Abdominal Radiology

, Volume 44, Issue 9, pp 3115–3126 | Cite as

Differentiation of hypervascular primary hepatic tumors showing hepatobiliary hypointensity on gadoxetic acid-enhanced magnetic resonance imaging

  • Hyun Jeong Park
  • Young Kon KimEmail author
  • Ji Hye Min
  • Jisun Lee
  • Soon Jin Lee
  • Eun Sun Lee
  • Soohyun Ahn



To determine the imaging features that help differentiate hypervascular primary hepatic tumors showing hepatobiliary hypointensity on gadoxetic acid MRI.


This study comprised 148 patients with pathologically proven hypervascular hepatic tumors who underwent gadoxetic acid MRI. Tumors included 23 atypical focal nodular hyperplasias (FNHs), 11 hepatocellular adenomas (HCAs), 15 neuroendocrine tumors (NETs), 25 intrahepatic cholangiocarcinomas (ICCs), and 74 hepatocellular carcinomas (HCCs). MRIs were analyzed for morphologic features, signal intensity, and enhancement pattern of the tumors to determine the differential features using multivariate logistic regression analysis. We evaluated the diagnostic performance of the MRI features for differentiating the five tumor types upon review by two observers.


Multivariate analysis revealed that reverse target sign on hepatobiliary phase in FNHs (p = 0.009), iso or hyperintensity on ADC map in FNHs and HCAs (p = 0.009, < 0.001, respectively), central hypointensity on arterial phase in NETs (p = 0.001), hepatobiliary target sign in ICCs (p = 0.002), the presence of septum and capsule in HCCs (all p < 0.001) were significant independent features of each tumor group over other tumor groups. Diagnostic accuracy for both observers was 98–98.6% for FNHs, 96.6–98% for HCAs, 97.3–98.6% for NETs, 90.5–94.6% for ICCs, and 85.8–93.2% for HCCs.


Ancillary MRI features established in our study can be helpful in the differentiation of hypervascular and hepatobiliary hypointense primary hepatic tumors on gadoxetic acid MRI.


Gadoxetic acid MRI Hypervascular hepatic tumor Ancillary feature 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

261_2019_2068_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 15 kb)


  1. 1.
    Neri E, Bali MA, Ba-Ssalamah A, Boraschi P, Brancatelli G, Alves FC, Grazioli L, Helmberger T, Lee JM, Manfredi R, Marti-Bonmati L, Matos C, Merkle EM, Op De Beeck B, Schima W, Skehan S, Vilgrain V, Zech C, Bartolozzi C (2016) ESGAR consensus statement on liver MR imaging and clinical use of liver-specific contrast agents. Eur Radiol 26:921-931. CrossRefGoogle Scholar
  2. 2.
    Choi JY, Lee JM, Sirlin CB (2014) CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology 272:635-654. CrossRefGoogle Scholar
  3. 3.
    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
  4. 4.
    Hamm B, Staks T, Muhler A, Bollow M, Taupitz M, Frenzel T, Wolf KJ, Weinmann HJ, Lange L (1995) Phase I clinical evaluation of Gd-EOB-DTPA as a hepatobiliary MR contrast agent: safety, pharmacokinetics, and MR imaging. Radiology 195:785-792. CrossRefGoogle Scholar
  5. 5.
    Stern W, Schick F, Kopp AF, Reimer P, Shamsi K, Claussen CD, Laniado M (2000) Dynamic MR imaging of liver metastases with Gd-EOB-DTPA. Acta Radiol 41:255-262CrossRefGoogle Scholar
  6. 6.
    Chen BB, Hsu CY, Yu CW, Wei SY, Kao JH, Lee HS, Shih TT (2012) Dynamic contrast-enhanced magnetic resonance imaging with Gd-EOB-DTPA for the evaluation of liver fibrosis in chronic hepatitis patients. Eur Radiol 22:171-180. CrossRefGoogle Scholar
  7. 7.
    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
  8. 8.
    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
  9. 9.
    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
  10. 10.
    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
  11. 11.
    Chung YE, Kim MJ, Kim YE, Park MS, Choi JY, Kim KW (2013) Characterization of incidental liver lesions: comparison of multidetector CT versus Gd-EOB-DTPA-enhanced MR imaging. PLoS One 8:e66141. CrossRefGoogle Scholar
  12. 12.
    Rimola J, Forner A, Reig M, Vilana R, de Lope CR, Ayuso C, Bruix J (2009) Cholangiocarcinoma in cirrhosis: absence of contrast washout in delayed phases by magnetic resonance imaging avoids misdiagnosis of hepatocellular carcinoma. Hepatology 50:791-798. CrossRefGoogle Scholar
  13. 13.
    Chong YS, Kim YK, Lee MW, Kim SH, Lee WJ, Rhim HC, Lee SJ (2012) Differentiating mass-forming intrahepatic cholangiocarcinoma from atypical hepatocellular carcinoma using gadoxetic acid-enhanced MRI. Clin Radiol 67:766-773. CrossRefGoogle Scholar
  14. 14.
    Jeong HT, Kim MJ, Chung YE, Choi JY, Park YN, Kim KW (2013) Gadoxetate disodium-enhanced MRI of mass-forming intrahepatic cholangiocarcinomas: imaging-histologic correlation. AJR Am J Roentgenol 201:W603-611. CrossRefGoogle Scholar
  15. 15.
    Kang Y, Lee JM, Kim SH, Han JK, Choi BI (2012) Intrahepatic mass-forming cholangiocarcinoma: enhancement patterns on gadoxetic acid-enhanced MR images. Radiology 264:751-760. CrossRefGoogle Scholar
  16. 16.
    Fujiwara H, Sekine S, Onaya H, Shimada K, Mikata R, Arai Y (2011) Ring-like enhancement of focal nodular hyperplasia with hepatobiliary-phase Gd-EOB-DTPA-enhanced magnetic resonance imaging: radiological-pathological correlation. Jpn J Radiol 29:739-743. CrossRefGoogle Scholar
  17. 17.
    Yoon JH, Kim JY (2014) Atypical Findings of Focal Nodular Hyperplasia with Gadoxetic Acid (Gd-EOB-DTPA)-Enhanced Magnetic Resonance Imaging. Iran J Radiol 11:e9269. Google Scholar
  18. 18.
    Grazioli L, Bondioni MP, Haradome H, Motosugi U, Tinti R, Frittoli B, Gambarini S, Donato F, Colagrande S (2012) Hepatocellular adenoma and focal nodular hyperplasia: value of gadoxetic acid-enhanced MR imaging in differential diagnosis. Radiology 262:520-529. CrossRefGoogle Scholar
  19. 19.
    van Kessel CS, de Boer E, ten Kate FJ, Brosens LA, Veldhuis WB, van Leeuwen MS (2013) Focal nodular hyperplasia: hepatobiliary enhancement patterns on gadoxetic-acid contrast-enhanced MRI. Abdom Imaging 38:490-501. CrossRefGoogle Scholar
  20. 20.
    Hwang YH, Lee SJ, Kang KY, Hur JS, Yee ST (2017) Immunosuppressive Effects of Bryoria sp. (Lichen-Forming Fungus) Extracts via Inhibition of CD8(+) T-Cell Proliferation and IL-2 Production in CD4(+) T Cells. J Microbiol Biotechnol 27:1189-1197. Google Scholar
  21. 21.
    Ishigami K, Yoshimitsu K, Nishihara Y, Irie H, Asayama Y, Tajima T, Nishie A, Hirakawa M, Ushijima Y, Okamoto D, Taketomi A, Honda H (2009) Hepatocellular carcinoma with a pseudocapsule on gadolinium-enhanced MR images: correlation with histopathologic findings. Radiology 250:435-443. CrossRefGoogle Scholar
  22. 22.
    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
  23. 23.
    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 64:1099-1107. CrossRefGoogle Scholar
  24. 24.
    Kadoya M, Matsui O, Takashima T, Nonomura A (1992) Hepatocellular carcinoma: correlation of MR imaging and histopathologic findings. Radiology 183:819-825. CrossRefGoogle Scholar
  25. 25.
    Suh YJ, Kim MJ, Choi JY, Park YN, Park MS, Kim KW (2011) Differentiation of hepatic hyperintense lesions seen on gadoxetic acid-enhanced hepatobiliary phase MRI. AJR Am J Roentgenol 197:W44-52. CrossRefGoogle Scholar
  26. 26.
    Chen ZG, Xu L, Zhang SW, Huang Y, Pan RH (2015) Lesion discrimination with breath-hold hepatic diffusion-weighted imaging: a meta-analysis. World J Gastroenterol 21:1621-1627. CrossRefGoogle Scholar
  27. 27.
    Taouli B, Koh DM (2010) Diffusion-weighted MR imaging of the liver. Radiology 254:47-66. CrossRefGoogle Scholar
  28. 28.
    Grazioli L, Olivetti L, Mazza G, Bondioni MP (2013) MR Imaging of Hepatocellular Adenomas and Differential Diagnosis Dilemma. Int J Hepatol 2013:374170. CrossRefGoogle Scholar
  29. 29.
    An HS, Park HS, Kim YJ, Jung SI, Jeon HJ (2013) Focal nodular hyperplasia: characterisation at gadoxetic acid-enhanced MRI and diffusion-weighted MRI. Br J Radiol 86:20130299. CrossRefGoogle Scholar
  30. 30.
    Karam AR, Shankar S, Surapaneni P, Kim YH, Hussain S (2010) Focal nodular hyperplasia: central scar enhancement pattern using Gadoxetate Disodium. J Magn Reson Imaging 32:341-344. CrossRefGoogle Scholar
  31. 31.
    Zech CJ, Grazioli L, Breuer J, Reiser MF, Schoenberg SO (2008) Diagnostic performance and description of morphological features of focal nodular hyperplasia in Gd-EOB-DTPA-enhanced liver magnetic resonance imaging: results of a multicenter trial. Invest Radiol 43:504-511. CrossRefGoogle Scholar
  32. 32.
    Joo I, Lee JM, Lee SM, Lee JS, Park JY, Han JK (2016) Diagnostic accuracy of liver imaging reporting and data system (LI-RADS) v2014 for intrahepatic mass-forming cholangiocarcinomas in patients with chronic liver disease on gadoxetic acid-enhanced MRI. J Magn Reson Imaging 44:1330-1338. CrossRefGoogle Scholar
  33. 33.
    Bader TR, Semelka RC, Chiu VC, Armao DM, Woosley JT (2001) MRI of carcinoid tumors: spectrum of appearances in the gastrointestinal tract and liver. J Magn Reson Imaging 14:261-269CrossRefGoogle Scholar
  34. 34.
    Woodard PK, Feldman JM, Paine SS, Baker ME (1995) Midgut carcinoid tumors: CT findings and biochemical profiles. J Comput Assist Tomogr 19:400-405CrossRefGoogle Scholar
  35. 35.
    Kim JE, Lee WJ, Kim SH, Rhim H, Song HJ, Park CK (2011) Three-phase helical computed tomographic findings of hepatic neuroendocrine tumors: pathologic correlation with revised WHO classification. J Comput Assist Tomogr 35:697-702. CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Hyun Jeong Park
    • 1
  • Young Kon Kim
    • 2
    Email author
  • Ji Hye Min
    • 3
  • Jisun Lee
    • 4
  • Soon Jin Lee
    • 2
  • Eun Sun Lee
    • 1
  • Soohyun Ahn
    • 5
  1. 1.Department of RadiologyChung-Ang University Hospital, Chung-Ang University College of MedicineSeoulRepublic of Korea
  2. 2.Department of Radiology and Center for Imaging Science, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulRepublic of Korea
  3. 3.Department of RadiologyChungnam National University Hospital, Chungnam National University College of MedicineDaejeonRepublic of Korea
  4. 4.Department of RadiologyChungbuk National University HospitalCheongjuRepublic of Korea
  5. 5.Department of MathematicsAjou UniversitySuwonRepublic of Korea

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