Korean J Radiol.  2019 Feb;20(2):236-245. 10.3348/kjr.2018.0339.

Identification of Arterial Hyperenhancement in CT and MRI in Patients with Hepatocellular Carcinoma: Value of Unenhanced Images

Affiliations
  • 1Department of Radiology, Hanyang University Medical Center, Hanyang University School of Medicine, Seoul, Korea.
  • 2Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea. kaienes.kang@samsung.com
  • 3Division of Hepatology, Department of Internal Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.
  • 4Statistics and Data Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

Abstract


OBJECTIVE
According to the current guidelines, arterial hyperenhancement for diagnosis of hepatocellular carcinoma (HCC) is determined using the arterial phase only. We investigated the optimal definition of arterial hyperenhancement in patients with HCC using computed tomography (CT) and magnetic resonance imaging (MRI).
MATERIALS AND METHODS
The Institutional Review Board approved this retrospective study. The requirement for informed consent was waived. Between January 2011 and September 2013, 147 consecutive patients with surgically proven HCCs with both pre-operative CT and MRI were included. Identification rates of arterial hyperenhancement on CT and magnetic resonance (MR) images using arterial phase only, dual phase (unenhanced and arterial phases), and also subtraction MR images were assessed qualitatively.
RESULTS
The identification rates for arterial hyperenhancement on CT were significantly different between arterial phase and dual phase (72.8% vs. 90.5%; p < 0.001), whereas the rates were similar on MRI (91.8% vs. 93.9%; p = 0.257). The identification rate of arterial hyperenhancement in MRI increased to 98.6% using subtraction MR images.
CONCLUSION
Visual comparison of arterial and unenhanced phases could be recommended instead of conventional qualitative arterial phase alone assessment to determine arterial hyperenhancement of HCCs, especially when using CT.

Keyword

Hepatocellular carcinoma; Arterial enhancement; Computed tomography; Magnetic resonance imaging; Diagnosis; Contrast; Dynamic imaging

MeSH Terms

Carcinoma, Hepatocellular*
Diagnosis
Ethics Committees, Research
Humans
Informed Consent
Magnetic Resonance Imaging*
Retrospective Studies

Figure

  • Fig. 1 Flow diagram for patient selection.CT = computed tomography, HCCs = hepatocellular carcinomas, MR = magnetic resonance, MRI = magnetic resonance imaging, TACE = transarterial chemoembolization

  • Fig. 2 Map showing identification of qualitative arterial hyperenhancement of HCCs according to used phase and imaging modality by consensus of two radiologists.Numbers in blue boxes represent changes in HCC attenuation or SI compared with surrounding liver on arterial phase. Numbers in green boxes indicate changes in presence of arterial hyperenhancement using dual phase images. Numbers in yellow boxes indicate changes in presence of arterial hyperenhancement using subtraction images. Some HCCs with weak arterial enhancement were not identified on even use of dual phase images. Arterial (−) = absence of arterial hyperenhancement, Arterial (+) = presence of arterial hyperenhancement, N.A. = not-available, SI = signal intensity

  • Fig. 3 Images of 54-year-old man with no arterial enhancement of HCC in arterial phase CT images.A. Unenhanced CT showed 2.9-cm HCC (asterisk) in segment VIII of liver. Black arrow indicates portal vein. B. On arterial phase, mass (asterisk) showed no arterial enhancement compared to surrounding liver. Enhancement of peripheral portal vein represents appropriate late arterial phase (black arrow). Neither radiologist identified arterial enhancement based on arterial phase CT images. Measured absolute HCC enhancement ratio on arterial phase CT was −6.8%. C. On T1-weighted unenhanced MR image, mass (asterisk) showed hypointensity compared to surrounding liver. D. On arterial phase MR image, mass (asterisk) was hyperintense to surrounding liver, representing arterial enhancement. Measured absolute HCC enhancement ratio on arterial phase MR images was 38.2%. E. Subtraction MR image clearly displayed arterial enhancement of index tumor (asterisk).

  • Fig. 4 Images of 42-year-old man with absence of arterial hyperenhancement of HCC in arterial phase CT and MR images.A. Unenhanced CT shows 4.8-cm HCC (asterisk) in segment V of liver. B. On arterial phase, mass (asterisk) showed no arterial hyperenhancement compared to surrounding liver. Measured absolute HCC enhancement ratio on arterial phase CT was −17.9%. C. On T1-weighted unenhanced MR image, mass (asterisk) was hypointense to surrounding liver. D. On arterial phase MR images, mass (asterisk) showed near-iso SI compared to surrounding liver. Neither radiologist identified arterial hyperenhancement based on arterial phase MR images. However, measured absolute HCC enhancement ratio on arterial phase MRI was 10.6%. E. Subtraction MR image showed peripheral arterial enhancing portion clearly within index tumor (asterisk), which can be differentiated with tumor capsule enhancement.

  • Fig. 5 Histogram of quantitative imaging analyses according to imaging modality.A. Absolute HCC enhancement ratio on arterial phase (median values; MRI = 50.26 vs. CT = 27.20; p < 0.001). B. Relative odds ratio of HCC enhancement on dual phases (median values: MRI = 1.81 vs. CT = 1.67; p = 0.001).


Reference

1. Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology. 2011; 53:1020–1022. PMID: 21374666.
Article
2. European Association For The Study Of The Liver. European Organisation For Research And Treatment Of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2012; 56:908–943. PMID: 22424438.
3. Kokudo N, Hasegawa K, Akahane M, Igaki H, Izumi N, Ichida T, et al. Evidence-based clinical practice guidelines for hepatocellular carcinoma: the Japan Society of Hepatology 2013 update (3rd JSH-HCC Guidelines). Hepatol Res. 2015; 45.
Article
4. Korean Liver Cancer Study Group (KLCSG). National Cancer Center, Korea (NCC). 2014 KLCSG-NCC Korea practice guideline for the management of hepatocellular carcinoma. Gut Liver. 2015; 9:267–317. PMID: 25918260.
5. Korean Society of Abdominal Radiology. Diagnosis of hepatocellular carcinoma with gadoxetic acid-enhanced MRI: 2016 consensus recommendations of the Korean Society of Abdominal Radiology. Korean J Radiol. 2017; 18:427–443. PMID: 28458595.
6. Yoon JH, Park JW, Lee JM. Noninvasive diagnosis of hepatocellular carcinoma: elaboration on Korean Liver Cancer Study Group-National Cancer Center Korea practice guidelines compared with other guidelines and remaining issues. Korean J Radiol. 2016; 17:7–24. PMID: 26798212.
Article
7. Park YN. Update on precursor and early lesions of hepatocellular carcinomas. Arch Pathol Lab Med. 2011; 135:704–715. PMID: 21631263.
Article
8. Hennedige T, Yang ZJ, Ong CK, Venkatesh SK. Utility of non-contrast-enhanced CT for improved detection of arterial phase hyperenhancement in hepatocellular carcinoma. Abdom Imaging. 2014; 39:1247–1254. PMID: 24943135.
Article
9. Yu JS, Kim YH, Rofsky NM. Dynamic subtraction magnetic resonance imaging of cirrhotic liver: assessment of high SIlesions on nonenhanced T1-weighted images. J Comput Assist Tomogr. 2005; 29:51–58. PMID: 15665683.
10. An C, Park MS, Kim D, Kim YE, Chung WS, Rhee H, et al. 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. 2013; 23:924–930. PMID: 23138382.
11. Bashir MR, Castelli P, Davenport MS, Larson D, Marin D, Hussain HK, et al. Respiratory motion artifact affecting hepatic arterial phase MR imaging with gadoxetate disodium is more common in patients with a prior episode of arterial phase motion associated with gadoxetate disodium. Radiology. 2015; 274:141–148. PMID: 25162310.
Article
12. Davenport MS, Viglianti BL, Al-Hawary MM, Caoili EM, Kaza RK, Liu PS, et al. Comparison of acute transient dyspnea after intravenous administration of gadoxetate disodium and gadobenate dimeglumine: effect on arterial phase image quality. Radiology. 2013; 266:452–461. PMID: 23192781.
Article
13. Haradome H, Grazioli L, Tsunoo M, Tinti R, Frittoli B, Gambarini S, et al. Can MR fluoroscopic triggering technique and slow rate injection provide appropriate arterial phase images with reducing artifacts on gadoxetic acid-DTPA (Gd-EOB-DTPA)-enhanced hepatic MR imaging? J Magn Reson Imaging. 2010; 32:334–340. PMID: 20677259.
Article
14. Grazioli L, Bondioni MP, Haradome H, Motosugi U, Tinti R, Frittoli B, et al. Hepatocellular adenoma and focal nodular hyperplasia: value of gadoxetic acid-enhanced MR imaging in differential diagnosis. Radiology. 2012; 262:520–529. PMID: 22282184.
Article
15. Roux M, Pigneur F, Calderaro J, Baranes L, Chiaradia M, Tselikas L, et al. Differentiation of focal nodular hyperplasia from hepatocellular adenoma: role of the quantitative analysis of gadobenate dimeglumine-enhanced hepatobiliary phase MRI. J Magn Reson Imaging. 2015; 42:1249–1258. PMID: 25851028.
Article
16. Haimerl M, Wächtler M, Zeman F, Verloh N, Platzek I, Schreyer AG, et al. Quantitative evaluation of enhancement patterns in focal solid liver lesions with Gd-EOB-DTPA-enhanced MRI. PLoS One. 2014; 9:e100315. PMID: 24950259.
Article
17. Taouli B, Johnson RS, Hajdu CH, Oei MT, Merad M, Yee H, et al. Hepatocellular carcinoma: perfusion quantification with dynamic contrast-enhanced MRI. AJR Am J Roentgenol. 2013; 201:795–800. PMID: 24059368.
Article
18. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part II. Extracellular agents, hepatobiliary agents, and ancillary imaging features. Radiology. 2014; 273:30–50. PMID: 25247563.
Article
19. Coleman WB. Mechanisms of human hepatocarcinogenesis. Curr Mol Med. 2003; 3:573–588. PMID: 14527088.
Article
20. Hamer OW, Aguirre DA, Casola G, Lavine JE, Woenckhaus M, Sirlin CB. Fatty liver: imaging patterns and pitfalls. Radiographics. 2006; 26:1637–1653. PMID: 17102041.
Article
21. Seçil M, Obuz F, Altay C, Gencel O, Iğci E, Sağol O, et al. The role of dynamic subtraction MRI in detection of hepatocellular carcinoma. Diagn Interv Radiol. 2008; 14:200–204. PMID: 19061165.
22. Sugimoto K, Kim SR, Imoto S, Tohyama M, Kim SK, Matsuoka T, et al. Characteristics of hypovascular versus hypervascular well-differentiated hepatocellular carcinoma smaller than 2 cm - Focus on tumor size, markers and imaging detectability. Dig Dis. 2015; 33:721–727. PMID: 26488580.
Article
23. Lee YJ, Lee JM, Lee JS, Lee HY, Park BH, Kim YH, et al. Hepatocellular carcinoma: diagnostic performance of multidetector CT and MR imaging-a systematic review and meta-analysis. Radiology. 2015; 275:97–109. PMID: 25559230.
Article
24. Kim SH, Kim SH, Lee J, Kim MJ, Jeon YH, Park Y, et al. Gadoxetic acid-enhanced MRI versus triple-phase MDCT for the preoperative detection of hepatocellular carcinoma. AJR Am J Roentgenol. 2009; 192:1675–1681. PMID: 19457834.
Article
Full Text Links
  • KJR
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr