additional nodules ranging 1–2 cm, both remain relatively insensitive for the detection of tiny satellite nodules below 1 cm. The therapeutic decision can be made in any particular patient on the basis of the tumoral extension, the liver function, and the general status. After curative and palliative therapeutic procedures, the monitoring of the response is mandatory to decide the next approach: to follow-up, to repeat the treatment, to modify the treatment indication, or to suspend the treatment. In this review, we discuss the most recent information on the imaging of HCC.


Hepatocellular carcinoma Diagnosis Ultrasonography Computed tomography Magnetic resonance imaging Percutaneous biopsy 


  1. 1.
    Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108PubMedCrossRefGoogle Scholar
  2. 2.
    Sangiovanni A, Prati GM, Fasani P, et al. (2006) The natural history of compensated cirrhosis due to hepatitis C virus: a 17-year cohort study of 214 patients. Hepatology 43:1303–1310PubMedCrossRefGoogle Scholar
  3. 3.
    Llovet JM, Bruix J (2008) Novel advancements in the management of hepatocellular carcinoma in 2008. J Hepatol 48:S20–S37PubMedCrossRefGoogle Scholar
  4. 4.
    Llovet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362:1907–1917PubMedCrossRefGoogle Scholar
  5. 5.
    Llovet JM, Fuster J, Bruix J (1999) Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30:1434–1440PubMedCrossRefGoogle Scholar
  6. 6.
    Bruix J, Sherman M (2010) Management of hepatocellular carcinoma: an update. American Association for the Study of Liver Diseases. http://www.aasld.org/practiceguidelines. Retrieved 4 October 2010.
  7. 7.
    Sherman M (2001) Alphafetoprotein: an obituary. J Hepatol 34:603–605PubMedCrossRefGoogle Scholar
  8. 8.
    Bolondi L (2003) Screening for hepatocellular carcinoma in cirrhosis. J Hepatol 39:1076–1084PubMedCrossRefGoogle Scholar
  9. 9.
    Brenner DJ, Hall EJ (2007) Computed tomography—an increasing source of radiation exposure. N Engl J Med 357:2277–2284PubMedCrossRefGoogle Scholar
  10. 10.
    Burrel M, Llovet JM, Ayuso C, et al. (2003) MRI angiography is superior to helical CT for detection of HCC prior to liver transplantation: an explant correlation. Hepatology 38:1034–1042PubMedGoogle Scholar
  11. 11.
    Lencioni R, Cioni D, Pina C, Crocetti L, Bartolozzi C (2005) Hepatocellular carcinoma. Imaging diagnosis. Semin Liver Dis 25:162–170PubMedCrossRefGoogle Scholar
  12. 12.
    Teefey SA, Hildeboldt CC, Dehdashti F, et al. (2003) Detection of primary hepatic malignancy in liver transplant candidates: prospective comparison of CT, MR imaging, US and PET. Radiology 226:533–542PubMedCrossRefGoogle Scholar
  13. 13.
    Trevisani F, De NS, Rapaccini G, et al. (2002) Semiannual and annual surveillance of cirrhotic patients for hepatocellular carcinoma: effects on cancer stage and patient survival (Italian experience). Am J Gastroenterol 97:734–744PubMedCrossRefGoogle Scholar
  14. 14.
    Kojiro M, Roskams T (2005) Early hepatocellular carcinoma and dysplastic nodules. Semin Liver Dis 25:133–142PubMedCrossRefGoogle Scholar
  15. 15.
    Lee MW, Kim YJ, Park HS, et al. (2010) Targeted sonography for small hepatocellular carcinoma discovered by CT or MRI: factors affecting sonographic detection. AJR Am J Roentgenol 194:W396–W400PubMedCrossRefGoogle Scholar
  16. 16.
    Terminology of nodular hepatocellular lesions. International Working Party. Hepatology 22:983–993 (1995)Google Scholar
  17. 17.
    Kojiro M, Wanless IR, Alves V, et al. (2009) Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology 658–664Google Scholar
  18. 18.
    Hayashi M, Matsui O, Ueda K, et al. (1999) Correlation between the blood supply and grade of malignancy of hepatocellular nodules associated with liver cirrhosis: evaluation by CT during intraarterial injection of contrast medium. AJR Am J Roentgenol 172:969–976PubMedGoogle Scholar
  19. 19.
    Efremidis SC, Hytiroglou P (2002) The multistep process of hepatocarcinogenesis in cirrhosis with imaging correlation. Eur Radiol 12:753–764PubMedCrossRefGoogle Scholar
  20. 20.
    Kudo M (2009) Multistep human hepatocarcinogenesis: correlation of imaging with pathology. J Gastroenterol 44:112–118PubMedCrossRefGoogle Scholar
  21. 21.
    Roncalli M, Roz E, Coggi G, et al. (1999) The vascular profile of regenerative and dysplastic nodules of the cirrhotic liver: implications for diagnosis and classification. Hepatology 30:1174–1178PubMedCrossRefGoogle Scholar
  22. 22.
    Kitao A, Zen Y, Matsui O, Gabata T, Nakamura Y (2009) Hepatocarcinogenesis: multistep changes of drainage vessels at CT during arterial portography and hepatic arteriography-radiologic-pathologic correlation. Radiology 252:605–614PubMedCrossRefGoogle Scholar
  23. 23.
    Huppertz A, Haraida S, Kraus A, et al. (2005) Enhancement of focal liver lesions at gadoxetic acid-enhanced MR imaging: correlation with histopathologic findings and spiral CT—initial observations. Radiology 234:468–478PubMedCrossRefGoogle Scholar
  24. 24.
    Frericks B, Loddenkemper CH, Huppertz A, et al. (2009) Qualitative and quantitative evaluation of hepatocellular carcinoma and cirrhotic liver enhancement using Gd-EOB-DTPA. AJR Am J Roentgenol 193:1053–1060PubMedCrossRefGoogle Scholar
  25. 25.
    Kogita S, Imai Y, Okada M, et al. (2010) Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol 20(10):2405–2413PubMedCrossRefGoogle Scholar
  26. 26.
    Bruix J, Sherman M, Llovet JM, et al. (2001) Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 35:421–430PubMedCrossRefGoogle Scholar
  27. 27.
    Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236PubMedCrossRefGoogle Scholar
  28. 28.
    Forner A, Vilana R, Ayuso C, et al. (2008) Diagnosis of hepatic nodules ≤20 mm in cirrhosis. Prospective validation of the non-invasive diagnostic criteria for hepatocellular carcinoma (HCC). Hepatology 47:97–104PubMedCrossRefGoogle Scholar
  29. 29.
    Sangiovanni A, Manini MA, Iavarone M, et al. (2010) The diagnostic and economic impact of contrast imaging technique in the diagnosis of small hepatocellular carcinoma in cirrhosis. Gut 59:570–571CrossRefGoogle Scholar
  30. 30.
    Bhayana D, Kim TK, Jang HJ, Burns PN, Wilson SR (2010) Hypervascular liver masses on contrast-enhanced ultrasound: the importance of washout. AJR Am J Roentgenol 194:977–983PubMedCrossRefGoogle Scholar
  31. 31.
    Chen LD, Xu HX, Xie XY, et al. (2010) Intrahepatic cholangiocarcinoma and hepatocellular carcinoma: differential diagnosis with contrast-enhanced ultrasound. Eur Radiol 20:743–753PubMedCrossRefGoogle Scholar
  32. 32.
    Vilana R, Forner A, Bianchi L, et al. (2010) Intrahepatic peripheral cholangiocarcinoma in cirrhotic patients may display a vascular pattern similar to hepatocellular carcinoma on contrast enhanced ultrasound. Hepatology 51:2020–2029PubMedCrossRefGoogle Scholar
  33. 33.
    Rimola J, Forner A, Reig M, et al. (2009) Cholangiocarcinoma in cirrhosis: absence of contrast washout in delayed phases by MR avoids misdiagnosis of hepatocellular carcinoma. Hepatology 50:791–798PubMedCrossRefGoogle Scholar
  34. 34.
    Bolondi L, Gaiani S, Celli N, et al. (2005) Characterization of small nodules in cirrhosis by assessment of vascularity: the problem of hypovascular hepatocellular carcinoma. Hepatology 42:27–34PubMedCrossRefGoogle Scholar
  35. 35.
    Ishigami K, Yoshimitsu K, Nishihara Y, et al. (2009) Hepatocellular carcinoma with a pseudocapsule on gadolinium enhanced MR images: correlation with histopathologic findings. Radiology 50:435–443CrossRefGoogle Scholar
  36. 36.
    Martín J, Sentís M, Zidan A, et al. (1995) Fatty metamorphosis of hepatocellular carcinoma: detection with chemical shift gradient-echo MR imaging. Radiology 195(1):125–130PubMedGoogle Scholar
  37. 37.
    Vandecaveye V, De Keyzer F, Verslype Ch, et al. (2009) Diffusion-weighted MRI provides additional value to conventional dynamic contrast-enhanced MRI for detection of hepatocellular carcinoma. Eur Radiol 19:2456–2466PubMedCrossRefGoogle Scholar
  38. 38.
    Kim YK, Kwak HS, Kim CS, et al. (2006) Hepatocellular carcinoma in patients with chronic liver disease: comparison of SPIO-enhanced MR imaging and 16-detector row CT. Radiology 238:531–541PubMedCrossRefGoogle Scholar
  39. 39.
    Kim YK, Kim CS, Chung GH, et al. (2006) Comparison of gadobenate dimeglumine-enhanced dynamic MRI and 16-MDCT for the detection of hepatocellular carcinoma. AJR Am J Roentgenol 186:149–157PubMedCrossRefGoogle Scholar
  40. 40.
    Kim SH, Kim SH, Lee J, et al. (2009) Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. AJR Am J Roentgenol 192:1675–1681PubMedCrossRefGoogle Scholar
  41. 41.
    Filippone A, Blakeborough A, Breuer J, et al. (2010) Enhancement of liver parenchyma after injection of hepatocyte-specific MRI contrast media: a comparison of gadoxetic acid and gadobenate dimeglumine. J Magn Reson Imaging 31:356–364PubMedCrossRefGoogle Scholar
  42. 42.
    Tsuboyama T, Onishi H, Kim T, et al. (2010) Hepatocellular carcinoma: hepatocyte-selective enhancement at gadoxetic acid-enhanced MR imaging—correlation with expression of sinusoidal and canalicular transporters and bile accumulation. Radiology 255(3):824–833PubMedCrossRefGoogle Scholar
  43. 43.
    Lee JY, Kim SH, Jeon YH, et al. (2010) Ferucarbotran-enhanced magnetic resonance imaging versus gadoxetic acid-enhanced magnetic resonance imaging for the preoperative detection of hepatocellular carcinoma: initial experience. J Comput Assist Tomogr 34(1):127–134PubMedCrossRefGoogle Scholar
  44. 44.
    Ahn SS, Kim MJ, Lim JS, et al. (2010) Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 255:459–466PubMedCrossRefGoogle Scholar
  45. 45.
    Motosugi U, Ichikawa T, Sou H, et al. (2010) Distinguishing hypervascular pseudolesions of the liver from hypervascular hepatocellular carcinomas with gadoxeticacid-enhanced MR imaging. Radiology 256(1):151–158PubMedCrossRefGoogle Scholar
  46. 46.
    Sun HY, Lee JM, Shin CH, Lee DH (2010) Gadoxetic acid-enhanced magnetic resonance imaging for differentiating small hepatocellular carcinomas (≤2 cm in diameter) from arterial enhancing pseudolesions. Special emphasis on hepatobiliary phase imaging. Invest Radiol 45:96–103PubMedCrossRefGoogle Scholar
  47. 47.
    Bruix J, Llovet JM (2009) Major achievements in hepatocellular carcinoma. Lancet 373:614–616PubMedCrossRefGoogle Scholar
  48. 48.
    Llovet JM, Schwartz M, Mazzaferro V (2005) Resection and liver transplantation for hepatocellular carcinoma. Semin Liver Dis 25(2):181–200PubMedCrossRefGoogle Scholar
  49. 49.
    World Health Organization (1979) WHO handbook for reporting results of cancer treatment. Geneva (Albany, N.Y.: World Health Organization; sold by WHO Publications Centre USA)Google Scholar
  50. 50.
    Therasse P, Arbuck SG, Eisenhauer EA, et al. (2000) New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 92(3):205–216PubMedCrossRefGoogle Scholar
  51. 51.
    Forner A, Ayuso C, Varela M, et al. (2009) Evaluation of tumor response after locoregional therapies in hepatocellular carcinoma: are response evaluation criteria in solid tumors reliable? Cancer 115(3):616–623PubMedCrossRefGoogle Scholar
  52. 52.
    Goldberg SN, Grassi CJ, Cardella JF, et al. (2005) Image-guided tumor ablation: standardization of terminology and reporting criteria. Radiology 235(3):728–739PubMedCrossRefGoogle Scholar
  53. 53.
    Lencioni R, Llovet JM (2010) Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis 30(1):52–60PubMedCrossRefGoogle Scholar
  54. 54.
    Cho YK, Kim JK, Kim WT, Chung JW (2010) Hepatic resection versus radiofrequency ablation for very early stage hepatocellular carcinoma: a Markov model analysis. Hepatology 51(4):1284–1290PubMedCrossRefGoogle Scholar
  55. 55.
    Orlando A, Leandro G, Olivo M, Andriulli A, Cottone M (2009) Radiofrequency thermal ablation vs. percutaneous ethanol injection for small hepatocellular carcinoma in cirrhosis: meta-analysis of randomized controlled trials. Am J Gastroenterol 104(2):514–524PubMedCrossRefGoogle Scholar
  56. 56.
    Dodd GD 3rd, Soulen MC, Kane RA, et al. (2000) Minimally invasive treatment of malignant hepatic tumors: at the threshold of a major breakthrough. Radiographics 20(1):9–27PubMedGoogle Scholar
  57. 57.
    Lu DS, Yu NC, Raman SS, et al. (2005) Radiofrequency ablation of hepatocellular carcinoma: treatment success as defined by histologic examination of the explanted liver. Radiology 234(3):954–960PubMedCrossRefGoogle Scholar
  58. 58.
    Vilana R, Bianchi L, Varela M, et al. (2006) Is microbubble-enhanced ultrasonography sufficient for assessment of response to percutaneous treatment in patients with early hepatocellular carcinoma? EurRadiol 16(11):2454–2462Google Scholar
  59. 59.
    Kim SK, Lim HK, Kim YH, et al. (2003) Hepatocellular carcinoma treated with radio-frequency ablation: spectrum of imaging findings. Radiographics 23(1):107–121PubMedCrossRefGoogle Scholar
  60. 60.
    Sala M, Llovet JM, Vilana R, et al. (2004) Initial response to percutaneous ablation predicts survival in patients with hepatocellular carcinoma. Hepatology 40(6):1352–1360PubMedCrossRefGoogle Scholar
  61. 61.
    Hong K, Kobeiter H, Georgiades CS, Torbenson MS, Geschwind JF (2005) Effects of the type of embolization particles on carboplatin concentration in liver tumors after transcatheter arterial chemoembolization in a rabbit model of liver cancer. J Vasc Interv Radiol 16(12):1711–1717PubMedCrossRefGoogle Scholar
  62. 62.
    Takayasu K, Arii S, Matsuo N, et al. (2000) Comparison of CT findings with resected specimens after chemoembolization with iodized oil for hepatocellular carcinoma. AJR Am J Roentgenol 175(3):699–704PubMedGoogle Scholar
  63. 63.
    Kloeckner R, Otto G, Biesterfeld S, et al. (2010) MDCT versus MRI assessment of tumor response after transarterialchemoembolization for the treatment of hepatocellular carcinoma. Cardiovasc Intervent Radiol 33(3):532–540PubMedCrossRefGoogle Scholar
  64. 64.
    Riaz A, Kulik L, Lewandowski RJ, et al. (2009) Radiologic-pathologic correlation of hepatocellular carcinoma treated with internal radiation using yttrium-90 microspheres. Hepatology 49(4):1185–1193PubMedCrossRefGoogle Scholar
  65. 65.
    Salem R, Thurston KG (2006) Radioembolization with 90yttrium microspheres: a state-of-the-art brachytherapy treatment for primary and secondary liver malignancies. Part 2: special topics. J Vasc Interv Radiol 17(9):1425–1439PubMedCrossRefGoogle Scholar
  66. 66.
    Llovet JM, Ricci S, Mazzaferro V, et al. (2008) Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359(4):378–390PubMedCrossRefGoogle Scholar
  67. 67.
    Cheng AL, Kang YK, Chen Z, et al. (2009) Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 10(1):25–34PubMedCrossRefGoogle Scholar
  68. 68.
    Sahani DV, Holalkere NS, Mueller PR, Zhu AX (2007) Advanced hepatocellular carcinoma: CT perfusion of liver and tumor tissue–initial experience. Radiology 243(3):736–743PubMedCrossRefGoogle Scholar
  69. 69.
    Schraml C, Schwenzer NF, Martirosian P, et al. (2009) Diffusion-weighted MRI of advanced hepatocellular carcinoma during sorafenib treatment: initial results. AJR Am J Roentgenol 193(4):W301–W307PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Carmen Ayuso
    • 1
  • Jordi Rimola
    • 2
  • Ángeles García-Criado
    • 2
  1. 1.Barcelona Clinic Liver Cancer (BCLC) Group, Radiology Department, Hospital ClínicUniversity of Barcelona, Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS)BarcelonaSpain
  2. 2.Barcelona Clinic Liver Cancer (BCLC) Group, Radiology Department, Hospital ClínicUniversity of BarcelonaBarcelonaSpain

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