Skip to main content
Log in

Retrospective validation of a new diagnostic criterion for hepatocellular carcinoma on gadoxetic acid-enhanced MRI: can hypointensity on the hepatobiliary phase be used as an alternative to washout with the aid of ancillary features?

  • Gastrointestinal
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To validate new diagnostic criteria for hepatocellular carcinoma (HCC) on gadoxetic acid-enhanced MR imaging (Gd-EOB-MRI) using hypointensity on the hepatobiliary phase (HBP) as an alternative to washout in combination with ancillary features.

Methods

This retrospective study included 288 patients at high risk for HCC with 387 nodules (HCCs, n=292; non-HCCs, n=95) showing arterial phase hyper-enhancement (APHE) ≥1 cm on Gd-EOB-MRI. Imaging diagnoses of HCCs were made using different criteria: APHE plus hypointensity on the portal venous phase (PVP) (criterion 1), APHE plus hypointensity on the PVP and/or transitional phase (TP) (criterion 2), APHE plus hypointensity on the PVP and/or TP and/or HBP (criterion 3), and criterion 3 plus non-LR-1/2/M according to the Liver Imaging Reporting and Data System (LI-RADS) v2017 considering ancillary features (criterion 4). Sensitivities and specificities of those criteria were compared using McNemar’s test.

Results

Among diagnostic criteria for HCCs, criteria 3 and 4 showed significantly higher sensitivities (93.8% and 92.5%, respectively) than criteria 1 and 2 (70.9% and 86.6%, respectively) (p values <0.001). The specificity of criterion 4 (87.4%) was shown to be significantly higher than that of criterion 3 (48.4%, p<0.001), albeit comparable to criterion 2 (86.3%, p>0.999) and significantly lower than criterion 1 (97.9%, p=0.002).

Conclusions

In the non-invasive diagnosis of HCCs on Gd-EOB-MRI, HBP hypointensity may be used as an alternative to washout enabling a highly sensitive diagnosis with little loss in specificity if it is used after excluding nodules considered to be benignities or non-HCC malignancies based on characteristic imaging features.

Key Points

• Gd-EOB-MRI enhancement and ancillary features can be used to diagnose HCC.

• Exclusion of LR-1/2/M improves specificity when HBP hypointensity is used.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AP:

Hepatic arterial phase

Gd-EOB-MRI:

Gadoxetic acid-enhanced magnetic resonance imaging

HBP:

Hepatobiliary phase

HCC:

Hepatocellular carcinoma

LI-RADS:

Liver Imaging Reporting and Data System

PVP:

Portal venous phase

TP:

Transitional phase

References

  1. Balogh J, Victor D 3rd, Asham EH et al (2016) Hepatocellular carcinoma: a review. J Hepatocell Carcinoma 3:41–53

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bertuccio P, Turati F, Carioli G et al (2017) Global trends and predictions in hepatocellular carcinoma mortality. J Hepatol 67:302–309

    Article  PubMed  Google Scholar 

  3. Heimbach JK, Kulik LM, Finn RS et al (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358–380

    Article  PubMed  Google Scholar 

  4. European Association for the Study of the Liver (2018) EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. https://doi.org/10.1016/j.jhep.2018.03.019

  5. Omata M, Cheng AL, Kokudo N et al (2017) Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatol Int 11:317–370

    Article  PubMed  Google Scholar 

  6. Korean Liver Cancer Study Group (KLCSG), National Cancer Center Korea (NCC) (2015) 2014 Korean Liver Cancer Study Group-National Cancer Center Korea practice guideline for the management of hepatocellular carcinoma. Korean J Radiol 16:465–522

    Article  Google Scholar 

  7. Xie DY, Ren ZG, Zhou J, Fan J, Gao Q (2017) Critical appraisal of Chinese 2017 guideline on the management of hepatocellular carcinoma. Hepatobiliary Surg Nutr 6:387–396

    Article  PubMed  PubMed Central  Google Scholar 

  8. Tang A, Cruite I, Mitchell DG, Sirlin CB (2018) Hepatocellular carcinoma imaging systems: why they exist, how they have evolved, and how they differ. Abdom Radiol (NY) 43:3–12

    Article  Google Scholar 

  9. Kudo M, Matsui O, Izumi N et al (2014) JSH Consensus-Based Clinical Practice Guidelines for the Management of Hepatocellular Carcinoma: 2014 Update by the Liver Cancer Study Group of Japan. Liver Cancer 3:458–468

    Article  PubMed  PubMed Central  Google Scholar 

  10. Roberts LR, Sirlin CB, Zaiem F et al (2018) Imaging for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Hepatology 67:401–421

    Article  PubMed  Google Scholar 

  11. Chou R, Cuevas C, Fu R et al (2015) Imaging techniques for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Ann Intern Med 162:697–711

    Article  PubMed  Google Scholar 

  12. Lee YJ, Lee JM, Lee JS et al (2015) Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology 275:97–109

    Article  PubMed  Google Scholar 

  13. Ye F, Liu J, Ouyang H (2015) Gadolinium ethoxybenzyl diethylenetriamine pentaacetic acid (Gd-EOB-DTPA)-enhanced magnetic resonance imaging and multidetector-row computed tomography for the diagnosis of hepatocellular carcinoma: a systematic review and meta-analysis. Medicine (Baltimore) 94:e1157

    Article  CAS  Google Scholar 

  14. Kim YN, Song JS, Moon WS, Hwang HP, Kim YK (2018) Intra-individual comparison of hepatocellular carcinoma imaging features on contrast-enhanced computed tomography, gadopentetate dimeglumine-enhanced MRI, and gadoxetic acid-enhanced MRI. Acta Radiol 59:639–648

    Article  PubMed  Google Scholar 

  15. Hanna RF, Miloushev VZ, Tang A et al (2016) Comparative 13-year meta-analysis of the sensitivity and positive predictive value of ultrasound, CT, and MRI for detecting hepatocellular carcinoma. Abdom Radiol (NY) 41:71–90

    Article  Google Scholar 

  16. 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

    Article  PubMed  Google Scholar 

  17. Li X, Li C, Wang R, Ren J, Yang J, Zhang Y (2015) Combined application of gadoxetic acid disodium-enhanced Magnetic Resonance Imaging (MRI) and Diffusion-Weighted Imaging (DWI) in the diagnosis of chronic liver disease-induced hepatocellular carcinoma: a meta-analysis. PLoS One 10:e0144247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kudo M, Izumi N, Kokudo N et al (2011) Management of hepatocellular carcinoma in Japan: consensus-based clinical practice guidelines proposed by the Japan Society of Hepatology (JSH) 2010 updated version. Dig Dis 29:339–364

    Article  PubMed  Google Scholar 

  19. Elsayes KM, Hooker JC, Agrons MM et al (2017) 2017 version of LI-RADS for CT and MR imaging: an update. Radiographics 37:1994–2017

    Article  PubMed  Google Scholar 

  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 25:2859–2868

  21. Tang A, Bashir MR, Corwin MT et al (2017) Evidence supporting LI-RADS major features for CT- and MR imaging-based diagnosis of hepatocellular carcinoma: a systematic review. Radiology. https://doi.org/10.1148/radiol.2017170554:170554

  22. Kim SS, Hwang JC, Lim SG, Ahn SJ, Cheong JY, Cho SW (2014) Effect of virological response to entecavir on the development of hepatocellular carcinoma in hepatitis B viral cirrhotic patients: comparison between compensated and decompensated cirrhosis. Am J Gastroenterol 109:1223–1233

    Article  CAS  PubMed  Google Scholar 

  23. An C, Park MS, Kim D et al (2013) Added value of subtraction imaging in detecting arterial enhancement in small (<3 cm) hepatic nodules on dynamic contrast-enhanced MRI in patients at high risk of hepatocellular carcinoma. Eur Radiol 23:924–930

    Article  PubMed  Google Scholar 

  24. Nino-Murcia M, Olcott EW, Jeffrey RB Jr, Lamm RL, Beaulieu CF, Jain KA (2000) Focal liver lesions: pattern-based classification scheme for enhancement at arterial phase CT. Radiology 215:746–751

    Article  CAS  PubMed  Google Scholar 

  25. Kielar AZ, Chernyak V, Bashir MR et al (2018) LI-RADS 2017: an update. J Magn Reson Imaging. https://doi.org/10.1002/jmri.26027

  26. 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 61:1056–1065

    Article  PubMed  Google Scholar 

  27. Joo I, Lee JM, Lee DH, Ahn SJ, Lee ES, Han JK (2017) Liver imaging reporting and data system v2014 categorization of hepatocellular carcinoma on gadoxetic acid-enhanced MRI: Comparison with multiphasic multidetector computed tomography. J Magn Reson Imaging 45:731–740

    Article  PubMed  Google Scholar 

  28. Allen BC, Ho LM, Jaffe TA, Miller CM, Mazurowski MA, Bashir MR (2018) Comparison of visualization rates of LI-RADS version 2014 major features with IV gadobenate dimeglumine or gadoxetate disodium in patients at risk for hepatocellular carcinoma. AJR Am J Roentgenol. https://doi.org/10.2214/AJR.17.18981:1-7

  29. Kim YY, An C, Kim S, Kim MJ (2017) Diagnostic accuracy of prospective application of the Liver Imaging Reporting and Data System (LI-RADS) in gadoxetate-enhanced MRI. Eur Radiol. https://doi.org/10.1007/s00330-017-5188-y

  30. Choi SH, Byun JH, Kim SY et al (2016) Liver imaging reporting and data system v2014 with gadoxetate disodium-enhanced magnetic resonance imaging: validation of LI-RADS category 4 and 5 criteria. Invest Radiol 51:483–490

    Article  CAS  PubMed  Google Scholar 

  31. Ronot M, Fouque O, Esvan M, Lebigot J, Aube C, Vilgrain V (2017) Comparison of the accuracy of AASLD and LI-RADS criteria for the non-invasive diagnosis of HCC smaller than 3 cm. J Hepatol. https://doi.org/10.1016/j.jhep.2017.12.014

  32. Korean Society of Abdominal Radiology (2017) Diagnosis of hepatocellular carcinoma with gadoxetic acid-enhanced MRI: 2016 consensus recommendations of the korean society of abdominal radiology. Korean J Radiol 18:427–443

    Article  Google Scholar 

  33. Kim HD, Lim YS, Han S et al (2015) Evaluation of early-stage hepatocellular carcinoma by magnetic resonance imaging with gadoxetic acid detects additional lesions and increases overall survival. Gastroenterology 148:1371–1382

    Article  CAS  PubMed  Google Scholar 

  34. Chen N, Motosugi U, Morisaka H et al (2016) Added Value of a Gadoxetic Acid-enhanced Hepatocyte-phase Image to the LI-RADS System for Diagnosing Hepatocellular Carcinoma. Magn Reson Med Sci 15:49–59

    Article  CAS  PubMed  Google Scholar 

  35. Joo I, Lee JM (2016) Recent advances in the imaging diagnosis of hepatocellular carcinoma: value of gadoxetic acid-enhanced MRI. Liver Cancer 5:67–87

    Article  CAS  PubMed  Google Scholar 

  36. Fraum TJ, Tsai R, Rohe E et al (2017) Differentiation of hepatocellular carcinoma from other hepatic malignancies in patients at risk: diagnostic performance of the liver imaging reporting and data system version 2014. Radiology. https://doi.org/10.1148/radiol.2017170114:170114

  37. Cerny M, Bergeron C, Billiard JS et al (2018) LI-RADS for MR imaging diagnosis of hepatocellular carcinoma: performance of major and ancillary features. Radiology. https://doi.org/10.1148/radiol.2018171678:171678

  38. Choi SH, Lee SS, Kim SY et al (2017) Intrahepatic cholangiocarcinoma in patients with cirrhosis: differentiation from hepatocellular carcinoma by using gadoxetic acid-enhanced MR imaging and dynamic CT. Radiology 282:771–781

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Chris Woo, B.A. for editing the manuscript.

Funding

The authors state that this work has not received any funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeong Min Lee.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Jeong Min Lee.

Conflict of interest

The authors of this article declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

The same study cohort has been previously reported in Eur Radiol 2015; 25: 2859-68.

Methodology

• Retrospective, diagnostic study, performed at one institution

Electronic supplementary material

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Joo, I., Lee, J.M., Lee, D.H. et al. Retrospective validation of a new diagnostic criterion for hepatocellular carcinoma on gadoxetic acid-enhanced MRI: can hypointensity on the hepatobiliary phase be used as an alternative to washout with the aid of ancillary features?. Eur Radiol 29, 1724–1732 (2019). https://doi.org/10.1007/s00330-018-5727-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-018-5727-1

Keywords

Navigation