European Radiology

, Volume 26, Issue 9, pp 3102–3111 | Cite as

Identification of Imaging Predictors Discriminating Different Primary Liver Tumours in Patients with Chronic Liver Disease on Gadoxetic Acid-enhanced MRI: a Classification Tree Analysis

  • Hyun Jeong Park
  • Kyung Mi JangEmail author
  • Tae Wook Kang
  • Kyoung Doo Song
  • Seong Hyun Kim
  • Young Kon Kim
  • Dong Ik Cha
  • Joungyoun Kim
  • Juna Goo



To identify predictors for the discrimination of intrahepatic cholangiocarcinoma (IMCC) and combined hepatocellular-cholangiocarcinoma (CHC) from hepatocellular carcinoma (HCC) for primary liver cancers on gadoxetic acid-enhanced MRI among high-risk chronic liver disease (CLD) patients using classification tree analysis (CTA).


A total of 152 patients with histopathologically proven IMCC (n = 40), CHC (n = 24) and HCC (n = 91) were enrolled. Tumour marker and MRI variables including morphologic features, signal intensity, and enhancement pattern were used to identify tumours suspicious for IMCC and CHC using CTA.


On CTA, arterial rim enhancement (ARE) was the initial splitting predictor for assessing the probability of tumours being IMCC or CHC. Of 43 tumours that were classified in a subgroup on CTA based on the presence of ARE, non-intralesional fat, and non-globular shape, 41 (95.3 %) were IMCCs (n = 29) or CHCs (n = 12). All 24 tumours showing fat on MRI were HCCs. The CTA model demonstrated sensitivity of 84.4 %, specificity of 97.8 %, and accuracy of 92.3 % for discriminating IMCCs and CHCs from HCCs.


We established a simple CTA model for classifying a high-risk group of CLD patients with IMCC and CHC. This model may be useful for guiding diagnosis for primary liver cancers in patients with CLD.

Key Points

Arterial rim enhancement was the initial splitting predictor on CTA.

CTA model achieved high sensitivity, specificity, and accuracy for discrimination of tumours.

This model may be useful for guiding diagnosis of primary liver cancers.


Hepatocellular carcinoma Cholangiocarcinoma Combined hepatocellular-cholangiocarcinoma Gadoxetic acid Classification tree analysis 



The scientific guarantor of this publication is J.M. Jang. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. One of the authors, J. Kim, has significant statistical expertise.. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. Methodology: retrospective, diagnostic or prognostic study, performed at one institution.


  1. 1.
    Sorensen HT, Friis S, Olsen JH et al (1998) Risk of liver and other types of cancer in patients with cirrhosis: a nationwide cohort study in Denmark. Hepatology 28:921–925CrossRefPubMedGoogle Scholar
  2. 2.
    Shaib YH, El-Serag HB, Davila JA, Morgan R, McGlynn KA (2005) Risk factors of intrahepatic cholangiocarcinoma in the United States: a case-control study. Gastroenterology 128:620–626CrossRefPubMedGoogle Scholar
  3. 3.
    Yamamoto S, Kubo S, Hai S et al (2004) Hepatitis C virus infection as a likely etiology of intrahepatic cholangiocarcinoma. Cancer Sci 95:592–595CrossRefPubMedGoogle Scholar
  4. 4.
    Jarnagin WR, Weber S, Tickoo SK et al (2002) Combined hepatocellular and cholangiocarcinoma: demographic, clinical, and prognostic factors. Cancer 94:2040–2046CrossRefPubMedGoogle Scholar
  5. 5.
    Chantajitr S, Wilasrusmee C, Lertsitichai P, Phromsopha N (2006) Combined hepatocellular and cholangiocarcinoma: clinical features and prognostic study in a Thai population. J Hepatobiliary Pancreat Surg 13:537–542CrossRefPubMedGoogle Scholar
  6. 6.
    Bruix J, Sherman M, American Association for the Study of Liver D (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Lieser MJ, Barry MK, Rowland C, Ilstrup DM, Nagorney DM (1998) Surgical management of intrahepatic cholangiocarcinoma: a 31-year experience. J Hepatobiliary Pancreat Surg 5:41–47CrossRefPubMedGoogle Scholar
  8. 8.
    Valverde A, Bonhomme N, Farges O, Sauvanet A, Flejou JF, Belghiti J (1999) Resection of intrahepatic cholangiocarcinoma: a Western experience. J Hepatobiliary Pancreat Surg 6:122–127CrossRefPubMedGoogle Scholar
  9. 9.
    Yin X, Zhang BH, Qiu SJ et al (2012) Combined hepatocellular carcinoma and cholangiocarcinoma: clinical features, treatment modalities, and prognosis. Ann Surg Oncol 19:2869–2876CrossRefPubMedGoogle Scholar
  10. 10.
    Sapisochin G, Fidelman N, Roberts JP, Yao FY (2011) Mixed hepatocellular cholangiocarcinoma and intrahepatic cholangiocarcinoma in patients undergoing transplantation for hepatocellular carcinoma. Liver Transpl 17:934–942CrossRefPubMedGoogle Scholar
  11. 11.
    Lee WS, Lee KW, Heo JS et al (2006) Comparison of combined hepatocellular and cholangiocarcinoma with hepatocellular carcinoma and intrahepatic cholangiocarcinoma. Surg Today 36:892–897CrossRefPubMedGoogle Scholar
  12. 12.
    Kadoya M, Matsui O, Takashima T, Nonomura A (1992) Hepatocellular carcinoma: correlation of MR imaging and histopathologic findings. Radiology 183:819–825CrossRefPubMedGoogle Scholar
  13. 13.
    Maetani Y, Itoh K, Watanabe C et al (2001) MR imaging of intrahepatic cholangiocarcinoma with pathologic correlation. AJR Am J Roentgenol 176:1499–1507CrossRefPubMedGoogle Scholar
  14. 14.
    Chong YS, Kim YK, Lee MW et al (2012) Differentiating mass-forming intrahepatic cholangiocarcinoma from atypical hepatocellular carcinoma using gadoxetic acid-enhanced MRI. Clin Radiol 67:766–773CrossRefPubMedGoogle Scholar
  15. 15.
    Burns PN, Wilson SR (2007) Focal liver masses: enhancement patterns on contrast-enhanced images—concordance of US scans with CT scans and MR images. Radiology 242:162–174CrossRefPubMedGoogle Scholar
  16. 16.
    Rimola J, Forner A, Reig M et al (2009) Cholangiocarcinoma in cirrhosis: absence of contrast washout in delayed phases by magnetic resonance imaging avoids misdiagnosis of hepatocellular carcinoma. Hepatology 50:791–798CrossRefPubMedGoogle Scholar
  17. 17.
    Kawamura Y, Ikeda K, Hirakawa M et al (2010) New classification of dynamic computed tomography images predictive of malignant characteristics of hepatocellular carcinoma. Hepatol Res 40:1006–1014CrossRefPubMedGoogle Scholar
  18. 18.
    Kang Y, Lee JM, Kim SH, Han JK, Choi BI (2012) Intrahepatic mass-forming cholangiocarcinoma: enhancement patterns on gadoxetic acid-enhanced MR images. Radiology 264:751–760CrossRefPubMedGoogle Scholar
  19. 19.
    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 38:793–801CrossRefPubMedGoogle Scholar
  20. 20.
    Choi YS, Rhee H, Choi JY et al (2013) Histological characteristics of small hepatocellular carcinomas showing atypical enhancement patterns on gadoxetic acid-enhanced MR imaging. J Magn Reson Imaging 37:1384–1391CrossRefPubMedGoogle Scholar
  21. 21.
    Choi JW, Lee JM, Kim SJ et al (2013) Hepatocellular carcinoma: imaging patterns on gadoxetic acid-enhanced MR Images and their value as an imaging biomarker. Radiology 267:776–786CrossRefPubMedGoogle Scholar
  22. 22.
    Shetty AS, Fowler KJ, Brunt EM, Agarwal S, Narra VR, Menias CO (2014) Combined hepatocellular-cholangiocarcinoma: what the radiologist needs to know about biphenotypic liver carcinoma. Abdom Imaging 39:310–322CrossRefPubMedGoogle Scholar
  23. 23.
    Silva MA, Hegab B, Hyde C, Guo B, Buckels JA, Mirza DF (2008) Needle track seeding following biopsy of liver lesions in the diagnosis of hepatocellular cancer: a systematic review and meta-analysis. Gut 57:1592–1596CrossRefPubMedGoogle Scholar
  24. 24.
    Khan SA, Davidson BR, Goldin R et al (2002) Guidelines for the diagnosis and treatment of cholangiocarcinoma: consensus document. Gut 51(Suppl 6):VI1–VI9PubMedPubMedCentralGoogle Scholar
  25. 25.
    Leo Breiman , Jerome Friedman, Charles J. Stone and R.A. Olshen (1984) Classification and Regression Trees. Chapman and Hall/CRCGoogle Scholar
  26. 26.
    Befeler AS, Hayashi PH, Di Bisceglie AM (2005) Liver transplantation for hepatocellular carcinoma. Gastroenterology 128:1752–1764CrossRefPubMedGoogle Scholar
  27. 27.
    Marti-Bonmati L, Talens A, del Olmo J et al (1993) Chronic hepatitis and cirrhosis: evaluation by means of MR imaging with histologic correlation. Radiology 188:37–43CrossRefPubMedGoogle Scholar
  28. 28.
    Koh J, Chung YE, Nahm JH et al (2015) Intrahepatic mass-forming cholangiocarcinoma: prognostic value of preoperative gadoxetic acid-enhanced MRI. Eur Radiol. doi: 10.1007/s00330-015-3846-5 PubMedCentralGoogle Scholar
  29. 29.
    American College of Radiology (2013) Liver Imaging Reporting and Data System version 2013.1. Accessed Jan 2013
  30. 30.
    El Malki HO, El Mejdoubi Y, Souadka A et al (2010) Predictive model of biliocystic communication in liver hydatid cysts using classification and regression tree analysis. BMC Surg 10:16CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Thomassin-Naggara I, Toussaint I, Perrot N et al (2011) Characterization of complex adnexal masses: value of adding perfusion- and diffusion-weighted MR imaging to conventional MR imaging. Radiology 258:793–803CrossRefPubMedGoogle Scholar
  32. 32.
    Nunes LW, Schnall MD, Orel SG (2001) Update of breast MR imaging architectural interpretation model. Radiology 219:484–494CrossRefPubMedGoogle Scholar
  33. 33.
    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–W611CrossRefPubMedGoogle Scholar
  34. 34.
    Hwang J, Kim YK, Park MJ et al (2012) Differentiating combined hepatocellular and cholangiocarcinoma from mass-forming intrahepatic cholangiocarcinoma using gadoxetic acid-enhanced MRI. J Magn Reson Imaging 36:881–889CrossRefPubMedGoogle Scholar
  35. 35.
    Kierans AS, Leonardou P, Hayashi P et al (2010) MRI findings of rapidly progressive hepatocellular carcinoma. Magn Reson Imaging 28:790–796CrossRefPubMedGoogle Scholar
  36. 36.
    An C, Kim DW, Park YN, Chung YE, Rhee H, Kim MJ (2015) Single Hepatocellular Carcinoma: Preoperative MR Imaging to Predict Early Recurrence after Curative Resection. Radiology 142394Google Scholar
  37. 37.
    Yu JS, Chung JJ, Kim JH, Kim KW (2007) Fat-containing nodules in the cirrhotic liver: chemical shift MRI features and clinical implications. AJR Am J Roentgenol 188:1009–1016CrossRefPubMedGoogle Scholar
  38. 38.
    Martin J, Sentis M, Zidan A et al (1995) Fatty metamorphosis of hepatocellular carcinoma: detection with chemical shift gradient-echo MR imaging. Radiology 195:125–130CrossRefPubMedGoogle Scholar
  39. 39.
    Kutami R, Nakashima Y, Nakashima O, Shiota K, Kojiro M (2000) Pathomorphologic study on the mechanism of fatty change in small hepatocellular carcinoma of humans. J Hepatol 33:282–289CrossRefPubMedGoogle Scholar
  40. 40.
    Asayama Y, Nishie A, Ishigami K et al (2015) Distinguishing intrahepatic cholangiocarcinoma from poorly differentiated hepatocellular carcinoma using precontrast and gadoxetic acid-enhanced MRI. Diagn Interv Radiol 21:96–104CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© European Society of Radiology 2015

Authors and Affiliations

  • Hyun Jeong Park
    • 1
  • Kyung Mi Jang
    • 2
    Email author
  • Tae Wook Kang
    • 2
  • Kyoung Doo Song
    • 2
  • Seong Hyun Kim
    • 2
  • Young Kon Kim
    • 2
  • Dong Ik Cha
    • 2
  • Joungyoun Kim
    • 3
  • Juna Goo
    • 3
  1. 1.Department of Radiology, Chung-Ang University HospitalChung-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.Biostatistics and Clinical Epidemiology Center, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulRepublic of Korea

Personalised recommendations