Abdominal Radiology

, Volume 44, Issue 9, pp 3078–3088 | Cite as

Optimal lexicon of gadoxetic acid-enhanced magnetic resonance imaging for the diagnosis of hepatocellular carcinoma modified from LI-RADS

  • Shin Hye Hwang
  • Sumi Park
  • Kyunghwa Han
  • Jin-young Choi
  • Young-Nyun Park
  • Mi-Suk ParkEmail author



To define the optimal lexicon of major imaging findings on gadoxetic acid-enhanced MRIs to diagnose HCC to improve diagnostic performance of the LI-RADS.


Two hundred forty-one hepatic lesions (149 HCC, six other malignancies, 86 benign lesions) in 177 treatment-naïve patients at risk of HCC who underwent gadoxetic acid-MRIs from January 2013 to December 2015 were retrospectively reviewed using either histopathological or follow-up imaging findings as a standard reference. Two board-certified radiologists independently evaluated the imaging features and categorized the nodules based on the original and the following modified definitions in LI-RADS: (1) washout appearance in the portal venous phase (PVP) only versus that in the PVP or transitional phase, and (2) enhancing capsule only versus enhancing or non-enhancing capsule. Diagnostic performance and inter-observer agreement of LR-5 were assessed and compared between the algorithms using generalized estimation equation.


The sensitivity [79.2% (95% confidence interval 71.9, 85.0)] and accuracy [84.6% (79.5, 88.7)] of LR-5 were significantly higher for modified lexicon compared with original LI-RADS [60.4% (52.3, 67.9) and 73.9% (67.9, 79.0); P < 0.001 in all cases]. There was no significant difference in specificity [93.5% (86.2, 97.0) and 95.7% (89.0, 98.4); P = 0.153]. Subgroups of lesions < or ≥ 2 cm showed similar tendencies. Inter-observer agreement for capsule appearance was fair to moderate, whereas that for other imaging findings was good to excellent.


Compared to original LI-RADS, LI-RADS with modified lexicon showed higher sensitivity for the diagnosis of HCC using gadoxetic acid-MRI, with similar specificity.


Hepatocellular carcinoma Diagnosis MRI (Magnetic resonance imaging) Gadoxetic acid 



All authors declare that they have nothing to disclose about funding with respect to this manuscript.

Compliance with ethical standards

Conflict of interest

The authors of this study declared that they have nothing to disclose regarding conflict of interest with respect to this manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Supplementary material

261_2019_2077_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 17 kb)


  1. 1.
    (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56(4):908-943.Google Scholar
  2. 2.
    Kudo M, Matsui O, Izumi N, Iijima H, Kadoya M, Imai Y (2014) Surveillance and diagnostic algorithm for hepatocellular carcinoma proposed by the Liver Cancer Study Group of Japan: 2014 update. Oncology 87 Suppl 1:7-21.Google Scholar
  3. 3.
    Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53(3):1020-1022.Google Scholar
  4. 4.
    Korean Liver Cancer Study Group, National Cancer Center, Korea (2015) 2014 Korean Liver Cancer Study Group-National Cancer Center Korea practice guideline for the management of hepatocellular carcinoma. Korean J Radiol 16(3):465-522.Google Scholar
  5. 5.
    Mitchell DG, Bruix J, Sherman M, Sirlin CB (2015) LI-RADS (Liver Imaging Reporting and Data System): summary, discussion, and consensus of the LI-RADS Management Working Group and future directions. Hepatology 61(3):1056-1065.Google Scholar
  6. 6.
    Lee VS (2017) Annual Oration: Driving Value through Imaging. Radiology 285(1):3-11.Google Scholar
  7. 7.
    Hope TA, Fowler KJ, Sirlin CB, Costa EA, Yee J, Yeh BM, Heiken JP (2015) Hepatobiliary agents and their role in LI-RADS. Abdom Imaging 40(3):613-625.Google Scholar
  8. 8.
    Song JS, Choi EJ, Hwang SB, Hwang HP, Choi H (2018) LI-RADS v2014 categorization of hepatocellular carcinoma: Intraindividual comparison between gadopentetate dimeglumine-enhanced MRI and gadoxetic acid-enhanced MRI. Eur Radiol
  9. 9.
    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(1):97-109.Google Scholar
  10. 10.
    Kierans AS, Kang SK, Rosenkrantz AB (2016) The Diagnostic Performance of Dynamic Contrast-enhanced MR Imaging for Detection of Small Hepatocellular Carcinoma Measuring Up to 2 cm: A Meta-Analysis. Radiology 278(1):82-94.Google Scholar
  11. 11.
    An C, Rhee H, Han K, Choi JY, Park YN, Park MS, Kim MJ, Park S (2017) Added value of smooth hypointense rim in the hepatobiliary phase of gadoxetic acid-enhanced MRI in identifying tumour capsule and diagnosing hepatocellular carcinoma. Eur Radiol 27(6):2610-2618.Google Scholar
  12. 12.
    Theise ND CM, Franceschi S (2010) Hepatocellular carcinoma. In: Bosman FT CF, Hruban RH, Theise ND (ed) WHO classification of tumours of the digestive system. Lyon: International agency of research on cancer, pp 205-216.Google Scholar
  13. 13.
    Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33(1):159-174.Google Scholar
  14. 14.
    Darnell A, Forner A, Rimola J, Reig M, Garcia-Criado A, Ayuso C, Bruix J (2015) Liver Imaging Reporting and Data System with MR Imaging: Evaluation in Nodules 20 mm or Smaller Detected in Cirrhosis at Screening US. Radiology 275(3):698-707.Google Scholar
  15. 15.
    Zhang YD, Zhu FP, Xu X, Wang Q, Wu CJ, Liu XS, Shi HB (2016) Liver Imaging Reporting and Data System:: Substantial Discordance Between CT and MR for Imaging Classification of Hepatic Nodules. Acad Radiol 23(3):344-352.Google Scholar
  16. 16.
    Becker AS, Barth BK, Marquez PH, Donati OF, Ulbrich EJ, Karlo C, Reiner CS, Fischer MA (2017) Increased interreader agreement in diagnosis of hepatocellular carcinoma using an adapted LI-RADS algorithm. Eur J Radiol 86:33-40.Google Scholar
  17. 17.
    Lee SE, An C, Hwang SH, Choi JY, Han K, Kim MJ (2018) Extracellular contrast agent-enhanced MRI: 15-min delayed phase may improve the diagnostic performance for hepatocellular carcinoma in patients with chronic liver disease. Eur Radiol 28(4):1551-1559.Google Scholar
  18. 18.
    Cha DI, Jang KM, Kim SH, Kang TW, Song KD (2017) Liver Imaging Reporting and Data System on CT and gadoxetic acid-enhanced MRI with diffusion-weighted imaging. Eur Radiol 27(10):4394-4405.Google Scholar
  19. 19.
    Yoon JH, Lee JM, Lee YJ, Lee KB, Han JK (2019) Added Value of sequentially performed gadoxetic acid-enhanced liver MRI for the diagnosis of small (10-19 mm) or atypical hepatic observations at contrast-enhanced CT: A prospective comparison. J Magn Reson Imaging 49(2):574-587.Google Scholar
  20. 20.
    Joo I, Lee JM, Lee DH, Jeon JH, Han JK, Choi BI (2015) Noninvasive diagnosis of hepatocellular carcinoma on gadoxetic acid-enhanced MRI: can hypointensity on the hepatobiliary phase be used as an alternative to washout? Eur Radiol 25(10):2859-2868.Google Scholar
  21. 21.
    Vilgrain V, Boulos L, Vullierme MP, Denys A, Terris B, Menu Y (2000) Imaging of atypical hemangiomas of the liver with pathologic correlation. Radiographics 20(2):379-397.Google Scholar
  22. 22.
    McFarland EG, Mayo-Smith WW, Saini S, Hahn PF, Goldberg MA, Lee MJ (1994) Hepatic hemangiomas and malignant tumors: improved differentiation with heavily T2-weighted conventional spin-echo MR imaging. Radiology 193(1):43-47.Google Scholar
  23. 23.
    Soyer P, Dufresne AC, Somveille E, Scherrer A (1997) Hepatic cavernous hemangioma: appearance on T2-weighted fast spin-echo MR imaging with and without fat suppression. AJR Am J Roentgenol 168(2):461-465.Google Scholar
  24. 24.
    Bennett GL, Petersein A, Mayo-Smith WW, Hahn PF, Schima W, Saini S (2000) Addition of gadolinium chelates to heavily T2-weighted MR imaging: limited role in differentiating hepatic hemangiomas from metastases. AJR Am J Roentgenol 174(2):477-485.Google Scholar
  25. 25.
    Park SH, Lee SS, Yu E, Kang HJ, Park Y, Kim SY, Lee SJ, Shin YM, Lee MG (2017) Combined hepatocellular-cholangiocarcinoma: Gadoxetic acid-enhanced MRI findings correlated with pathologic features and prognosis. J Magn Reson Imaging 46(1):267-280.Google Scholar
  26. 26.
    Fowler KJ, Potretzke TA, Hope TA, Costa EA, Wilson SR (2018) LI-RADS M (LR-M): definite or probable malignancy, not specific for hepatocellular carcinoma. Abdom Radiol (NY) 43(1):149-157.Google Scholar
  27. 27.
    Horvat N, Nikolovski I, Long N, et al. (2018) Imaging features of hepatocellular carcinoma compared to intrahepatic cholangiocarcinoma and combined tumor on MRI using liver imaging and data system (LI-RADS) version 2014. Abdom Radiol (NY) 43(1):169-178.Google Scholar
  28. 28.
    Fowler KJ, Sheybani A, Parker RA, 3rd, Doherty S, E MB, Chapman WC, Menias CO (2013) Combined hepatocellular and cholangiocarcinoma (biphenotypic) tumors: imaging features and diagnostic accuracy of contrast-enhanced CT and MRI. AJR Am J Roentgenol 201(2):332-339.Google Scholar
  29. 29.
    Korean Society of Abdominal R (2017) Diagnosis of Hepatocellular Carcinoma with Gadoxetic Acid-Enhanced MRI: 2016 Consensus Recommendations of the Korean Society of Abdominal Radiology. Korean J Radiol 18(3):427-443.Google Scholar
  30. 30.
    Kim JH, Won HJ, Shin YM, Kim KA, Kim PN (2011) Radiofrequency ablation for the treatment of primary intrahepatic cholangiocarcinoma. AJR Am J Roentgenol 196(2):W205-209.Google Scholar
  31. 31.
    Takahashi K, Obeid J, Burmeister CS, Bruno DA, Kazimi MM, Yoshida A, Abouljoud MS, Schnickel GT (2016) Intrahepatic Cholangiocarcinoma in the Liver Explant After Liver Transplantation: Histological Differentiation and Prognosis. Ann Transplant 21:208-215.Google Scholar
  32. 32.
    Forner A, Vilana R, Ayuso C, et al. (2008) Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: Prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 47(1):97-104.Google Scholar
  33. 33.
    Park MS, Kim S, Patel J, Hajdu CH, Do RK, Mannelli L, Babb JS, Taouli B (2012) Hepatocellular carcinoma: detection with diffusion-weighted versus contrast-enhanced magnetic resonance imaging in pretransplant patients. Hepatology 56(1):140-148.Google Scholar
  34. 34.
    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(2):360-366.Google Scholar
  35. 35.
    Rimola J, Forner A, Tremosini S, Reig M, Vilana R, Bianchi L, Rodriguez-Lope C, Sole M, Ayuso C, Bruix J (2012) Non-invasive diagnosis of hepatocellular carcinoma </= 2 cm in cirrhosis. Diagnostic accuracy assessing fat, capsule and signal intensity at dynamic MRI. J Hepatol 56(6):1317-1323.Google Scholar
  36. 36.
    Choi SH, Byun JH, Lim YS, Yu E, Lee SJ, Kim SY, Won HJ, Shin YM, Kim PN (2016) Diagnostic criteria for hepatocellular carcinoma 3 cm with hepatocyte-specific contrast-enhanced magnetic resonance imaging. J Hepatol 64(5):1099-1107.Google Scholar
  37. 37.
    Cho ES, Choi JY (2015) MRI features of hepatocellular carcinoma related to biologic behavior. Korean J Radiol 16(3):449-464.Google Scholar
  38. 38.
    Fowler KJ, Tang A, Santillan C, et al. (2018) Interreader Reliability of LI-RADS Version 2014 Algorithm and Imaging Features for Diagnosis of Hepatocellular Carcinoma: A Large International Multireader Study. Radiology 286(1):173-185.Google Scholar
  39. 39.
    Chernyak V, Flusberg M, Law A, Kobi M, Paroder V, Rozenblit AM (2018) Liver Imaging Reporting and Data System: Discordance Between Computed Tomography and Gadoxetate-Enhanced Magnetic Resonance Imaging for Detection of Hepatocellular Carcinoma Major Features. J Comput Assist Tomogr 42(1):155-161.Google Scholar
  40. 40.
    Ehman EC, Behr SC, Umetsu SE, Fidelman N, Yeh BM, Ferrell LD, Hope TA (2016) Rate of observation and inter-observer agreement for LI-RADS major features at CT and MRI in 184 pathology proven hepatocellular carcinomas. Abdom Radiol (NY) 41(5):963-969.Google Scholar
  41. 41.
    Zhang YD, Zhu FP, Xu X, Wang Q, Wu CJ, Liu XS, Shi HB (2016) Classifying CT/MR findings in patients with suspicion of hepatocellular carcinoma: Comparison of liver imaging reporting and data system and criteria-free Likert scale reporting models. J Magn Reson Imaging 43(2):373-383.Google Scholar
  42. 42.
    An C, Choi YA, Choi D, Paik YH, Ahn SH, Kim MJ, Paik SW, Han KH, Park MS (2015) Growth rate of early-stage hepatocellular carcinoma in patients with chronic liver disease. Clin Mol Hepatol 21(3):279-286.Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of RadiologyNational Health Insurance Service Ilsan HospitalGoyangSouth Korea
  2. 2.Department of RadiologySeverance HospitalSeoulSouth Korea
  3. 3.Department of Radiology, Severance HospitalYonsei University College of MedicineSeoulSouth Korea
  4. 4.Department of PathologyYonsei University College of MedicineSeoulSouth Korea

Personalised recommendations