Abdominal Radiology

, Volume 42, Issue 1, pp 179–190 | Cite as

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

  • Cecilia Besa
  • Sara Lewis
  • Pari V. Pandharipande
  • Jagpreet Chhatwal
  • Amita Kamath
  • Nancy Cooper
  • Ashley Knight-Greenfield
  • James S. Babb
  • Paolo Boffetta
  • Norma Padron
  • Claude B. Sirlin
  • Bachir TaouliEmail author



The purpose of this study was to evaluate the diagnostic performance of a “simulated” abbreviated MRI (AMRI) protocol using diffusion-weighted imaging (DWI) and T1-weighted (T1w) imaging obtained at the hepatobiliary phase (HBP) post gadoxetic acid injection alone and in combination, compared to dynamic contrast-enhanced (CE)-T1w imaging for the detection of hepatocellular carcinoma (HCC).


This was an IRB approved HIPAA compliant retrospective single institution study including patients with liver disease who underwent gadoxetic acid-enhanced MRI for HCC diagnosis. Three independent observers assessed 2 sets of images (full CE-set and AMRI including DWI+T1w-HBP). Diagnostic performance of T1w-HBP and DWI alone and in combination was compared to that of CE-set. All imaging sets included unenhanced T1w and T2w sequences. A preliminary analysis was performed to assess cost savings of AMRI protocol compared to a full MRI study.


174 patients including 62 with 80 HCCs were assessed. Equivalent per-patient sensitivity and negative predictive value (NPV) were observed for DWI (85.5% and 92.2%, pooled data) and T1w-HBP (89.8% and 94.2%) (P = 0.1–0.7), while these were significantly lower for the full AMRI protocol (DWI+T1w-HBP, 80.6% and 80%, P = 0.02) when compared to CE-set (90.3% and 94.9%). Higher specificity and positive predictive value were observed for CE-set vs. AMRI (P = 0.02). The estimated cost reduction of AMRI versus full MRI ranged between 30.7 and 49.0%.


AMRI using DWI and T1w-HBP has a clinically acceptable sensitivity and NPV for HCC detection. This could serve as the basis for a future study assessing AMRI for HCC screening and surveillance.


Hepatocellular carcinoma MRI Diffusion-weighted imaging Gadoxetic acid 


Compliance with Ethical Standards

Conflict of interest

C. B. Sirlin is a consultant to Bayer Healthcare and a member of an advisory board for Bayer Healthcare.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

The Institutional Review Board at our institution approved this single-center retrospective study and the need for informed consent was waived.


  1. 1.
    Davarpanah AH, Weinreb JC (2013) The role of imaging in hepatocellular carcinoma: the present and future. J Clin Gastroenterol 47(Suppl):S7–10. doi: 10.1097/MCG.0b013e31827f0d3d CrossRefPubMedGoogle Scholar
  2. 2.
    Bruix J, Sherman M, American Association for the Study of Liver D (2011) Management of hepatocellular carcinoma: an update. Hepatology 53(3):1020–1022. doi: 10.1002/hep.24199 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Bluemke DA, Sahani D, Amendola M, et al. (2005) Efficacy and safety of MR imaging with liver-specific contrast agent: U.S. multicenter phase III study. Radiology 237(1):89–98. doi: 10.1148/radiol.2371031842 CrossRefPubMedGoogle Scholar
  4. 4.
    Bartolozzi C, Crocetti L, Lencioni R, et al. (2007) Biliary and reticuloendothelial impairment in hepatocarcinogenesis: the diagnostic role of tissue-specific MR contrast media. Eur Radiol 17(10):2519–2530. doi: 10.1007/s00330-007-0602-5 CrossRefPubMedGoogle Scholar
  5. 5.
    Park MJ, Kim YK, Lee MW, et al. (2012) Small hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns. Radiology 264(3):761–770. doi: 10.1148/radiol.12112517 CrossRefPubMedGoogle Scholar
  6. 6.
    Lee MH, Kim SH, Park MJ, Park CK, Rhim H (2011) Gadoxetic acid-enhanced hepatobiliary phase MRI and high-b-value diffusion-weighted imaging to distinguish well-differentiated hepatocellular carcinomas from benign nodules in patients with chronic liver disease. AJR Am J Roentgenol 197(5):W868–875. doi: 10.2214/AJR.10.6237 CrossRefPubMedGoogle Scholar
  7. 7.
    Ahn SS, Kim MJ, Lim JS, et al. (2010) Added value of gadoxetic acid-enhanced hepatobiliary phase MR imaging in the diagnosis of hepatocellular carcinoma. Radiology 255(2):459–466. doi: 10.1148/radiol.10091388 CrossRefPubMedGoogle Scholar
  8. 8.
    Sano K, Ichikawa T, Motosugi U, et al. (2011) Imaging study of early hepatocellular carcinoma: usefulness of gadoxetic acid-enhanced MR imaging. Radiology 261(3):834–844. doi: 10.1148/radiol.11101840 CrossRefPubMedGoogle Scholar
  9. 9.
    Di Martino M, Marin D, Guerrisi A, et al. (2010) Intraindividual comparison of gadoxetate disodium-enhanced MR imaging and 64-section multidetector CT in the Detection of hepatocellular carcinoma in patients with cirrhosis. Radiology 256(3):806–816. doi: 10.1148/radiol.10091334 CrossRefPubMedGoogle Scholar
  10. 10.
    Kim SH, Kim SH, Lee J, et al. (2009) Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. AJR Am J Roentgenol 192(6):1675–1681. doi: 10.2214/AJR.08.1262 CrossRefPubMedGoogle Scholar
  11. 11.
    Choi JS, Kim MJ, Choi JY, et al. (2010) Diffusion-weighted MR imaging of liver on 3.0-Tesla system: effect of intravenous administration of gadoxetic acid disodium. Eur Radiol 20(5):1052–1060. doi: 10.1007/s00330-009-1651-8 CrossRefPubMedGoogle Scholar
  12. 12.
    Kim YK, Kim YK, Park HJ, et al. (2014) Noncontrast MRI with diffusion-weighted imaging as the sole imaging modality for detecting liver malignancy in patients with high risk for hepatocellular carcinoma. Magn Reson Imaging 32(6):610–618. doi: 10.1016/j.mri.2013.12.021 CrossRefPubMedGoogle Scholar
  13. 13.
    Muhi A, Ichikawa T, Motosugi U, et al. (2012) Diffusion- and T(2)-weighted MR imaging of the liver: effect of intravenous administration of gadoxetic acid disodium. Magn Reson Med Sci 11(3):185–191CrossRefPubMedGoogle Scholar
  14. 14.
    Parikh T, Drew SJ, Lee VS, et al. (2008) Focal liver lesion detection and characterization with diffusion-weighted MR imaging: comparison with standard breath-hold T2-weighted imaging. Radiology 246(3):812–822CrossRefPubMedGoogle Scholar
  15. 15.
    Cruite I, Schroeder M, Merkle EM, Sirlin CB (2010) Gadoxetate disodium-enhanced MRI of the liver: part 2, protocol optimization and lesion appearance in the cirrhotic liver. AJR Am J Roentgenol 195(1):29–41. doi: 10.2214/AJR.10.4538 CrossRefPubMedGoogle Scholar
  16. 16.
    Fattovich G, Giustina G, Degos F, et al. (1997) Morbidity and mortality in compensated cirrhosis type C: a retrospective follow-up study of 384 patients. Gastroenterology 112(2):463–472CrossRefPubMedGoogle Scholar
  17. 17.
    Njei B, Rotman Y, Ditah I, Lim JK (2015) Emerging trends in hepatocellular carcinoma incidence and mortality. Hepatology 61(1):191–199. doi: 10.1002/hep.27388 CrossRefPubMedGoogle Scholar
  18. 18.
    Altekruse SF, Henley SJ, Cucinelli JE, McGlynn KA (2014) Changing hepatocellular carcinoma incidence and liver cancer mortality rates in the United States. Am J Gastroenterol 109(4):542–553. doi: 10.1038/ajg.2014.11 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    European Association For The Study Of The Liver (2012) EASL–EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56(4):908–943. doi: 10.1016/j.jhep.2011.12.001 CrossRefGoogle Scholar
  20. 20.
    Hecht EM, Holland AE, Israel GM, et al. (2006) Hepatocellular carcinoma in the cirrhotic liver: gadolinium-enhanced 3D T1-weighted MR imaging as a stand-alone sequence for diagnosis. Radiology 239(2):438–447. doi: 10.1148/radiol.2392050551 CrossRefPubMedGoogle Scholar
  21. 21.
    Forner A, Vilana R, Ayuso C, et al. (2008) Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology 47(1):97–104. doi: 10.1002/hep.21966 CrossRefPubMedGoogle Scholar
  22. 22.
    Sun HY, Lee JM, Shin CI, et al. (2010) Gadoxetic acid-enhanced magnetic resonance imaging for differentiating small hepatocellular carcinomas (≤2 cm in diameter) from arterial enhancing pseudolesions: special emphasis on hepatobiliary phase imaging. Invest Radiol 45(2):96–103. doi: 10.1097/RLI.0b013e3181c5faf7 CrossRefPubMedGoogle Scholar
  23. 23.
    Bashir MR, Gupta RT, Davenport MS, et al. (2013) Hepatocellular carcinoma in a North American population: does hepatobiliary MR imaging with Gd-EOB-DTPA improve sensitivity and confidence for diagnosis? J Magn Reson Imaging JMRI 37(2):398–406. doi: 10.1002/jmri.23818 CrossRefPubMedGoogle Scholar
  24. 24.
    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(12):3877–3882. doi: 10.1016/j.ejrad.2012.07.021 CrossRefPubMedGoogle Scholar
  25. 25.
    Kitao A, Zen Y, Matsui O, et al. (2010) Hepatocellular carcinoma: signal intensity at gadoxetic acid-enhanced MR Imaging–correlation with molecular transporters and histopathologic features. Radiology 256(3):817–826. doi: 10.1148/radiol.10092214 CrossRefPubMedGoogle Scholar
  26. 26.
    Kogita S, Imai Y, Okada M, et al. (2010) Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol 20(10):2405–2413. doi: 10.1007/s00330-010-1812-9 CrossRefPubMedGoogle Scholar
  27. 27.
    Xu PJ, Yan FH, Wang JH, et al. (2010) Contribution of diffusion-weighted magnetic resonance imaging in the characterization of hepatocellular carcinomas and dysplastic nodules in cirrhotic liver. J Comput Assist Tomogr 34(4):506–512. doi: 10.1097/RCT.0b013e3181da3671 CrossRefPubMedGoogle Scholar
  28. 28.
    Kim JE, Kim SH, Lee SJ, Rhim H (2011) Hypervascular hepatocellular carcinoma 1 cm or smaller in patients with chronic liver disease: characterization with gadoxetic acid-enhanced MRI that includes diffusion-weighted imaging. AJR Am J Roentgenol 196(6):W758–765. doi: 10.2214/AJR.10.4394 CrossRefPubMedGoogle Scholar
  29. 29.
    Hwang J, Kim YK, Kim JM, et al. (2014) Pretransplant diagnosis of hepatocellular carcinoma by gadoxetic acid-enhanced and diffusion-weighted magnetic resonance imaging. Liver Transplant 20(12):1436–1446. doi: 10.1002/lt.23974 Google Scholar
  30. 30.
    Piana G, Trinquart L, Meskine N, et al. (2011) New MR imaging criteria with a diffusion-weighted sequence for the diagnosis of hepatocellular carcinoma in chronic liver diseases. J Hepatol 55(1):126–132. doi: 10.1016/j.jhep.2010.10.023 CrossRefPubMedGoogle Scholar
  31. 31.
    Park MS, Kim S, Patel J, et al. (2012) Hepatocellular carcinoma: detection with diffusion-weighted versus contrast-enhanced magnetic resonance imaging in pretransplant patients. Hepatology 56(1):140–148. doi: 10.1002/hep.25681 CrossRefPubMedGoogle Scholar
  32. 32.
    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(996):1010–1016. doi: 10.1259/bjr/66686028 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Golfieri R, Renzulli M, Lucidi V, et al. (2011) Contribution of the hepatobiliary phase of Gd-EOB-DTPA-enhanced MRI to Dynamic MRI in the detection of hypovascular small (≤2 cm) HCC in cirrhosis. Eur Radiol 21(6):1233–1242. doi: 10.1007/s00330-010-2030-1 CrossRefPubMedGoogle Scholar
  34. 34.
    Fattovich G, Stroffolini T, Zagni I, Donato F (2004) Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 127(5 Suppl 1):S35–50CrossRefPubMedGoogle Scholar
  35. 35.
    Kudo M (2009) Multistep human hepatocarcinogenesis: correlation of imaging with pathology. J Gastroenterol 44(Suppl 19):112–118. doi: 10.1007/s00535-008-2274-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Cecilia Besa
    • 1
    • 2
  • Sara Lewis
    • 2
  • Pari V. Pandharipande
    • 3
  • Jagpreet Chhatwal
    • 3
  • Amita Kamath
    • 2
  • Nancy Cooper
    • 2
  • Ashley Knight-Greenfield
    • 1
  • James S. Babb
    • 4
  • Paolo Boffetta
    • 5
  • Norma Padron
    • 6
  • Claude B. Sirlin
    • 7
  • Bachir Taouli
    • 1
    • 2
    Email author
  1. 1.Translational and Molecular Imaging InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA
  2. 2.Department of RadiologyIcahn School of Medicine at Mount SinaiNew YorkUSA
  3. 3.Institute for Technology Assessment, Department of RadiologyMassachusetts General HospitalBostonUSA
  4. 4.Department of RadiologyNew York University Langone Medical CenterNew YorkUSA
  5. 5.Division of Cancer Prevention and ControlDepartment of Oncological Sciences, Icahn School of Medicine at Mount SinaiNew YorkUSA
  6. 6.Department of Population Health Science and PolicyIcahn School of Medicine at Mount SinaiNew YorkUSA
  7. 7.Liver Imaging Group, Department of RadiologyUniversity of CaliforniaSan DiegoUSA

Personalised recommendations