Skip to main content
SpringerLink
Log in

Hepatobiliary phase of gadoxetic acid–enhanced MRI in patients with HCC: prognostic features before resection, ablation, or TACE

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

Abstract

Objectives

Patients with hepatocellular carcinoma (HCC) receiving different treatments might have specific prognostic factors that can be captured in the hepatobiliary phase (HBP) of gadoxetic acid–enhanced magnetic resonance imaging (GA-MRI). We aimed to identify the clinical findings and HBP features with prognostic value in patients with HCC.

Methods

In this retrospective, single-institution study, we included patients with Barcelona Clinic Liver Cancer very early/early stage HCC who underwent GA-MRI before treatment. After performing propensity score matching, 183 patients received the following treatments: resection, radiofrequency ablation (RFA), and transarterial chemoembolization (TACE) (n = 61 for each). Cox regression models were used to identify clinical factors and HBP features associated with disease-free survival (DFS) and overall survival (OS).

Results

In the resection group, large tumor size was associated with poor DFS (hazard ratio [HR] 4.159 per centimeter; 95% confidence interval [CI], 1.669–10.365) and poor OS (HR 8.498 per centimeter; 95% CI, 1.072–67.338). In the RFA group, satellite nodules on HBP images were associated with poor DFS (HR 5.037; 95% CI, 1.061–23.903) and poor OS (HR 9.398; 95% CI, 1.480–59.668). Peritumoral hypointensity on HBP images was also associated with poor OS (HR 13.062; 95% CI, 1.627–104.840). In addition, serum albumin levels and the prothrombin time-international normalized ratio were associated with DFS and/or OS. Finally, in the TACE group, no variables were associated with DFS/OS.

Conclusions

Different HBP features and clinical factors were associated with DFS/OS among patients with HCC receiving different treatments.

Key Points

• In patients who underwent resection for HCC, a large tumor size on HBP images was associated with poor disease-free survival and overall survival.

• In the RFA group, satellite nodules and peritumoral hypointensity on HBP images, along with decreased serum albumin levels and PT-INR, were associated with poor disease-free survival and/or overall survival.

• In the TACE group, no clinical or HBP imaging features were associated with disease-free survival or overall survival.

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

Access this article

Log in via an institution

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

AFP:

Alpha-fetoprotein

BCLC:

Barcelona Clinic Liver Cancer

GA-MRI:

Gadoxetic acid–enhanced magnetic resonance imaging

HBP:

Hepatobiliary phase

HCC:

Hepatocellular carcinoma

MVI:

Microvascular invasion

PT-INR:

Prothrombin time-international normalized ratio

RFA:

Radiofrequency ablation

TACE:

Transarterial chemoembolization

References

  1. Marrero JA, Kulik LM, Sirlin CB et al (2018) Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American Association for the Study of Liver Diseases. Hepatology 68:723–750

    Article  Google Scholar 

  2. European Association for the Study of the Liver (2018) EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 69:182–236

  3. Korean Liver Cancer Association (KLCA); National Cancer Center (NCC), Goyang, Korea (2019) 2018 Korean Liver Cancer Association-National Cancer Center Korea practice guidelines for the management of hepatocellular carcinoma. Korean J Radiol 20:1042–1113

  4. 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  Google Scholar 

  5. 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

    Article  Google Scholar 

  6. Renzulli M, Biselli M, Brocchi S et al (2018) New hallmark of hepatocellular carcinoma, early hepatocellular carcinoma and high-grade dysplastic nodules on Gd-EOB-DTPA MRI in patients with cirrhosis: a new diagnostic algorithm. Gut 67:1674–1682

    Article  CAS  Google Scholar 

  7. Kim YY, Park MS, Aljoqiman KS, Choi JY, Kim MJ (2019) Gadoxetic acid-enhanced magnetic resonance imaging: hepatocellular carcinoma and mimickers. Clin Mol Hepatol 25:223–233

    Article  PubMed  Google Scholar 

  8. Hamm B, Staks T, Muhler A et al (1995) Phase I clinical evaluation of Gd-EOB-DTPA as a hepatobiliary MR contrast agent: safety, pharmacokinetics, and MR imaging. Radiology 195:785–792

    Article  CAS  Google Scholar 

  9. Huppertz A, Balzer T, Blakeborough A et al (2004) Improved detection of focal liver lesions at MR imaging: multicenter comparison of gadoxetic acid-enhanced MR images with intraoperative findings. Radiology 230:266–275

    Article  Google Scholar 

  10. Lee S, Kim SH, Lee JE, Sinn DH, Park CK (2017) Preoperative gadoxetic acid-enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma. J Hepatol 67:526–534

    Article  CAS  Google Scholar 

  11. Ahn SJ, Kim JH, Park SJ, Kim ST, Han JK (2019) Hepatocellular carcinoma: preoperative gadoxetic acid-enhanced MR imaging can predict early recurrence after curative resection using image features and texture analysis. Abdom Radiol (NY) 44:539–548

    Article  Google Scholar 

  12. Yamashita T, Kitao A, Matsui O et al (2014) Gd-EOB-DTPA-enhanced magnetic resonance imaging and alpha-fetoprotein predict prognosis of early-stage hepatocellular carcinoma. Hepatology 60:1674–1685

    Article  CAS  PubMed  Google Scholar 

  13. Lee S, Kang TW, Song KD et al (2019) Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Ann Surg. https://doi.org/10.1097/SLA.0000000000003268

  14. Romanzi A, Ariizumi S, Kotera Y et al (2020) Hepatocellular carcinoma with a non-smooth tumor margin on hepatobiliary-phase gadoxetic acid disodium-enhanced magnetic resonance imaging. Is sectionectomy the suitable treatment? J Hepatobiliary Pancreat Sci. https://doi.org/10.1002/jhbp.743

  15. Besa C, Lewis S, Pandharipande PV et al (2017) Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid. Abdom Radiol (NY) 42:179–190

    Article  Google Scholar 

  16. Teratani T, Yoshida H, Shiina S et al (2006) Radiofrequency ablation for hepatocellular carcinoma in so-called high-risk locations. Hepatology 43:1101–1108

    Article  Google Scholar 

  17. Golfieri R, Cappelli A, Cucchetti A et al (2011) Efficacy of selective transarterial chemoembolization in inducing tumor necrosis in small (<5 cm) hepatocellular carcinomas. Hepatology 53:1580–1589

    Article  Google Scholar 

  18. McDonald RJ, McDonald JS, Kallmes DF, Carter RE (2013) Behind the numbers: propensity score analysis-a primer for the diagnostic radiologist. Radiology 269:640–645

    Article  Google Scholar 

  19. Ariizumi S, Kitagawa K, Kotera Y et al (2011) A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Sci 18:575–585

    Article  Google Scholar 

  20. An C, Rhee H, Han K et al (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 27:2610–2618

    Article  Google Scholar 

  21. Kim KA, Kim MJ, Jeon HM et al (2012) Prediction of microvascular invasion of hepatocellular carcinoma: usefulness of peritumoral hypointensity seen on gadoxetate disodium-enhanced hepatobiliary phase images. J Magn Reson Imaging 35:629–634

    Article  Google Scholar 

  22. 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 

  23. Tamada T, Ito K, Yamamoto A et al (2013) Simple Method for evaluating the degree of liver parenchymal enhancement in the hepatobiliary phase of gadoxetic acid-enhanced magnetic resonance imaging. J Magn Reson Imaging 37:1115–1121

    Article  Google Scholar 

  24. Tamada T, Ito K, Sone T, Kanki A, Sato T, Higashi H (2011) Gd-EOB-DTPA enhanced MR imaging: evaluation of biliary and renal excretion in normal and cirrhotic livers. Eur J Radiol 80:e207–e211

    Article  Google Scholar 

  25. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  26. Chen SL, Xiao H, Xie ZL et al (2020) The presence of microvascular invasion guides treatment strategy in recurrent HBV-related HCC. Eur Radiol 30:3473–3485

    Article  Google Scholar 

  27. Renzulli M, Brocchi S, Cucchetti A et al (2016) Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology 279:432–442

    Article  Google Scholar 

  28. Lu DS, Siripongsakun S, Kyong Lee J et al (2013) Complete tumor encapsulation on magnetic resonance imaging: a potentially useful imaging biomarker for better survival in solitary large hepatocellular carcinoma. Liver Transpl 19:283–291

    Article  Google Scholar 

  29. McHugh PP, Gilbert J, Vera S, Koch A, Ranjan D, Gedaly R (2010) Alpha-fetoprotein and tumour size are associated with microvascular invasion in explanted livers of patients undergoing transplantation with hepatocellular carcinoma. HPB (Oxford) 12:56–61

    Article  Google Scholar 

  30. Kim JY, Kim MJ, Kim KA, Jeong HT, Park YN (2012) Hyperintense HCC on hepatobiliary phase images of gadoxetic acid-enhanced MRI: correlation with clinical and pathological features. Eur J Radiol 81:3877–3882

    Article  PubMed  Google Scholar 

  31. Zhang L, Yu X, Wei W et al (2020) Prediction of HCC microvascular invasion with gadobenate-enhanced MRI: correlation with pathology. Eur Radiol. https://doi.org/10.1007/s00330-020-06895-6

  32. Lee S, Kim KW, Jeong WK et al (2020) Gadoxetic acid-enhanced MRI as a predictor of recurrence of HCC after liver transplantation. Eur Radiol 30:987–995

    Article  Google Scholar 

  33. Kim B, Lee JH, Kim JK, Kim HJ, Kim YB, Lee D (2018) The capsule appearance of hepatocellular carcinoma in gadoxetic acid-enhanced MR imaging: correlation with pathology and dynamic CT. Medicine (Baltimore) 97:e11142

    Article  Google Scholar 

  34. Lee S, Kim SH, Hwang JA, Lee JE, Ha SY (2019) Pre-operative ADC predicts early recurrence of HCC after curative resection. Eur Radiol 29:1003–1012

    Article  Google Scholar 

  35. Muhi A, Ichikawa T, Motosugi U et al (2013) Diffusion-weighted imaging of hepatocellular carcinoma for predicting early recurrence and survival after hepatectomy. Hepatol Int 7:662–668

    Article  Google Scholar 

  36. Rhee H, Cho ES, Nahm JH et al (2020) Gadoxetic acid-enhanced MRI of macrotrabecular-massive hepatocellular carcinoma and its prognostic implications. J Hepatol. https://doi.org/10.1016/j.jhep.2020.08.013

  37. Kim BK, Kim KA, An C et al (2015) Prognostic role of magnetic resonance imaging vs. computed tomography for hepatocellular carcinoma undergoing chemoembolization. Liver Int 35:1722–1730

    Article  Google Scholar 

  38. Park C, Kim JH, Kim PH et al (2020) Imaging predictors of survival in patients with single small hepatocellular carcinoma treated with transarterial chemoembolization. Korean J Radiol. https://doi.org/10.3348/kjr.2020.0325

  39. Bellest L, Eschwège V, Poupon R, Chazouillères O, Robert A (2007) A modified international normalized ratio as an effective way of prothrombin time standardization in hepatology. Hepatology 46:528–534

    Article  Google Scholar 

  40. Garcia-Martinez R, Caraceni P, Bernardi M, Gines P, Arroyo V, Jalan R (2013) Albumin: pathophysiologic basis of its role in the treatment of cirrhosis and its complications. Hepatology 58:1836–1846

    Article  CAS  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

  1. Department of Radiology, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Republic of Korea

    Jae Seok Bae, Jung Hoon Kim, Dong Ho Lee, Jae Hyun Kim & Joon Koo Han

  2. Department of Radiology, Seoul National University College of Medicine, 103 Daehak-ro, Jongno-gu, Seoul, 03080, Republic of Korea

    Jae Seok Bae, Jung Hoon Kim, Dong Ho Lee, Jae Hyun Kim & Joon Koo Han

  3. Department of Surgery, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul, 03080, Republic of Korea

    Jung Hoon Kim & Joon Koo Han

Authors
  1. Jae Seok Bae
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jung Hoon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong Ho Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jae Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joon Koo Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jung Hoon Kim.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Joon Koo Han.

Conflict of interest

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.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

This retrospective study was approved by our Institutional Review Board, and patient informed consent was waived.

Ethical approval

Institutional Review Board approval was obtained (IRB No. 1901-036-1001).

Methodology

• retrospective

• cross-sectional study

• performed at one institution

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 56 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bae, J.S., Kim, J.H., Lee, D.H. et al. Hepatobiliary phase of gadoxetic acid–enhanced MRI in patients with HCC: prognostic features before resection, ablation, or TACE. Eur Radiol 31, 3627–3637 (2021). https://doi.org/10.1007/s00330-020-07499-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-020-07499-w

Keywords

Search

Navigation