European Radiology

, Volume 29, Issue 4, pp 2058–2068 | Cite as

Intra-individual comparison of gadolinium-enhanced MRI using pseudo-golden-angle radial acquisition with gadoxetic acid-enhanced MRI for diagnosis of HCCs using LI-RADS

  • Yoon-Chul Kim
  • Ji Hye Min
  • Young Kon KimEmail author
  • Soon Jin Lee
  • Soohyun Ahn
  • Eunju Kim
  • Hans Peeters
Magnetic Resonance



To determine the usefulness of extracellular contrast agent (ECA)-enhanced multiphasic liver magnetic resonance imaging (MRI) using a pseudo-golden-angle radial acquisition scheme by intra-individual comparison with gadoxetic acid-MRI (EOB-MRI) with regard to image quality and the diagnosis of hepatocellular carcinoma (HCC).

Materials and methods

This prospective study enrolled 15 patients with 18 HCCs who underwent EOB-MRI using a Cartesian approach and ECA-MRI using the pseudo-golden-angle radial acquisition scheme (free-breathing continuous data acquisition for 64 s following ECA injection, generating six images). Two reviewers evaluated the arterial and portal phases of each MRI for artifacts, organ sharpness, and conspicuity of intrahepatic vessels and the hepatic tumors. A Liver Imaging Reporting and Data System category was also assigned to each lesion.


There were no differences in the subjective image quality analysis between the arterial phases of two MRIs (p > 0.05). However, ghosting artifact was seen only in EOB-MRI (N = 3). Six HCCs showed different signal intensities in the arterial phase or portal phase between the two MRIs; five HCCs showed arterial hyperenhancement on ECA-MRI, but not on EOB-MRI. The capsule was observed in 15 HCCs on ECA-MRI and 6 HCCs on EOB-MRI. Five and one HCC were assigned as LR-5 and LR-4 with ECA-MRI and LR-4 and LR-3 with EOB-MRI, respectively.


Free-breathing ECA-enhanced multiphasic liver MRI using a pseudo-golden-angle radial acquisition was more sensitive in detecting arterial hyperenhancement of HCC than conventional EOB-MRI, and the image quality was acceptable.

Key Points

• The pseudo-golden-angle radial acquisition scheme can be applied to perform free-breathing multiphasic dynamic liver MRI.

• Adopting the pseudo-golden-angle radial acquisition scheme can improve the detection of arterial enhancement of HCC.

• The pseudo-golden-angle radial acquisition scheme enables motion-free liver MRI.


Magnetic resonance imaging Carcinoma Hepatocellular Liver Artifacts 



Arterial phase


Extracellular contrast agent


Gadoxetic acid-enhanced MRI


Golden-angle radial sparse parallel


Hepatobiliary phase


Hepatocellular carcinoma


Liver Imaging Reporting and Data System


Magnetic resonance imaging


Pseudo-golden-angle radial acquisition scheme


Portal venous phase



Young Kon Kim received institutional research fund from Guerbet.

Compliance with ethical standards


The scientific guarantor of this publication is Sun Jin Lee in Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea.

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

Soohyun Ahn (author) who is working as an associate professor at the Department of Mathematics of Ajou University is responsible for the statistical analysis of this study.

Informed consent

Written informed consent was obtained from each patient before enrollment in the study.

Ethical approval

This prospective study was approved by our institutional review board and followed the Declaration of Helsinki and subsequent amendments.


• Prospective

• Case-control study

• Performed at one institution

Supplementary material

330_2018_5771_MOESM1_ESM.docx (20 kb)
ESM 1 (DOCX 20 kb)


  1. 1.
    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 275:97–109CrossRefPubMedGoogle Scholar
  2. 2.
    Khalili K, Kim TK, Jang HJ et al (2011) Optimization of imaging diagnosis of 1-2 cm hepatocellular carcinoma: an analysis of diagnostic performance and resource utilization. J Hepatol 54:723–728CrossRefPubMedGoogle Scholar
  3. 3.
    Marin D, Di Martino M, Guerrisi A et al (2009) Hepatocellular carcinoma in patients with cirrhosis: qualitative comparison of gadobenate dimeglumine-enhanced MR imaging and multiphasic 64-section CT. Radiology 251:85–95CrossRefPubMedGoogle Scholar
  4. 4.
    Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Fujita N, Nishie A, Kubo Y et al (2015) Hepatocellular carcinoma: clinical significance of signal heterogeneity in the hepatobiliary phase of gadoxetic acid-enhanced MR imaging. Eur Radiol 25:211–220CrossRefPubMedGoogle Scholar
  6. 6.
    Onishi H, Kim T, Imai Y et al (2012) Hypervascular hepatocellular carcinomas: detection with gadoxetate disodium-enhanced MR imaging and multiphasic multidetector CT. Eur Radiol 22:845–854CrossRefPubMedGoogle Scholar
  7. 7.
    Akai H, Yasaka K, Nojima M et al (2018) Gadoxetate disodium-induced tachypnoea and the effect of dilution method: a proof-of-concept study in mice. Eur Radiol 28:692–697CrossRefPubMedGoogle Scholar
  8. 8.
    Pietryga JA, Burke LM, Marin D, Jaffe TA, Bashir MR (2014) Respiratory motion artifact affecting hepatic arterial phase imaging with gadoxetate disodium: examination recovery with a multiple arterial phase acquisition. Radiology 271:426–434CrossRefPubMedGoogle Scholar
  9. 9.
    Yoo JL, Lee CH, Park YS et al (2016) The short breath-hold technique, controlled aliasing in parallel imaging results in higher acceleration, can be the first step to overcoming a degraded hepatic arterial phase in liver magnetic resonance imaging: a prospective randomized control study. Invest Radiol 51:440–446CrossRefPubMedGoogle Scholar
  10. 10.
    Park YS, Lee CH, Yoo JL et al (2016) Hepatic arterial phase in gadoxetic acid-enhanced liver magnetic resonance imaging: analysis of respiratory patterns and their effect on image quality. Invest Radiol 51:127–133CrossRefPubMedGoogle Scholar
  11. 11.
    Park YS, Lee CH, Kim IS et al (2014) Usefulness of controlled aliasing in parallel imaging results in higher acceleration in gadoxetic acid-enhanced liver magnetic resonance imaging to clarify the hepatic arterial phase. Invest Radiol 49:183–188CrossRefPubMedGoogle Scholar
  12. 12.
    Kim SM, Heo SH, Kim JW et al (2014) Hepatic arterial phase on gadoxetic acid-enhanced liver MR imaging: a randomized comparison of 0.5 mL/s and 1 mL/s injection rates. Korean J Radiol 15:605–612CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Tamada T, Ito K, Yoshida K et al (2011) Comparison of three different injection methods for arterial phase of Gd-EOB-DTPA enhanced MR imaging of the liver. Eur J Radiol 80:e284–e288CrossRefPubMedGoogle Scholar
  14. 14.
    Kim YK, Lin WC, Sung K et al (2017) Reducing artifacts during arterial phase of gadoxetate disodium-enhanced MR imaging: dilution method versus reduced injection rate. Radiology 283:429–437CrossRefPubMedGoogle Scholar
  15. 15.
    Song JS, Choi EJ, Park EH, Lee JH (2018) Comparison of transient severe motion in gadoxetate disodium and gadopentetate dimeglumine-enhanced MRI: effect of modified breath-holding method. Eur Radiol 28:1132–1139CrossRefPubMedGoogle Scholar
  16. 16.
    Gutzeit A, Matoori S, Froehlich JM et al (2016) Reduction in respiratory motion artefacts on gadoxetate-enhanced MRI after training technicians to apply a simple and more patient-adapted breathing command. Eur Radiol 26:2714–2722CrossRefPubMedGoogle Scholar
  17. 17.
    Weiss J, Taron J, Othman AE et al (2017) Feasibility of self-gated isotropic radial late-phase MR imaging of the liver. Eur Radiol 27:985–994CrossRefPubMedGoogle Scholar
  18. 18.
    Koda M, Matsunaga Y, Ueki M et al (2004) Qualitative assessment of tumor vascularity in hepatocellular carcinoma by contrast-enhanced coded ultrasound: comparison with arterial phase of dynamic CT and conventional color/power Doppler ultrasound. Eur Radiol 14:1100–1108CrossRefPubMedGoogle Scholar
  19. 19.
    Rohrer M, Bauer H, Mintorovitch J, Requardt M, Weinmann HJ (2005) Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol 40:715–724CrossRefPubMedGoogle Scholar
  20. 20.
    Min JH, Kim YK, Kang TW et al (2018) Artifacts during the arterial phase of gadoxetate disodium-enhanced MRI: multiple arterial phases using view-sharing from two different vendors versus single arterial phase imaging. Eur Radiol 28:3335–3346CrossRefPubMedGoogle Scholar
  21. 21.
    Lustig M, Donoho D, Pauly JM (2007) Sparse MRI: the application of compressed sensing for rapid MR imaging. Magn Reson Med 58:1182–1195CrossRefPubMedGoogle Scholar
  22. 22.
    Chandarana H, Feng L, Block TK et al (2013) Free-breathing contrast-enhanced multiphase MRI of the liver using a combination of compressed sensing, parallel imaging, and golden-angle radial sampling. Invest Radiol 48:10–16CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Chandarana H, Block TK, Rosenkrantz AB et al (2011) Free-breathing radial 3D fat-suppressed T1-weighted gradient echo sequence: a viable alternative for contrast-enhanced liver imaging in patients unable to suspend respiration. Invest Radiol 46:648–653CrossRefPubMedGoogle Scholar
  24. 24.
    Chandarana H, Feng L, Ream J et al (2015) Respiratory motion-resolved compressed sensing reconstruction of free-breathing radial acquisition for dynamic liver magnetic resonance imaging. Invest Radiol 50:749–756CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Yoon JH, Lee JM, Yu MH et al (2018) Evaluation of transient motion during gadoxetic acid-enhanced multiphasic liver magnetic resonance imaging using free-breathing golden-angle radial sparse parallel magnetic resonance imaging. Invest Radiol 53:52–61CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Feng L, Grimm R, Block KT et al (2014) Golden-angle radial sparse parallel MRI: combination of compressed sensing, parallel imaging, and golden-angle radial sampling for fast and flexible dynamic volumetric MRI. Magn Reson Med 72:707–717CrossRefPubMedGoogle Scholar
  27. 27.
    Winkelmann S, Schaeffter T, Koehler T, Eggers H, Doessel O (2007) An optimal radial profile order based on the golden ratio for time-resolved MRI. IEEE Trans Med Imaging 26:68–76CrossRefPubMedGoogle Scholar
  28. 28.
    Chan RW, Ramsay EA, Cheung EY, Plewes DB (2012) The influence of radial undersampling schemes on compressed sensing reconstruction in breast MRI. Magn Reson Med 67:363–377CrossRefPubMedGoogle Scholar
  29. 29.
    Usman M, Atkinson D, Odille F et al (2013) Motion corrected compressed sensing for free-breathing dynamic cardiac MRI. Magn Reson Med 70:504–516CrossRefPubMedGoogle Scholar
  30. 30.
    Hedderich DM, Weiss K, Spiro JE et al (2018) Clinical evaluation of free-breathing contrast-enhanced T1w MRI of the liver using pseudo golden angle radial k-space sampling. Rofo 190:601–609CrossRefPubMedGoogle Scholar
  31. 31.
    Chandarana H, Block TK, Ream J et al (2015) Estimating liver perfusion from free-breathing continuously acquired dynamic gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced acquisition with compressed sensing reconstruction. Invest Radiol 50:88–94CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Uecker M, Ong F, Tamir J et al (2015) Berkeley advanced reconstruction toolbox. In: Proceedings of the 23rd Annual Meeting of ISMRM, Toronto, p 2486Google Scholar
  33. 33.
    Eggers H, Brendel B, Duijndam A, Herigault G (2011) Dual-echo Dixon imaging with flexible choice of echo times. Magn Reson Med 65:96–107CrossRefPubMedGoogle Scholar
  34. 34.
    Deák Z, Grimm JM, Treitl M et al (2013) Filtered back projection, adaptive statistical iterative reconstruction, and a model-based iterative reconstruction in abdominal CT: an experimental clinical study. Radiology 266:197–206CrossRefPubMedGoogle Scholar
  35. 35.
    Elsayes KM, Hooker JC, Agrons MM et al (2017) 2017 version of LI-RADS for CT and MR imaging: an update. Radiographics 37:1994–2017CrossRefPubMedGoogle Scholar
  36. 36.
    Park G, Kim YK, Kim CS, Yu HC, Hwang SB (2010) Diagnostic efficacy of gadoxetic acid-enhanced MRI in the detection of hepatocellular carcinomas: comparison with gadopentetate dimeglumine. Br J Radiol 83:1010–1016CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Mori K, Yoshioka H, Takahashi N et al (2005) Triple arterial phase dynamic MRI with sensitivity encoding for hypervascular hepatocellular carcinoma: comparison of the diagnostic accuracy among the early, middle, late, and whole triple arterial phase imaging. AJR Am J Roentgenol 184:63–69CrossRefPubMedGoogle Scholar
  38. 38.
    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 25:2859–2868CrossRefPubMedGoogle Scholar
  39. 39.
    Doo KW, Lee CH, Choi JW, Lee J, Kim KA, Park CM (2009) “Pseudo washout” sign in high-flow hepatic hemangioma on gadoxetic acid contrast-enhanced MRI mimicking hypervascular tumor. AJR Am J Roentgenol 193:W490–W496CrossRefPubMedGoogle Scholar
  40. 40.
    Okamoto D, Yoshimitsu K, Nishie A et al (2012) Enhancement pattern analysis of hypervascular hepatocellular carcinoma on dynamic MR imaging with histopathological correlation: validity of portal phase imaging for predicting tumor grade. Eur J Radiol 81:1116–1121CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  1. 1.Clinical Research Institute, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulRepublic of Korea
  2. 2.Department of Radiology, Chungnam National University HospitalChungnam National University College of MedicineDaejeonRepublic of Korea
  3. 3.Department of Radiology and Center for Imaging Science, Samsung Medical CenterSungkyunkwan University School of MedicineSeoulRepublic of Korea
  4. 4.Department of MathematicsAjou UniversitySuwonRepublic of Korea
  5. 5.MR Clinical Scientist Philips Korea, Sowol-ro 2-gil, Joong-guSeoulRepublic of Korea
  6. 6.MR Clinical Scientist Philips Netherlands: Veenpluis 4-6, Building QR-0.113, 5684 PC BestNetherlands

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