J Liver Cancer.  2023 Mar;23(1):143-156. 10.17998/jlc.2023.02.16.

Radiologic features of hepatocellular carcinoma related to prognosis

Affiliations
  • 1Department of Radiology, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea
  • 2Department of Radiology, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
  • 3Research Institute of Radiological Science, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
  • 4Center for Clinical Imaging Data Science, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea

Abstract

The cross-sectional imaging findings play a crucial role in the diagnosis of hepatocellular carcinoma (HCC). Recent studies have shown that imaging findings of HCC are not only relevant for the diagnosis of HCC, but also for identifying genetic and pathologic characteristics and determining prognosis. Imaging findings such as rim arterial phase hyperenhancement, arterial phase peritumoral hyperenhancement, hepatobiliary phase peritumoral hypointensity, non-smooth tumor margin, low apparent diffusion coefficient, and the LR-M category of the Liver Imaging-Reporting and Data System have been reported to be associated with poor prognosis. In contrast, imaging findings such as enhancing capsule appearance, hepatobiliary phase hyperintensity, and fat in mass have been reported to be associated with a favorable prognosis. Most of these imaging findings were examined in retrospective, single-center studies that were not adequately validated. However, the imaging findings can be applied for deciding the treatment strategy for HCC, if their significance can be confirmed by a large multicenter study. In this literature, we would like to review imaging findings related to the prognosis of HCC as well as their associated clinicopathological characteristics.

Keyword

Carcinoma, hepatocellular; Magnetic resonance imaging; Multidetector computed tomography; Prognosis

Figure

  • Figure 1. Hepatocellular carcinoma with fatty change in a 60-year-old woman. Approximately 1.8 cm non-rim arterial phase hyperenhancing hepatic nodule (arrow) (A) remains iso to slightly hyperintense in the hepatic parenchyma without washout appearance in the portal venous phase (B). In dual gradient-echo T1-weighted images (C, D), the signal intensity of the tumor decreased in the opposed-phase (arrowhead) (D) compared to the in-phase (C), suggesting the presence of intralesional fat. On pathologic examination, the lesion was Edmondson-Steiner grade I-II, which showed fatty changes in 60% of the tumor area.

  • Figure 2. Hepatocellular carcinoma (HCC) with rim arterial phase hyperenhancement and non-smooth tumor margin in a 61-year-old man. In pre-contrast (A), arterial (B), portal venous (C), and hepatobiliary (D) phase images of gadoxetate-enhanced magnetic resonance imaging, a 1.8 cm hepatic nodule shows rim-like peripheral hyperenhancement in the arterial phase (arrow). Note the non-smooth margins of the tumor. On pathological examination, the lesion was a poorly differentiated HCC with microvascular invasion.

  • Figure 3. Hepatocellular carcinoma showing low apparent diffusion coefficient and LR-M features in a 68-year-old man. An approximately 3 cm hepatic mass showing irregular rim hyperenhancement (arrow) in the arterial phase (A). The lesion displays high signal intensity on diffusion-weighted imaging (b=800) (B) and low signal intensity in the apparent diffusion coefficient map (C), indicating diffusion restriction. Diffusion restriction is more pronounced in the periphery of the tumor, exhibiting a targetoid pattern (arrowheads in B, C). On pathological examination, the lesion showed positive expression of keratin 19 and microvascular invasion.

  • Figure 4. Hepatocellular carcinoma showing LR-M features and non-smooth tumor margin in a 57-year-old man. An approximately 6.5 cm hepatic mass shows rim hyperenhancement in the arterial phase (A), progressive enhancement in the transitional (B), and hepatobiliary phases (C). The mass had a targetoid appearance, as the signal intensities in the arterial and hepatobiliary phases exhibited a concentric layout. Note the arterial phase peritumoral hyperenhancement, hepatobiliary phase peritumoral hypointensity, and non-smooth tumor margins. On pathological examination of the percutaneous biopsy specimen, the lesion was poorly differentiated and positive for keratin 19.

  • Figure 5. Hepatocellular carcinoma (HCC) with arterial phase peritumoral hyperenhancement and hepatobiliary phase peritumoral hypointensity in a 61-year-old man. In the arterial phase (A) and subtraction image from the pre-contrast scan (B) of gadoxetic acid-enhanced magnetic resonance imaging, arterial phase peritumoral hyperenhancement is seen (arrow) along with intratumoral hyperenhancement. In the portal venous phase (C), peritumoral hyperenhancement faded to nearly isointense to the hepatic parenchyma. In the hepatobiliary phase (D), an irregular area of peritumoral hypointensity (arrowhead) is observed. On pathological examination, the lesion was an EdmondsonSteiner grade III HCC with microvascular invasion.

  • Figure 6. Hepatocellular carcinoma (HCC) with arterial phase peritumoral hyperenhancement, hepatobiliary phase peritumoral hypointensity, and non-smooth tumor margin in a 41-year-old woman. Arterial phase peritumoral hyperenhancement is seen (arrow) along with intratumoral hyperenhancement in the arterial phase (A) of the gadoxetic acid-enhanced magnetic resonance imaging. In the hepatobiliary phase (B), an irregular area of peritumoral hypointensity was observed (arrowhead). The margin of the tumor protrudes into the hepatic parenchyma and shows a non-smooth margin. On pathological examination, the lesion was multinodular confluent, macrotrabecular-massive HCC with microvascular invasion.

  • Figure 7. Hepatocellular carcinoma with enhancing capsular appearance and hepatobiliary phase hyperintensity in a 79-year-old man. An approximately 4 cm hepatic mass shows non-rim hyperenhancement (arrow) in the arterial phase (A) and washout appearance in the portal venous phase (B) of gadoxetic acid-enhanced magnetic resonance imaging. A smooth enhancing capsule (arrowheads) on the periphery of the lesion is seen in the portal venous (B) and transitional phases (C). The entire mass is hyperintense in the hepatobiliary phase (D). Pathological examination revealed complete capsule formation and nuclear expression of β-catenin, suggesting β-catenin pathway activation.


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Reference

References

1. Torbenson MS, Ng IOL, Park YN, Roncalli M, Sakamoto M. Hepatocellular carcinoma. In : . Digestive system tumours. 5th ed. Lyon: International Agency for Research on Cancer;2019. p. 229–239.
2. Reig M, Forner A, Rimola J, Ferrer-Fàbrega J, Burrel M, GarciaCriado Á, et al. BCLC strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol. 2022; 76:681–693.
Article
3. Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017; 67:93–99.
Article
4. Yau T, Tang VY, Yao TJ, Fan ST, Lo CM, Poon RT. Development of Hong Kong liver cancer staging system with treatment stratification for patients with hepatocellular carcinoma. Gastroenterology. 2014; 146:1691–1700.e3.
Article
5. Kitao A, Zen Y, Matsui O, Gabata T, Kobayashi S, Koda W, et al. Hepatocellular carcinoma: signal intensity at gadoxetic acid-enhanced MR Imaging--correlation with molecular transporters and histopathologic features. Radiology. 2010; 256:817–826.
Article
6. Korean Liver Cancer Association (KLCA); National Cancer Center (NCC). 2022 KLCA-NCC Korea practice guidelines for the management of hepatocellular carcinoma. J Liver Cancer. 2022; Dec. 9. . doi: 10.17998/jlc.2022.11.07. [Epub ahead of print].
7. Marrero JA, Kulik LM, Sirlin CB, Zhu AX, Finn RS, Abecassis MM et al. diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018; 68:723–750.
Article
8. European Association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018; 69:182–236.
9. Jeon Y, Kwon SM, Rhee H, Yoo JE, Chung T, Woo HG, et al. Molecular and radiopathologic spectrum between HCC and intrahepatic cholangiocarcinoma. Hepatology. 2023; 77:92–108.
Article
10. Rhee H, Cho ES, Nahm JH, Jang M, Chung YE, Baek SE, et al. Gadoxetic acid-enhanced MRI of macrotrabecular-massive hepatocellular carcinoma and its prognostic implications. J Hepatol. 2021; 74:109–121.
Article
11. Kang HJ, Kim H, Lee DH, Hur BY, Hwang YJ, Suh KS, et al. Gadoxetate-enhanced MRI features of proliferative hepatocellular carcinoma are prognostic after surgery. Radiology. 2021; 300:572–582.
Article
12. Rhee H, Kim H, Park YN. Clinico-radio-pathological and molecular features of hepatocellular carcinomas with keratin 19 expression. Liver Cancer. 2020; 9:663–681.
Article
13. American College of Radiology. LI-RADS® CT/MRI [Internet]. Reston (VA): American College of Radiology;2018. [cited 2022 Dec 26]. Available from: https://www.acr.org/Clinical-Resources/Reporting-and-Data-Systems/LI-RADS/LI-RADS-CT-MRI-v2018.
14. Jha RC, Mitchell DG, Weinreb JC, Santillan CS, Yeh BM, Francois R, et al. LI-RADS categorization of benign and likely benign findings in patients at risk of hepatocellular carcinoma: a pictorial atlas. AJR Am J Roentgenol. 2014; 203:W48–W69.
Article
15. Park HJ, Jang KM, Kang TW, Song KD, Kim SH, Kim YK, et al. Identification of imaging predictors discriminating different primary liver tumours in patients with chronic liver disease on gadoxetic acid-enhanced MRI: a classification tree analysis. Eur Radiol. 2016; 26:3102–3111.
Article
16. Kadoya M, Matsui O, Takashima T, Nonomura A. Hepatocellular carcinoma: correlation of MR imaging and histopathologic findings. Radiology. 1992; 183:819–825.
Article
17. Kutami R, Nakashima Y, Nakashima O, Shiota K, Kojiro M. Pathomorphologic study on the mechanism of fatty change in small hepatocellular carcinoma of humans. J Hepatol. 2000; 33:282–289.
Article
18. Shibahara J, Ando S, Sakamoto Y, Kokudo N, Fukayama M. Hepatocellular carcinoma with steatohepatitic features: a clinicopathological study of Japanese patients. Histopathology. 2014; 64:951–962.
Article
19. Qin J, Higashi T, Nakagawa S, Fujiwara N, Yamashita YI, Beppu T, et al. Steatohepatitic variant of hepatocellular carcinoma is associated with both alcoholic steatohepatitis and nonalcoholic steatohepatitis: a study of 2 cohorts with molecular insights. Am J Surg Pathol. 2020; 44:1406–1412.
Article
20. Aykutlu U, Argon A, Orman M, Ulukaya S, Zeytunlu M, Karasu Z, et al. Steatotic and steatohepatitic hepatocellular carcinomas: features in a series with predominantly viral etiology. Am J Surg Pathol. 2021; 45:1252–1263.
21. Min JH, Kim YK, Lim S, Jeong WK, Choi D, Lee WJ. Prediction of microvascular invasion of hepatocellular carcinomas with gadoxetic acid-enhanced MR imaging: impact of intra-tumoral fat detected on chemical-shift images. Eur J Radiol. 2015; 84:1036–1043.
Article
22. Salomao M, Remotti H, Vaughan R, Siegel AB, Lefkowitch JH, Moreira RK. The steatohepatitic variant of hepatocellular carcinoma and its association with underlying steatohepatitis. Hum Pathol. 2012; 43:737–746.
Article
23. Siripongsakun S, Lee JK, Raman SS, Tong MJ, Sayre J, Lu DS. MRI detection of intratumoral fat in hepatocellular carcinoma: potential biomarker for a more favorable prognosis. AJR Am J Roentgenol. 2012; 199:1018–1025.
Article
24. Chen J, Zhou J, Kuang S, Zhang Y, Xie S, He B, et al. Liver imaging reporting and data system category 5: MRI predictors of microvascular invasion and recurrence after hepatectomy for hepatocellular carcinoma. AJR Am J Roentgenol. 2019; 213:821–830.
Article
25. Hermida M, Preel A, Assenat E, Piron L, Cassinotto C, UrsicBedoya J, et al. Small steatotic HCC: a radiological variant associated with improved outcome after ablation. Hepatol Commun. 2020; 5:689–700.
Article
26. 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.
Article
27. Lee S, Kim SH, Lee JE, Sinn DH, Park CK. Preoperative gadoxetic acid-enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma. J Hepatol. 2017; 67:526–534.
Article
28. An C, Kim DW, Park YN, Chung YE, Rhee H, Kim MJ. Single hepatocellular carcinoma: preoperative MR imaging to predict early recurrence after curative resection. Radiology. 2015; 276:433–443.
Article
29. Kawamura Y, Ikeda K, Seko Y, Hosaka T, Kobayashi M, Saitoh S, et al. Heterogeneous type 4 enhancement of hepatocellular carcinoma on dynamic CT is associated with tumor recurrence after radiofrequency ablation. AJR Am J Roentgenol. 2011; 197:W665–W673.
Article
30. Rhee H, An C, Kim HY, Yoo JE, Park YN, Kim MJ. Hepatocellular carcinoma with irregular rim-like arterial phase hyperenhancement: more aggressive pathologic features. Liver Cancer. 2019; 8:24–40.
Article
31. Fang JH, Zhou HC, Zhang C, Shang LR, Zhang L, Xu J, et al. A novel vascular pattern promotes metastasis of hepatocellular carcinoma in an epithelial-mesenchymal transition-independent manner. Hepatology. 2015; 62:452–465.
Article
32. Renne SL, Woo HY, Allegra S, Rudini N, Yano H, Donadon M, et al. Vessels Encapsulating Tumor Clusters (VETC) is a powerful predictor of aggressive hepatocellular carcinoma. Hepatology. 2020; 71:183–195.
Article
33. Kitao A, Matsui O, Zhang Y, Ogi T, Nakada S, Sato Y, et al. Dynamic CT and gadoxetic acid-enhanced MRI characteristics of P53-mutated hepatocellular carcinoma. Radiology. 2023; 306:e220531.
Article
34. Hong SB, Choi SH, Kim SY, Shim JH, Lee SS, Byun JH, et al. MRI features for predicting microvascular invasion of hepatocellular carcinoma: a systematic review and meta-analysis. Liver Cancer. 2021; 10:94–106.
Article
35. Kierans AS, Leonardou P, Hayashi P, Brubaker LM, Elazzazi M, Shaikh F, et al. MRI findings of rapidly progressive hepatocellular carcinoma. Magn Reson Imaging. 2010; 28:790–796.
Article
36. An C, Park S, Chung YE, Kim DY, Kim SS, Kim MJ, et al. Curative resection of single primary hepatic malignancy: liver imaging reporting and data system category LR-M portends a worse prognosis. AJR Am J Roentgenol. 2017; 209:576–583.
Article
37. Kim BK, Kim KA, An C, Yoo EJ, Park JY, Kim DY, et al. Prognostic role of magnetic resonance imaging vs. computed tomography for hepatocellular carcinoma undergoing chemoembolization. Liver Int. 2015; 35:1722–1730.
Article
38. Fowler KJ, Burgoyne A, Fraum TJ, Hosseini M, Ichikawa S, Kim S, et al. Pathologic, molecular, and prognostic radiologic features of hepatocellular carcinoma. Radiographics. 2021; 41:1611–1631.
Article
39. Matsui O, Kobayashi S, Sanada J, Kouda W, Ryu Y, Kozaka K, et al. Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multistep hepatocarcinogenesis. Abdom Imaging. 2011; 36:264–272.
Article
40. Renzulli M, Brocchi S, Cucchetti A, Mazzotti F, Mosconi C, Sportoletti C, et al. Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology. 2016; 279:432–442.
Article
41. Nishie A, Yoshimitsu K, Asayama Y, Irie H, Tajima T, Hirakawa M, et al. Radiologic detectability of minute portal venous invasion in hepatocellular carcinoma. AJR Am J Roentgenol. 2008; 190:81–87.
Article
42. Kim H, Park MS, Choi JY, Park YN, Kim MJ, Kim KS, et al. Can microvessel invasion of hepatocellular carcinoma be predicted by pre-operative MRI? Eur Radiol. 2009; 19:1744–1751.
Article
43. Yang H, Han P, Huang M, Yue X, Wu L, Li X, et al. The role of gadoxetic acid-enhanced MRI features for predicting microvascular invasion in patients with hepatocellular carcinoma. Abdom Radiol (NY). 2022; 47:948–956.
Article
44. Wei H, Yang T, Chen J, Duan T, Jiang H, Song B. Prognostic implications of CT/MRI LI-RADS in hepatocellular carcinoma: state of the art and future directions. Liver Int. 2022; 42:2131–2144.
Article
45. Wei H, Jiang H, Liu X, Qin Y, Zheng T, Liu S, et al. Can LI-RADS imaging features at gadoxetic acid-enhanced MRI predict aggressive features on pathology of single hepatocellular carcinoma? Eur J Radiol. 2020; 132:109312.
Article
46. Zhang L, Kuang S, Chen J, Zhang Y, Zhao B, Peng H, et al. The role of preoperative dynamic contrast-enhanced 3.0-T MR imaging in predicting early recurrence in patients with early-stage hepatocellular carcinomas after curative resection. Front Oncol. 2019; 9:1336.
Article
47. Kitao A, Zen Y, Matsui O, Gabata T, Nakanuma Y. Hepatocarcinogenesis: multistep changes of drainage vessels at CT during arterial portography and hepatic arteriography--radiologic-pathologic correlation. Radiology. 2009; 252:605–614.
Article
48. Rhee H, Chung T, Yoo JE, Nahm JH, Woo HY, Choi GH, et al. Gross type of hepatocellular carcinoma reflects the tumor hypoxia, fibrosis, and stemness-related marker expression. Hepatol Int. 2020; 14:239–248.
Article
49. Ishizaki M, Ashida K, Higashi T, Nakatsukasa H, Kaneyoshi T, Fujiwara K, et al. The formation of capsule and septum in human hepatocellular carcinoma. Virchows Arch. 2001; 438:574–580.
Article
50. Iguchi T, Aishima S, Sanefuji K, Fujita N, Sugimachi K, Gion T, et al. Both fibrous capsule formation and extracapsular penetration are powerful predictors of poor survival in human hepatocellular carcinoma: a histological assessment of 365 patients in Japan. Ann Surg Oncol. 2009; 16:2539–2546.
Article
51. Ishigami K, Yoshimitsu K, Nishihara Y, Irie H, Asayama Y, Tajima T, et al. Hepatocellular carcinoma with a pseudocapsule on gadolinium-enhanced MR images: correlation with histopathologic findings. Radiology. 2009; 250:435–443.
Article
52. 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. 2017; 27:2610–2618.
Article
53. Wakasa K, Sakurai M, Kuroda C, Marukawa T, Monden M, Okamura J, et al. Effect of transcatheter arterial embolization on the boundary architecture of hepatocellular carcinoma. Cancer. 1990; 65:913–919.
Article
54. Wu TH, Yu MC, Chen TC, Lee CF, Chan KM, Wu TJ, et al. Encapsulation is a significant prognostic factor for better outcome in large hepatocellular carcinoma. J Surg Oncol. 2012; 105:85–90.
Article
55. Lai EC, Ng IO, Ng MM, Lok AS, Tam PC, Fan ST, et al. Longterm results of resection for large hepatocellular carcinoma: a multivariate analysis of clinicopathological features. Hepatology. 1990; 11:815–818.
Article
56. Witjes CD, Willemssen FE, Verheij J, van der Veer SJ, Hansen BE, Verhoef C, et al. Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging. 2012; 36:641–647.
Article
57. Bartolozzi C, Battaglia V, Bargellini I, Bozzi E, Campani D, Pollina LE, et al. Contrast-enhanced magnetic resonance imaging of 102 nodules in cirrhosis: correlation with histological findings on explanted livers. Abdom Imaging. 2013; 38:290–296.
Article
58. Kim JY, Kim MJ, Kim KA, Jeong HT, Park YN. Hyperintense HCC on hepatobiliary phase images of gadoxetic acid-enhanced MRI: correlation with clinical and pathological features. Eur J Radiol. 2012; 81:3877–3882.
Article
59. Yamashita T, Kitao A, Matsui O, Hayashi T, Nio K, Kondo M, et al. Gd-EOB-DTPA-enhanced magnetic resonance imaging and alpha-fetoprotein predict prognosis of early-stage hepatocellular carcinoma. Hepatology. 2014; 60:1674–1685.
Article
60. Kitao A, Matsui O, Yoneda N, Kozaka K, Kobayashi S, Koda W, et al. Gadoxetic acid-enhanced MR imaging for hepatocellular carcinoma: molecular and genetic background. Eur Radiol. 2020; 30:3438–3447.
Article
61. Ba-Ssalamah A, Antunes C, Feier D, Bastati N, Hodge JC, Stift J, et al. Morphologic and molecular features of hepatocellular adenoma with gadoxetic acid-enhanced MR imaging. Radiology. 2015; 277:104–113.
Article
62. 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.
Article
63. Kitao A, Matsui O, Yoneda N, Kozaka K, Kobayashi S, Koda W, et al. Hypervascular hepatocellular carcinoma: correlation between biologic features and signal intensity on gadoxetic acid-enhanced MR images. Radiology. 2012; 265:780–789.
Article
64. Yoneda N, Matsui O, Kitao A, Kita R, Kozaka K, Koda W, et al. Hypervascular hepatocellular carcinomas showing hyperintensity on hepatobiliary phase of gadoxetic acid-enhanced magnetic resonance imaging: a possible subtype with mature hepatocyte nature. Jpn J Radiol. 2013; 31:480–490.
Article
65. Choi JW, Lee JM, Kim SJ, Yoon JH, Baek JH, Han JK, et al. Hepatocellular carcinoma: imaging patterns on gadoxetic acid-enhanced MR images and their value as an imaging biomarker. Radiology. 2013; 267:776–786.
Article
66. Kim KA, Kim MJ, Jeon HM, Kim KS, Choi JS, Ahn SH, et al. Prediction of microvascular invasion of hepatocellular carcinoma: usefulness of peritumoral hypointensity seen on gadoxetate disodiumenhanced hepatobiliary phase images. J Magn Reson Imaging. 2012; 35:629–634.
Article
67. Lee S, Kim KW, Jeong WK, Jeong SY, Hwang JA, Choi JS, et al. Liver imaging reporting and data system category on magnetic resonance imaging predicts recurrence of hepatocellular carcinoma after liver transplantation within the milan criteria: a multicenter study. Ann Surg Oncol. 2021; 28:6782–6789.
Article
68. Wei H, Jiang H, Zheng T, Zhang Z, Yang C, Ye Z, et al. LI-RADS category 5 hepatocellular carcinoma: preoperative gadoxetic acidenhanced MRI for early recurrence risk stratification after curative resection. Eur Radiol. 2021; 31:2289–2302.
Article
69. Kang TW, Rhim H, Lee J, Song KD, Lee MW, Kim YS, et al. Magnetic resonance imaging with gadoxetic acid for local tumour progression after radiofrequency ablation in patients with hepatocellular carcinoma. Eur Radiol. 2016; 26:3437–3446.
Article
70. Kim AY, Sinn DH, Jeong WK, Kim YK, Kang TW, Ha SY, et al. Hepatobiliary MRI as novel selection criteria in liver transplantation for hepatocellular carcinoma. J Hepatol. 2018; 68:1144–1152.
Article
71. Ariizumi S, Kitagawa K, Kotera Y, Takahashi Y, Katagiri S, Kuwatsuru R, et al. 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. 2011; 18:575–585.
Article
72. Nakashima Y, Nakashima O, Tanaka M, Okuda K, Nakashima M, Kojiro M. Portal vein invasion and intrahepatic micrometastasis in small hepatocellular carcinoma by gross type. Hepatol Res. 2003; 26:142–147.
Article
73. Sumie S, Kuromatsu R, Okuda K, Ando E, Takata A, Fukushima N, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol. 2008; 15:1375–1382.
Article
74. Chou CT, Chen RC, Lin WC, Ko CJ, Chen CB, Chen YL. Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. AJR Am J Roentgenol. 2014; 203:W253–W259.
Article
75. Jiang H, Wei J, Fu F, Wei H, Qin Y, Duan T, et al. Predicting microvascular invasion in hepatocellular carcinoma: a dualinstitution study on gadoxetate disodium-enhanced MRI. Liver Int. 2022; 42:1158–1172.
Article
76. Chen J, Wu Z, Xia C, Jiang H, Liu X, Duan T, et al. Noninvasive prediction of HCC with progenitor phenotype based on gadoxetic acid-enhanced MRI. Eur Radiol. 2020; 30:1232–1242.
Article
77. Taouli B, Koh DM. Diffusion-weighted MR imaging of the liver. Radiology. 2010; 254:47–66.
Article
78. Deng J, Rhee TK, Sato KT, Salem R, Haines K, Paunesku T, et al. In vivo diffusion-weighted imaging of liver tumor necrosis in the VX2 rabbit model at 1.5 Tesla. Invest Radiol. 2006; 41:410–414.
Article
79. Nakanishi M, Chuma M, Hige S, Omatsu T, Yokoo H, Nakanishi K, et al. Relationship between diffusion-weighted magnetic resonance imaging and histological tumor grading of hepatocellular carcinoma. Ann Surg Oncol. 2012; 19:1302–1309.
Article
80. Nishie A, Tajima T, Asayama Y, Ishigami K, Kakihara D, Nakayama T, et al. Diagnostic performance of apparent diffusion coefficient for predicting histological grade of hepatocellular carcinoma. Eur J Radiol. 2011; 80:e29–e33.
Article
81. Heo SH, Jeong YY, Shin SS, Kim JW, Lim HS, Lee JH, et al. Apparent diffusion coefficient value of diffusion-weighted imaging for hepatocellular carcinoma: correlation with the histologic differentiation and the expression of vascular endothelial growth factor. Korean J Radiol. 2010; 11:295–303.
Article
82. Suh YJ, Kim MJ, Choi JY, Park MS, Kim KW. Preoperative prediction of the microvascular invasion of hepatocellular carcinoma with diffusion-weighted imaging. Liver Transpl. 2012; 18:1171–1178.
Article
83. Surov A, Pech M, Omari J, Fischbach F, Damm R, Fischbach K, et al. Diffusion-weighted imaging reflects tumor grading and microvascular invasion in hepatocellular carcinoma. Liver Cancer. 2021; 10:10–24.
Article
84. Xu P, Zeng M, Liu K, Shan Y, Xu C, Lin J. Microvascular invasion in small hepatocellular carcinoma: is it predictable with preoperative diffusion-weighted imaging? J Gastroenterol Hepatol. 2014; 29:330–336.
Article
85. Jeong HT, Kim MJ, Kim YE, Park YN, Choi GH, Choi JS. MRI features of hepatocellular carcinoma expressing progenitor cell markers. Liver Int. 2012; 32:430–440.
Article
86. Choi SY, Kim SH, Park CK, Min JH, Lee JE, Choi YH, et al. Imaging features of gadoxetic acid-enhanced and diffusion-weighted MR imaging for identifying cytokeratin 19-positive hepatocellular carcinoma: a retrospective observational study. Radiology. 2018; 286:897–908.
Article
87. Chen J, Xia C, Duan T, Cao L, Jiang H, Liu X, et al. Macrotrabecular-massive hepatocellular carcinoma: imaging identification and prediction based on gadoxetic acid-enhanced magnetic resonance imaging. Eur Radiol. 2021; 31:7696–7704.
Article
88. Hu XX, Yang ZX, Liang HY, Ding Y, Grimm R, Fu CX, et al. Wholetumor MRI histogram analyses of hepatocellular carcinoma: correlations with Ki-67 labeling index. J Magn Reson Imaging. 2017; 46:383–392.
Article
89. Huang Z, Xu X, Meng X, Hou Z, Liu F, Hua Q, et al. Correlations between ADC values and molecular markers of Ki-67 and HIF-1α in hepatocellular carcinoma. Eur J Radiol. 2015; 84:2464–2469.
Article
90. Lee S, Kim SH, Hwang JA, Lee JE, Ha SY. Pre-operative ADC predicts early recurrence of HCC after curative resection. Eur Radiol. 2019; 29:1003–1012.
Article
91. Sasaki M, Yamada K, Watanabe Y, Matsui M, Ida M, Fujiwara S, et al. Variability in absolute apparent diffusion coefficient values across different platforms may be substantial: a multivendor, multi-institutional comparison study. Radiology. 2008; 249:624–630.
Article
92. van der Pol CB, Lim CS, Sirlin CB, McGrath TA, Salameh JP, Bashir MR, et al. Accuracy of the liver imaging reporting and data system in computed tomography and magnetic resonance image analysis of hepatocellular carcinoma or overall malignancy-a systematic review. Gastroenterology. 2019; 156:976–986.
Article
93. Lee S, Kim SS, Roh YH, Choi JY, Park MS, Kim MJ. Diagnostic performance of CT/MRI liver imaging reporting and data system v2017 for hepatocellular carcinoma: a systematic review and meta-analysis. Liver Int. 2020; 40:1488–1497.
Article
94. Kim DH, Choi SH, Park SH, Kim KW, Byun JH, Kim SY, et al. Liver imaging reporting and data system category M: a systematic review and meta-analysis. Liver Int. 2020; 40:1477–1487.
Article
95. Lee S, Kim YY, Shin J, Hwang SH, Roh YH, Chung YE, et al. CT and MRI liver imaging reporting and data system version 2018 for hepatocellular carcinoma: a systematic review with meta-analysis. J Am Coll Radiol. 2020; 17:1199–1206.
Article
96. Shin J, Lee S, Kim SS, Chung YE, Choi JY, Park MS, et al. Characteristics and early recurrence of hepatocellular carcinomas categorized as LR-M: comparison with those categorized as LR-4 or 5. J Magn Reson Imaging. 2021; 54:1446–1454.
Article
97. Hu XX, Wang WT, Yang L, Yang ZX, Liang HY, Ding Y, et al. MR features based on LI-RADS identify cytokeratin 19 status of hepatocellular carcinomas. Eur J Radiol. 2019; 113:7–14.
Article
98. Choi SH, Lee SS, Park SH, Kim KM, Yu E, Park Y, et al. LI-RADS classification and prognosis of primary liver cancers at gadoxetic acid-enhanced MRI. Radiology. 2019; 290:388–397.
Article
99. Moon JY, Min JH, Kim YK, Cha D, Hwang JA, Ko SE, et al. Prognosis after curative resection of single hepatocellular carcinoma with a focus on LI-RADS targetoid appearance on preoperative gadoxetic acid-enhanced MRI. Korean J Radiol. 2021; 2211:1786–1796.
Article
100. Min JH, Lee MW, Park HS, Lee DH, Park HJ, Lim S, et al. Interobserver variability and diagnostic performance of gadoxetic acidenhanced MRI for predicting microvascular invasion in hepatocellular carcinoma. Radiology. 2020; 297:573–581.
Article
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