Korean J Radiol.  2017 Jun;18(3):427-443. 10.3348/kjr.2017.18.3.427.

Diagnosis of Hepatocellular Carcinoma with Gadoxetic Acid-Enhanced MRI: 2016 Consensus Recommendations of the Korean Society of Abdominal Radiology

Abstract

Diagnosis of hepatocellular carcinoma (HCC) with gadoxetic acid-enhanced liver magnetic resonance imaging (MRI) poses certain unique challenges beyond the scope of current guidelines. The regional heterogeneity of HCC in demographic characteristics, prevalence, surveillance, and socioeconomic status necessitates different treatment approaches, leading to variations in survival outcomes. Considering the medical practices in Korea, the Korean Society of Abdominal Radiology (KSAR) study group for liver diseases has developed expert consensus recommendations for diagnosis of HCC by gadoxetic acid-enhanced MRI with updated perspectives, using a modified Delphi method. During the 39th Scientific Assembly and Annual Meeting of KSAR (2016), consensus was reached on 12 of 16 statements. These recommendations might serve to ensure a more standardized diagnosis of HCC by gadoxetic acid-enhanced MRI.

Keyword

Liver; Hepatocellular carcinoma; Magnetic resonance imaging; Gadoxetic acid; Consensus; Guidelines

MeSH Terms

Carcinoma, Hepatocellular/*diagnosis/diagnostic imaging/pathology
Contrast Media/*chemistry
Gadolinium DTPA/*chemistry
Humans
Liver Neoplasms/*diagnosis/diagnostic imaging/pathology
Magnetic Resonance Imaging
Radiography, Abdominal
Republic of Korea
Sensitivity and Specificity
Societies, Scientific
Tomography, X-Ray Computed
Contrast Media
Gadolinium DTPA

Figure

  • Fig. 1 HCC in 56-year-old man.A. Pre-contrast T1-weighted image shows hyperintense nodule (arrow) in segment VI of liver. B. In arterial-phase of gadoxetic acid-enhanced magnetic resonance imaging, nodule (arrow) exhibits hyperintensity relative to surrounding liver parenchyma. C. Subtraction image obtained by subtracting pre-contrast-enhanced and arterial-phase T1-weighted images depicts true arterial enhancement of nodule (arrow). HCC = hepatocellular carcinoma

  • Fig. 2 HCC in 82-year-old man with chronic hepatitis C.A-C. In gadoxetic acid-enhanced magnetic resonance images, 5-cm mass (arrows) exhibits arterial hyperenhancement (A), slight hyperintensity in portal venous phase (PVP) (B), and hypointensity in transitional phase (C). Washout appearance of nodule in PVP only might lead to false-negative diagnosis of HCC based on enhancement pattern. D. It (arrow) shows hypointensity on HBP. HBP = hepatobiliary phase, HCC = hepatocellular carcinoma

  • Fig. 3 Sub-centimeter-sized HCC in 56-year-old man with chronic hepatitis B.Gadoxetic acid-enhanced MR image demonstrates 0.8-cm nodule (arrows) in right lobe of liver, adjacent to portal vein (A). Nodule exhibits arterial hyperenhancement, persistent hyperintensity during portal venous phase (B), and hypointensity during transitional (C), and hepatobiliary phases (D). Lesion (arrows) also exhibits other ancillary features, including intermediate hyperintensity on T2-weighted images (E), and restricted diffusion (F). Lesion was pathologically confirmed as HCC after hepatic resection. HCC = hepatocellular carcinoma

  • Fig. 4 HCC with hepatobiliary phase (HBP) capsule appearance in 59-year-old female hepatitis B virus carrier.A. 2.8-cm tumor (arrow) in right posterior hepatic section shows hyperenhancement in arterial phase. B-D. Tumor (arrows) becomes hypointense relative to liver from portal phase (B), to late portal phase (C), and to transitional phase (3 minutes) (D), and shows no conventional capsule appearance (peripheral rim of smooth hyperenhancement). Note that smooth hypointense rim (arrow) begins to appear in transitional phase. E. In HBP, smooth hypointense rim (arrow) clearly surrounds tumor. F. Surgical specimen revealed well-capsulated tumor (cut in half), which was confirmed as HCC with complete fibrous capsule on microscopic examination. HCC = hepatocellular carcinoma

  • Fig. 5 Moderately differentiated HCC in 60-year-old man.2.1-cm-sized small hepatic nodule shows (arrows) isointensity during unenhanced T1-weighted image (A), arterial-phase (B), on portal venous and 3 minutes transitional-phase image (not shown) (C), and 20 minutes hepatobiliary-phase images after administration of gadoxetic acid (D). This lesion (arrows) is seen as hyperintense on single-shot echo-planar diffusion-weighed imaging at b = 800 sec/mm2 (E) and T2-weighted image (F). Surgical specimen revealed 2-cm, single nodular type HCC with Edmondson grade II (G). HCC = hepatocellular carcinoma


Reference

1. Kudo M, Matsui O, Izumi N, Iijima H, Kadoya M, Imai Y, et al. JSH consensus-based clinical practice guidelines for the management of hepatocellular carcinoma: 2014 update by the Liver Cancer Study Group of Japan. Liver Cancer. 2014; 3:458–468. PMID: 26280007.
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. Bruix J, Sherman M. American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma: an update. Hepatology. 2011; 53:1020–1022. PMID: 21374666.
Article
4. Korean Liver Cancer Study Group (KLCSG). National Cancer Center, Korea (NCC). 2014 Korean Liver Cancer Study Group-National Cancer Center Korea practice guideline for the management of hepatocellular carcinoma. Korean J Radiol. 2015; 16:465–522. PMID: 25995680.
5. American College of Radiology. Liver Imaging Reporting and Data System (LI-RADS) version 2014. Accessed December 1, 2016. Available at: https://www.acr.org/Quality-Safety/Resources/LIRADS.
6. Sherman M. The radiological diagnosis of hepatocellular carcinoma. Am J Gastroenterol. 2010; 105:610–612. PMID: 20203642.
Article
7. El-Serag HB. Hepatocellular carcinoma. N Engl J Med. 2011; 365:1118–1127. PMID: 21992124.
Article
8. Graf D, Vallböhmer D, Knoefel WT, Kröpil P, Antoch G, Sagir A, et al. Multimodal treatment of hepatocellular carcinoma. Eur J Intern Med. 2014; 25:430–437. PMID: 24666568.
Article
9. Shukla A, Vadeyar H, Rela M, Shah S. Liver transplantation: East versus West. J Clin Exp Hepatol. 2013; 3:243–253. PMID: 25755506.
Article
10. de Villa V, Lo CM. Liver transplantation for hepatocellular carcinoma in Asia. Oncologist. 2007; 12:1321–1331. PMID: 18055852.
11. 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
12. Kagawa Y, Okada M, Kumano S, Katsube T, Imaoka I, Tanigawa N, et al. Optimal scanning protocol of arterial dominant phase for hypervascular hepatocellular carcinoma with gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced MR. J Magn Reson Imaging. 2011; 33:864–872. PMID: 21448951.
Article
13. Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: part I. Development, growth, and spread: key pathologic and imaging aspects. Radiology. 2014; 272:635–654. PMID: 25153274.
Article
14. Llovet JM. Updated treatment approach to hepatocellular carcinoma. J Gastroenterol. 2005; 40:225–235. PMID: 15830281.
Article
15. Mitchell DG, Bruix J, Sherman M, Sirlin CB. LI-RADS (Liver Imaging Reporting and Data System): summary, discussion, and consensus of the LI-RADS Management Working Group and future directions. Hepatology. 2015; 61:1056–1065. PMID: 25041904.
Article
16. 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.
17. Nino-Murcia M, Olcott EW, Jeffrey RB Jr, Lamm RL, Beaulieu CF, Jain KA. Focal liver lesions: pattern-based classification scheme for enhancement at arterial phase CT. Radiology. 2000; 215:746–751. PMID: 10831693.
Article
18. Ebara M, Fukuda H, Kojima Y, Morimoto N, Yoshikawa M, Sugiura N, et al. Small hepatocellular carcinoma: relationship of signal intensity to histopathologic findings and metal content of the tumor and surrounding hepatic parenchyma. Radiology. 1999; 210:81–88. PMID: 9885591.
Article
19. Kadoya M, Matsui O, Takashima T, Nonomura A. Hepatocellular carcinoma: correlation of MR imaging and histopathologic findings. Radiology. 1992; 183:819–825. PMID: 1316622.
Article
20. Lutz AM, Willmann JK, Goepfert K, Marincek B, Weishaupt D. Hepatocellular carcinoma in cirrhosis: enhancement patterns at dynamic gadolinium- and superparamagnetic iron oxide-enhanced T1-weighted MR imaging. Radiology. 2005; 237:520–528. PMID: 16192317.
Article
21. Reimer P, Rummeny EJ, Shamsi K, Balzer T, Daldrup HE, Tombach B, et al. Phase II clinical evaluation of Gd-EOB-DTPA: dose, safety aspects, and pulse sequence. Radiology. 1996; 199:177–183. PMID: 8633143.
Article
22. 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.
23. Winters SD, Jackson S, Armstrong GA, Birchall IW, Lee KH, Low G. Value of subtraction MRI in assessing treatment response following image-guided loco-regional therapies for hepatocellular carcinoma. Clin Radiol. 2012; 67:649–655. PMID: 22300821.
Article
24. Zhu RX, Seto WK, Lai CL, Yuen MF. Epidemiology of hepatocellular carcinoma in the Asia-Pacific region. Gut Liver. 2016; 10:332–339. PMID: 27114433.
Article
25. Rohrer M, Bauer H, Mintorovitch J, Requardt M, Weinmann HJ. Comparison of magnetic properties of MRI contrast media solutions at different magnetic field strengths. Invest Radiol. 2005; 40:715–724. PMID: 16230904.
Article
26. Hamm B, Staks T, Mühler A, Bollow M, Taupitz M, Frenzel T, et al. Phase I clinical evaluation of Gd-EOB-DTPA as a hepatobiliary MR contrast agent: safety, pharmacokinetics, and MR imaging. Radiology. 1995; 195:785–792. PMID: 7754011.
Article
27. Davenport MS, Caoili EM, Kaza RK, Hussain HK. Matched within-patient cohort study of transient arterial phase respiratory motion-related artifact in MR imaging of the liver: gadoxetate disodium versus gadobenate dimeglumine. Radiology. 2014; 272:123–131. PMID: 24617733.
Article
28. Kim SY, Park SH, Wu EH, Wang ZJ, Hope TA, Chang WC, et al. Transient respiratory motion artifact during arterial phase MRI with gadoxetate disodium: risk factor analyses. AJR Am J Roentgenol. 2015; 204:1220–1227. PMID: 26001231.
Article
29. Tamada T, Ito K, Yoshida K, Kanki A, Higaki A, Tanimoto D, et al. Comparison of three different injection methods for arterial phase of Gd-EOB-DTPA enhanced MR imaging of the liver. Eur J Radiol. 2011; 80:e284–e288. PMID: 21296514.
Article
30. Zech CJ, Vos B, Nordell A, Urich M, Blomqvist L, Breuer J, et al. Vascular enhancement in early dynamic liver MR imaging in an animal model: comparison of two injection regimen and two different doses Gd-EOB-DTPA (gadoxetic acid) with standard Gd-DTPA. Invest Radiol. 2009; 44:305–310. PMID: 19462484.
Article
31. 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
32. Nakamura S, Nakaura T, Kidoh M, Utsunomiya D, Doi Y, Harada K, et al. Timing of the hepatic arterial phase at Gd-EOB-DTPA-enhanced hepatic dynamic MRI: comparison of the test-injection and the fixed-time delay method. J Magn Reson Imaging. 2013; 38:548–554. PMID: 23744782.
Article
33. Fujinaga Y, Ohya A, Tokoro H, Yamada A, Ueda K, Ueda H, et al. Radial volumetric imaging breath-hold examination (VIBE) with k-space weighted image contrast (KWIC) for dynamic gadoxetic acid (Gd-EOB-DTPA)-enhanced MRI of the liver: advantages over Cartesian VIBE in the arterial phase. Eur Radiol. 2014; 24:1290–1299. PMID: 24633374.
Article
34. Pietryga JA, Burke LM, Marin D, Jaffe TA, Bashir MR. Respiratory motion artifact affecting hepatic arterial phase imaging with gadoxetate disodium: examination recovery with a multiple arterial phase acquisition. Radiology. 2014; 271:426–434. PMID: 24475864.
Article
35. Hope TA, Fowler KJ, Sirlin CB, Costa EA, Yee J, Yeh BM, et al. Hepatobiliary agents and their role in LI-RADS. Abdom Imaging. 2015; 40:613–625. PMID: 25287679.
Article
36. 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; 273:30–35. PMID: 25247563.
Article
37. Choi SH, Byun JH, Lim YS, Yu E, Lee SJ, Kim SY, et al. Diagnostic criteria for hepatocellular carcinoma ≤ 3 cm with hepatocyte-specific contrast-enhanced magnetic resonance imaging. J Hepatol. 2016; 64:1099–1107. PMID: 26820629.
38. Joo I, Lee JM, Lee DH, Jeon JH, Han JK, Choi BI. 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. 2015; 25:2859–2868. PMID: 25773941.
Article
39. Kudo M, Matsui O, Izumi N, Iijima H, Kadoya M, Imai Y. Liver Cancer Study Group of Japan. Surveillance and diagnostic algorithm for hepatocellular carcinoma proposed by the Liver Cancer Study Group of Japan: 2014 update. Oncology. 2014; 87(Suppl 1):7–21.
Article
40. Joo I, Lee JM. Recent advances in the imaging diagnosis of hepatocellular carcinoma: value of gadoxetic acid-enhanced MRI. Liver Cancer. 2016; 5:67–87. PMID: 26989660.
Article
41. 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
42. 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
43. Haradome H, Grazioli L, Tinti R, Morone M, Motosugi U, Sano K, et al. Additional value of gadoxetic acid-DTPA-enhanced hepatobiliary phase MR imaging in the diagnosis of early-stage hepatocellular carcinoma: comparison with dynamic triple-phase multidetector CT imaging. J Magn Reson Imaging. 2011; 34:69–78. PMID: 21598343.
Article
44. Lee DH, Lee JM, Baek JH, Shin CI, Han JK, Choi BI. Diagnostic performance of gadoxetic acid-enhanced liver MR imaging in the detection of HCCs and allocation of transplant recipients on the basis of the Milan criteria and UNOS guidelines: correlation with histopathologic findings. Radiology. 2015; 274:149–160. PMID: 25203131.
Article
45. Channual S, Tan N, Siripongsakun S, Lassman C, Lu DS, Raman SS. Gadoxetate disodium-enhanced MRI to differentiate dysplastic nodules and grade of hepatocellular carcinoma: correlation with histopathology. AJR Am J Roentgenol. 2015; 205:546–553. PMID: 26295640.
Article
46. Jeong WK, Kim YK, Song KD, Choi D, Lim HK. The MR imaging diagnosis of liver diseases using gadoxetic acid: emphasis on hepatobiliary phase. Clin Mol Hepatol. 2013; 19:360–366. PMID: 24459639.
Article
47. Joo I, Lee JM, Lee DH, Ahn SJ, Lee ES, Han JK. 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. 2017; 45:731–740. PMID: 27474328.
Article
48. Park VY, Choi JY, Chung YE, Kim H, Park MS, Lim JS, et al. Dynamic enhancement pattern of HCC smaller than 3 cm in diameter on gadoxetic acid-enhanced MRI: comparison with multiphasic MDCT. Liver Int. 2014; 34:1593–1602. PMID: 24673802.
49. Shah A, Tang A, Santillan C, Sirlin C. Cirrhotic liver: what's that nodule? The LI-RADS approach. J Magn Reson Imaging. 2016; 43:281–294. PMID: 25996905.
Article
50. Doo KW, Lee CH, Choi JW, Lee J, Kim KA, Park CM. “Pseudo washout” sign in high-flow hepatic hemangioma on gadoxetic acid contrast-enhanced MRI mimicking hypervascular tumor. AJR Am J Roentgenol. 2009; 193:W490–W496. PMID: 19933623.
Article
51. Péporté AR, Sommer WH, Nikolaou K, Reiser MF, Zech CJ. Imaging features of intrahepatic cholangiocarcinoma in Gd-EOB-DTPA-enhanced MRI. Eur J Radiol. 2013; 82:e101–e106. PMID: 23159401.
Article
52. Kang Y, Lee JM, Kim SH, Han JK, Choi BI. Intrahepatic mass-forming cholangiocarcinoma: enhancement patterns on gadoxetic acid-enhanced MR images. Radiology. 2012; 264:751–760. PMID: 22798225.
Article
53. Nam SJ, Yu JS, Cho ES, Kim JH, Chung JJ. High-flow haemangiomas versus hypervascular hepatocellular carcinoma showing “pseudo-washout” on gadoxetic acid-enhanced hepatic MRI: value of diffusion-weighted imaging in the differential diagnosis of small lesions. Clin Radiol. 2017; 72:247–254. PMID: 27789027.
Article
54. Outwater EK, Ito K, Siegelman E, Martin CE, Bhatia M, Mitchell DG. Rapidly enhancing hepatic hemangiomas at MRI: distinction from malignancies with T2-weighted images. J Magn Reson Imaging. 1997; 7:1033–1039. PMID: 9400846.
Article
55. Takahashi K, Obeid J, Burmeister CS, Bruno DA, Kazimi MM, Yoshida A, et al. Intrahepatic cholangiocarcinoma in the liver explant after liver transplantation: histological differentiation and prognosis. Ann Transplant. 2016; 21:208–215. PMID: 27068242.
Article
56. Kim JH, Won HJ, Shin YM, Kim KA, Kim PN. Radiofrequency ablation for the treatment of primary intrahepatic cholangiocarcinoma. AJR Am J Roentgenol. 2011; 196:W205–W209. PMID: 21257864.
Article
57. Roskams T. Anatomic pathology of hepatocellular carcinoma: impact on prognosis and response to therapy. Clin Liver Dis. 2011; 15:245–259. vii–x. PMID: 21689611.
Article
58. Park MJ, Kim YS, Lee WJ, Lim HK, Rhim H, Lee J. Outcomes of follow-up CT for small (5-10-mm) arterially enhancing nodules in the liver and risk factors for developing hepatocellular carcinoma in a surveillance population. Eur Radiol. 2010; 20:2397–2404. PMID: 20559837.
Article
59. Forner A, Vilana R, Ayuso C, Bianchi L, Solé M, Ayuso JR, et al. Diagnosis of hepatic nodules 20 mm or smaller in cirrhosis: prospective validation of the noninvasive diagnostic criteria for hepatocellular carcinoma. Hepatology. 2008; 47:97–104. PMID: 18069697.
Article
60. Hwang SH, Yu JS, Kim KW, Kim JH, Chung JJ. Small hypervascular enhancing lesions on arterial phase images of multiphase dynamic computed tomography in cirrhotic liver: fate and implications. J Comput Assist Tomogr. 2008; 32:39–45. PMID: 18303286.
61. Holland AE, Hecht EM, Hahn WY, Kim DC, Babb JS, Lee VS, et al. Importance of small (< or = 20-mm) enhancing lesions seen only during the hepatic arterial phase at MR imaging of the cirrhotic liver: evaluation and comparison with whole explanted liver. Radiology. 2005; 237:938–944. PMID: 16306035.
62. Byrnes V, Shi H, Kiryu S, Rofsky NM, Afdhal NH. The clinical outcome of small (< 20 mm) arterially enhancing nodules on MRI in the cirrhotic liver. Am J Gastroenterol. 2007; 102:1654–1659. PMID: 17521396.
63. Yu MH, Kim JH, Yoon JH, Kim HC, Chung JW, Han JK, et al. Small (≤ 1-cm) hepatocellular carcinoma: diagnostic performance and imaging features at gadoxetic acid-enhanced MR imaging. Radiology. 2014; 271:748–760. PMID: 24588677.
64. Lee MW, Kim YJ, Park HS, Yu NC, Jung SI, Ko SY, et al. Targeted sonography for small hepatocellular carcinoma discovered by CT or MRI: factors affecting sonographic detection. AJR Am J Roentgenol. 2010; 194:W396–W400. PMID: 20410384.
Article
65. Kim PN, Choi D, Rhim H, Rha SE, Hong HP, Lee J, et al. Planning ultrasound for percutaneous radiofrequency ablation to treat small (≤ 3 cm) hepatocellular carcinomas detected on computed tomography or magnetic resonance imaging: a multicenter prospective study to assess factors affecting ultrasound visibility. J Vasc Interv Radiol. 2012; 23:627–634. PMID: 22387030.
Article
66. 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
67. Sano K, Ichikawa T, Motosugi U, Sou H, Muhi AM, Matsuda M, et al. Imaging study of early hepatocellular carcinoma: usefulness of gadoxetic acid-enhanced MR imaging. Radiology. 2011; 261:834–844. PMID: 21998047.
Article
68. Chen L, Zhang L, Bao J, Zhang J, Li C, Xia Y, et al. Comparison of MRI with liver-specific contrast agents and multidetector row CT for the detection of hepatocellular carcinoma: a meta-analysis of 15 direct comparative studies. Gut. 2013; 62:1520–1521. PMID: 23929696.
Article
69. Kierans AS, Kang SK, Rosenkrantz AB. The diagnostic performance of dynamic contrast-enhanced MR imaging for detection of small hepatocellular carcinoma measuring up to 2 cm: a meta-analysis. Radiology. 2016; 278:82–94. PMID: 26098460.
Article
70. Song KD, Kim SH, Lim HK, Jung SH, Sohn I, Kim HS. Subcentimeter hypervascular nodule with typical imaging findings of hepatocellular carcinoma in patients with history of hepatocellular carcinoma: natural course on serial gadoxetic acid-enhanced MRI and diffusion-weighted imaging. Eur Radiol. 2015; 25:2789–2796. PMID: 25735515.
Article
71. Jang KM, Kim SH, Kim YK, Choi D. Imaging features of subcentimeter hypointense nodules on gadoxetic acid-enhanced hepatobiliary phase MR imaging that progress to hypervascular hepatocellular carcinoma in patients with chronic liver disease. Acta Radiol. 2015; 56:526–535. PMID: 24838304.
Article
72. Livraghi T, Meloni F, Di Stasi M, Rolle E, Solbiati L, Tinelli C, et al. Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: is resection still the treatment of choice? Hepatology. 2008; 47:82–89. PMID: 18008357.
Article
73. Arii S, Yamaoka Y, Futagawa S, Inoue K, Kobayashi K, Kojiro M, et al. The Liver Cancer Study Group of Japan. Results of surgical and nonsurgical treatment for small-sized hepatocellular carcinomas: a retrospective and nationwide survey in Japan. Hepatology. 2000; 32:1224–1229. PMID: 11093728.
Article
74. Takayama T, Makuuchi M, Hirohashi S, Sakamoto M, Yamamoto J, Shimada K, et al. Early hepatocellular carcinoma as an entity with a high rate of surgical cure. Hepatology. 1998; 28:1241–1246. PMID: 9794907.
Article
75. Lu DS, Yu NC, Raman SS, Limanond P, Lassman C, Murray K, et al. Radiofrequency ablation of hepatocellular carcinoma: treatment success as defined by histologic examination of the explanted liver. Radiology. 2005; 234:954–960. PMID: 15681691.
Article
76. Kang TW, Rhim H. Recent advances in tumor ablation for hepatocellular carcinoma. Liver Cancer. 2015; 4:176–187. PMID: 26674766.
Article
77. Park MJ, Kim YK, Lee MW, Lee WJ, Kim YS, Kim SH, et al. Small hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns. Radiology. 2012; 264:761–770. PMID: 22843769.
Article
78. Lee MH, Kim SH, Park MJ, Park CK, Rhim H. 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. 2011; 197:W868–W875. PMID: 22021534.
Article
79. Kim JE, Kim SH, Lee SJ, Rhim H. 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. 2011; 196:W758–W765. PMID: 21606265.
Article
80. Park MJ, Kim YK, Lee MH, Lee JH. Validation of diagnostic criteria using gadoxetic acid-enhanced and diffusion-weighted MR imaging for small hepatocellular carcinoma (<= 2.0 cm) in patients with hepatitis-induced liver cirrhosis. Acta Radiol. 2013; 54:127–136. PMID: 23148300.
81. Shindoh J, Andreou A, Aloia TA, Zimmitti G, Lauwers GY, Laurent A, et al. Microvascular invasion does not predict long-term survival in hepatocellular carcinoma up to 2 cm: reappraisal of the staging system for solitary tumors. Ann Surg Oncol. 2013; 20:1223–1229. PMID: 23179993.
82. Hwang S, Lee YJ, Kim KH, Ahn CS, Moon DB, Ha TY, et al. The impact of tumor size on long-term survival outcomes after resection of solitary hepatocellular carcinoma: single-institution experience with 2558 patients. J Gastrointest Surg. 2015; 19:1281–1290. PMID: 25956724.
Article
83. Sangiovanni A, Manini MA, Iavarone M, Romeo R, Forzenigo LV, Fraquelli M, et al. The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis. Gut. 2010; 59:638–644. PMID: 19951909.
Article
84. Khalili K, Kim TK, Jang HJ, Haider MA, Khan L, Guindi M, et al. Optimization of imaging diagnosis of 1–2 cm hepatocellular carcinoma: an analysis of diagnostic performance and resource utilization. J Hepatol. 2011; 54:723–728. PMID: 21156219.
85. Wu LM, Xu JR, Gu HY, Hua J, Chen J, Zhu J, et al. Is liver-specific gadoxetic acid-enhanced magnetic resonance imaging a reliable tool for detection of hepatocellular carcinoma in patients with chronic liver disease? Dig Dis Sci. 2013; 58:3313–3325. PMID: 23884757.
Article
86. Kitao A, Matsui O, Yoneda N, Kozaka K, Shinmura R, Koda W, et al. The uptake transporter OATP8 expression decreases during multistep hepatocarcinogenesis: correlation with gadoxetic acid enhanced MR imaging. Eur Radiol. 2011; 21:2056–2066. PMID: 21626360.
Article
87. Choi JY, Lee HC, Yim JH, Shim JH, Lim YS, Shin YM, et al. Focal nodular hyperplasia or focal nodular hyperplasia-like lesions of the liver: a special emphasis on diagnosis. J Gastroenterol Hepatol. 2011; 26:1004–1009. PMID: 21251063.
Article
88. Kogita S, Imai Y, Okada M, Kim T, Onishi H, Takamura M, et al. Gd-EOB-DTPA-enhanced magnetic resonance images of hepatocellular carcinoma: correlation with histological grading and portal blood flow. Eur Radiol. 2010; 20:2405–2413. PMID: 20490505.
Article
89. Yoon JH, Lee JM, Yang HK, Lee KB, Jang JJ, Han JK, et al. Non-hypervascular hypointense nodules ≥ 1 cm on the hepatobiliary phase of gadoxetic acid-enhanced magnetic resonance imaging in cirrhotic livers. Dig Dis. 2014; 32:678–689. PMID: 25376284.
90. Golfieri R, Grazioli L, Orlando E, Dormi A, Lucidi V, Corcioni B, et al. Which is the best MRI marker of malignancy for atypical cirrhotic nodules: hypointensity in hepatobiliary phase alone or combined with other features? Classification after Gd-EOB-DTPA administration. J Magn Reson Imaging. 2012; 36:648–657. PMID: 22592930.
Article
91. Akai H, Matsuda I, Kiryu S, Tajima T, Takao H, Watanabe Y, et al. Fate of hypointense lesions on Gd-EOB-DTPA-enhanced magnetic resonance imaging. Eur J Radiol. 2012; 81:2973–2977. PMID: 22280873.
Article
92. Motosugi U. Hypovascular hypointense nodules on hepatocyte phase gadoxetic acid-enhanced MR images: too early or too progressed to determine hypervascularity. Radiology. 2013; 267:317–318.
Article
93. Ichikawa S, Ichikawa T, Motosugi U, Sano K, Morisaka H, Enomoto N, et al. Presence of a hypovascular hepatic nodule showing hypointensity on hepatocyte-phase image is a risk factor for hypervascular hepatocellular carcinoma. J Magn Reson Imaging. 2014; 39:293–297. PMID: 23633285.
Article
94. Kim YK, Lee WJ, Park MJ, Kim SH, Rhim H, Choi D. Hypovascular hypointense nodules on hepatobiliary phase gadoxetic acid-enhanced MR images in patients with cirrhosis: potential of DW imaging in predicting progression to hypervascular HCC. Radiology. 2012; 265:104–114. PMID: 22891358.
Article
95. Yamamoto A, Ito K, Tamada T, Higaki A, Kanki A, Sato T, et al. Newly developed hypervascular hepatocellular carcinoma during follow-up periods in patients with chronic liver disease: observation in serial gadoxetic acid-enhanced MRI. AJR Am J Roentgenol. 2013; 200:1254–1260. PMID: 23701061.
Article
96. Lee DH, Lee JM, Lee JY, Kim SH, Kim JH, Yoon JH, et al. Non-hypervascular hepatobiliary phase hypointense nodules on gadoxetic acid-enhanced MRI: risk of HCC recurrence after radiofrequency ablation. J Hepatol. 2015; 62:1122–1130. PMID: 25529623.
Article
97. Toyoda H, Kumada T, Tada T, Sone Y, Maeda A, Kaneoka Y. Non-hypervascular hypointense nodules on Gd-EOB-DTPA-enhanced MRI as a predictor of outcomes for early-stage HCC. Hepatol Int. 2015; 9:84–92. PMID: 25788383.
Article
98. Merkle EM, Zech CJ, Bartolozzi C, Bashir MR, Ba-Ssalamah A, Huppertz A, et al. Consensus report from the 7th international forum for liver magnetic resonance imaging. Eur Radiol. 2016; 26:674–682. PMID: 26070500.
Article
99. Motosugi U, Bannas P, Sano K, Reeder SB. Hepatobiliary MR contrast agents in hypovascular hepatocellular carcinoma. J Magn Reson Imaging. 2015; 41:251–265. PMID: 25104398.
Article
100. Choi BI, Lee JM, Kim TK, Dioguardi Burgio M, Vilgrain V. Diagnosing borderline hepatic nodules in hepatocarcinogenesis: imaging performance. AJR Am J Roentgenol. 2015; 205:10–21. PMID: 26102378.
Article
101. Golfieri R, Renzulli M, Lucidi V, Corcioni B, Trevisani F, Bolondi L. 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. 2011; 21:1233–1242. PMID: 21293864.
102. Hwang J, Kim YK, Jeong WK, Choi D, Rhim H, Lee WJ. Nonhypervascular hypointense nodules at gadoxetic acid-enhanced MR imaging in chronic liver disease: diffusion-weighted imaging for characterization. Radiology. 2015; 276:137–146. PMID: 25734551.
Article
103. Xu PJ, Yan FH, Wang JH, Shan Y, Ji Y, Chen CZ. Contribution of diffusion-weighted magnetic resonance imaging in the characterization of hepatocellular carcinomas and dysplastic nodules in cirrhotic liver. J Comput Assist Tomogr. 2010; 34:506–512. PMID: 20657216.
Article
104. Hyodo T, Murakami T, Imai Y, Okada M, Hori M, Kagawa Y, et al. Hypovascular nodules in patients with chronic liver disease: risk factors for development of hypervascular hepatocellular carcinoma. Radiology. 2013; 266:480–490. PMID: 23362095.
Article
105. Takechi M, Tsuda T, Yoshioka S, Murata S, Tanaka H, Hirooka M, et al. Risk of hypervascularization in small hypovascular hepatic nodules showing hypointense in the hepatobiliary phase of gadoxetic acid-enhanced MRI in patients with chronic liver disease. Jpn J Radiol. 2012; 30:743–751. PMID: 23001373.
Article
106. Takayama Y, Nishie A, Nakayama T, Asayama Y, Ishigami K, Kakihara D, et al. Hypovascular hepatic nodule showing hypointensity in the hepatobiliary phase of gadoxetic acid-enhanced MRI in patients with chronic liver disease: prediction of malignant transformation. Eur J Radiol. 2012; 81:3072–3078. PMID: 22673776.
Article
107. Di Pietropaolo M, Briani C, Federici GF, Marignani M, Begini P, Delle Fave G, et al. Comparison of diffusion-weighted imaging and gadoxetic acid-enhanced MR images in the evaluation of hepatocellular carcinoma and hypovascular hepatocellular nodules. Clin Imaging. 2015; 39:468–475. PMID: 25748089.
Article
108. Midorikawa Y, Takayama T, Nara S, Hashimoto T, Omichi K, Ebisawa K, et al. No need of immediate treatment for hypovascular tumors associated with hepatocellular carcinoma. World J Surg. 2016; 40:2460–2465. PMID: 27142625.
Article
109. Matsuda M, Ichikawa T, Amemiya H, Maki A, Watanabe M, Kawaida H, et al. Preoperative gadoxetic acid-enhanced MRI and simultaneous treatment of early hepatocellular carcinoma prolonged recurrence-free survival of progressed hepatocellular carcinoma patients after hepatic resection. HPB Surg. 2014; 2014:641685. PMID: 24701029.
Article
110. Midorikawa Y, Takayama T, Shimada K, Nakayama H, Higaki T, Moriguchi M, et al. Marginal survival benefit in the treatment of early hepatocellular carcinoma. J Hepatol. 2013; 58:306–311. PMID: 23063418.
Article
111. An C, Rhee H, Han K, Choi JY, Park YN, Park MS, et al. 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. 2016; 10. 21. [Epup]. DOI: 10.1007/s00330-016-4634-6.
Article
112. Galea N, Cantisani V, Taouli B. Liver lesion detection and characterization: role of diffusion-weighted imaging. J Magn Reson Imaging. 2013; 37:1260–1276. PMID: 23712841.
Article
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