Abdominal Radiology

, Volume 44, Issue 7, pp 2366–2376 | Cite as

Diagnosis of recurrent HCC: intraindividual comparison of gadoxetic acid MRI and extracellular contrast-enhanced MRI

  • Jae Hyun Yim
  • Young Kon KimEmail author
  • Ji Hye Min
  • Jisun Lee
  • Tae Wook Kang
  • Soon Jin Lee



To compare the efficacy of magnetic resonance imaging (MRI) with hepatobiliary agents (HBA-MRI) and MRI with extracellular contrast agents (ECA-MRI) for detection of recurrent hepatocellular carcinoma (HCC) after multiple treatments.


The institutional review board approved this retrospective study and waived the requirement for informed patient consent. A total of 135 patients with suspected HCC recurrence after 2–5 treatments (surgery, transarterial chemoembolization, and/or radiofrequency ablation) underwent both HBA-MRI and ECA-MRI within a 1 month interval. HBA-MRI and ECA-MRI were analyzed for HCC detection by two observers using a five-point scale. The diagnostic performances according to MRI modality were compared.


A total of 136 liver lesions (121 HCCs and 15 benign lesions; median size, 1.9 cm) were identified. ECA-MRI showed greater sensitivity (90.9% vs. 76.9% for observer 1; 91.7% vs. 78.5% for observer 2) and accuracy (91.2% vs. 78.7% for observer 1; 91.9% vs. 80.2% for observer 2) than HBA-MRI for both observers (P = 0.002, 0.003). Fifteen (12.4%) HCCs were correctly diagnosed with ECA-MRI but not with HBA-MRI by both observers. Interobserver agreement was excellent (0.885) for ECA-MRI and substantial (0.749) for HBA-MRI.


For detection of recurrent HCC, ECA-MRI was superior to HBA-MRI in terms of sensitivity and accuracy. Therefore, ECA-MRI could be the preferred imaging modality over HBA-MRI for assessing HCC recurrence following multiple treatments.


Liver Hepatocellular carcinoma Magnetic resonance imaging Contrast agents Recurrence 



Magnetic resonance imaging


Hepatobiliary agents


Extracellular contrast agents


Hepatocellular carcinoma


Computed tomography


Gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid


Liver Reporting and Data System


Hepatobiliary phase


Transitional phase


Portal venous phase


T2-weighted image


Diffusion-weighted image


Receiver operating characteristics


Under the ROC curve


Positive predictive value


Negative predictive value


Radiofrequency ablation


Transarterial chemoembolization


Supplementary material

261_2019_1968_MOESM1_ESM.docx (28 kb)
Supplementary material 1 (DOCX 28 kb)


  1. 1.
    Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020-1022. CrossRefGoogle Scholar
  2. 2.
    (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56:908-943.
  3. 3.
    Forner A, Vilana R, Ayuso C, Bianchi L, Sole M, Ayuso JR, Boix L, Sala M, Varela M, Llovet JM, Bru C, Bruix J (2008) Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 47:97-104. CrossRefGoogle Scholar
  4. 4.
    Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, Zhu AX, Murad MH, Marrero JA (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358-380. CrossRefGoogle Scholar
  5. 5.
    (2018) EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol 69:182-236.
  6. 6.
    Kim YK, Kim CS, Han YM, Yu HC, Choi D (2011) Detection of small hepatocellular carcinoma: intraindividual comparison of gadoxetic acid-enhanced MRI at 3.0 and 1.5 T. Invest Radiol 46:383-389. CrossRefGoogle Scholar
  7. 7.
    Sun HY, Lee JM, Shin CI, Lee DH, Moon SK, Kim KW, Han JK, Choi BI (2010) Gadoxetic acid-enhanced magnetic resonance imaging for differentiating small hepatocellular carcinomas (< or =2 cm in diameter) from arterial enhancing pseudolesions: special emphasis on hepatobiliary phase imaging. Invest Radiol 45:96-103. CrossRefGoogle Scholar
  8. 8.
    Elsayes KM, Hooker JC, Agrons MM, Kielar AZ, Tang A, Fowler KJ, Chernyak V, Bashir MR, Kono Y, Do RK, Mitchell DG, Kamaya A, Hecht EM, Sirlin CB (2017) 2017 Version of LI-RADS for CT and MR Imaging: An Update. Radiographics 37:1994-2017. CrossRefGoogle Scholar
  9. 9.
    Omata M, Cheng AL, Kokudo N, Kudo M, Lee JM, Jia J, Tateishi R, Han KH, Chawla YK, Shiina S, Jafri W, Payawal DA, Ohki T, Ogasawara S, Chen PJ, Lesmana CRA, Lesmana LA, Gani RA, Obi S, Dokmeci AK, Sarin SK (2017) Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatol Int 11:317-370. CrossRefGoogle Scholar
  10. 10.
    Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology 273:30-50. CrossRefGoogle Scholar
  11. 11.
    Vogl TJ, Kummel S, Hammerstingl R, Schellenbeck M, Schumacher G, Balzer T, Schwarz W, Muller PK, Bechstein WO, Mack MG, Sollner O, Felix R (1996) Liver tumors: comparison of MR imaging with Gd-EOB-DTPA and Gd-DTPA. Radiology 200:59-67. CrossRefGoogle Scholar
  12. 12.
    Ahn SS, Kim MJ, Lim JS, Hong HS, Chung YE, Choi JY (2010) Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 255:459-466. CrossRefGoogle Scholar
  13. 13.
    Motosugi U, Ichikawa T, Sou H, Sano K, Tominaga L, Muhi A, Araki T (2010) Distinguishing hypervascular pseudolesions of the liver from hypervascular hepatocellular carcinomas with gadoxetic acid-enhanced MR imaging. Radiology 256:151-158. CrossRefGoogle Scholar
  14. 14.
    Park HJ, Kim YK, Park MJ, Lee WJ (2013) Small intrahepatic mass-forming cholangiocarcinoma: target sign on diffusion-weighted imaging for differentiation from hepatocellular carcinoma. Abdom Imaging 38:793-801. CrossRefGoogle Scholar
  15. 15.
    Yang K, Cheng YS, Yang JJ, Jiang X, Guo JX (2017) Primary hepatic neuroendocrine tumors: multi-modal imaging features with pathological correlations. Cancer Imaging 17:20. CrossRefGoogle Scholar
  16. 16.
    Yu JI, Kim JS, Park HC, Lim DH, Han YY, Lim HC, Paik SW (2013) Evaluation of anatomical landmark position differences between respiration-gated MRI and four-dimensional CT for radiation therapy in patients with hepatocellular carcinoma. Br J Radiol 86:20120221. CrossRefGoogle Scholar
  17. 17.
    Serste T, Barrau V, Ozenne V, Vullierme MP, Bedossa P, Farges O, Valla DC, Vilgrain V, Paradis V, Degos F (2012) Accuracy and disagreement of computed tomography and magnetic resonance imaging for the diagnosis of small hepatocellular carcinoma and dysplastic nodules: role of biopsy. Hepatology 55:800-806. CrossRefGoogle Scholar
  18. 18.
    Ronot M, Fouque O, Esvan M, Lebigot J, Aube C, Vilgrain V (2018) Comparison of the accuracy of AASLD and LI-RADS criteria for the non-invasive diagnosis of HCC smaller than 3cm. J Hepatol 68:715-723. CrossRefGoogle Scholar
  19. 19.
    Bennett BM (1972) On comparisons of sensitivity, specificity and predictive value of a number of diagnostic procedures. Biometrics 28:793-800CrossRefGoogle Scholar
  20. 20.
    Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159-174CrossRefGoogle Scholar
  21. 21.
    Lee YJ, Lee JM, Lee JS, Lee HY, Park BH, Kim YH, Han JK, Choi BI (2015) Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology 275:97-109. CrossRefGoogle Scholar
  22. 22.
    Obuchowski NA, McClish DK (1997) Sample size determination for diagnostic accuracy studies involving binormal ROC curve indices. Stat Med 16:1529-1542CrossRefGoogle Scholar
  23. 23.
    Lee S, Kim KM, Lee SJ, Lee KH, Lee DY, Kim MD, Kim DY, Kim SU, Won JY (2017) Hepatic arterial damage after transarterial chemoembolization for the treatment of hepatocellular carcinoma: comparison of drug-eluting bead and conventional chemoembolization in a retrospective controlled study. Acta Radiol 58:131-139. CrossRefGoogle Scholar
  24. 24.
    Suh CH, Shin JH, Yoon HM, Yoon HK, Ko GY, Gwon DI, Kim JH, Sung KB (2014) Angiographic evaluation of hepatic arterial injury after cisplatin and Gelfoam-based transcatheter arterial chemoembolization for hepatocellular carcinoma in a 205 patient cohort during a 6-year follow-up. Br J Radiol 87:20140054. CrossRefGoogle Scholar
  25. 25.
    Kudo M (2009) Multistep human hepatocarcinogenesis: correlation of imaging with pathology. J Gastroenterol 44 Suppl 19:112-118. CrossRefGoogle Scholar
  26. 26.
    Yu MH, Kim JH, Yoon JH, Kim HC, Chung JW, Han JK, Choi BI (2014) Small (</=1-cm) hepatocellular carcinoma: diagnostic performance and imaging features at gadoxetic acid-enhanced MR imaging. Radiology 271:748-760. CrossRefGoogle Scholar
  27. 27.
    Tamada T, Ito K, Sone T, Yamamoto A, Yoshida K, Kakuba K, Tanimoto D, Higashi H, Yamashita T (2009) Dynamic contrast-enhanced magnetic resonance imaging of abdominal solid organ and major vessel: comparison of enhancement effect between Gd-EOB-DTPA and Gd-DTPA. J Magn Reson Imaging 29:636-640. CrossRefGoogle Scholar
  28. 28.
    Kim HS, Kim M-J, Chung J-J, Lim JS, Chung YE, Park M-S, Kim KW (2011) Focal Liver Lesion Detection in Gadoxetic Acid-enhanced Liver MRI: Effects of Scan Delay, Hepatic Function, and Magnetic Field Strength. J Korean Soc Magn Reson Med 15:226-233CrossRefGoogle Scholar
  29. 29.
    Khan AS, Hussain HK, Johnson TD, Weadock WJ, Pelletier SJ, Marrero JA (2010) 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 32:360-366. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Radiology and Center for Imaging Science, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulRepublic of Korea
  2. 2.Department of RadiologyChungnam National University Hospital, Chungnam National University College of MedicineDaejeonRepublic of Korea
  3. 3.Department of RadiologyChungbuk National University HospitalCheongjuRepublic of Korea

Personalised recommendations