Research progress of magnetic resonance imaging in evaluating microvascular invasion of hepatocellular carcinoma_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

DUAN Ting , HUANG Zixing ,  SONG Bin

Department of Radiology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P.R.China;

Corresponding author：

SONG Bin, Email: anicesong@vip.sina.com

Keywords：

hepatocellular carcinoma; microvascular invasion; magnetic resonance imaging

DOI：

10.7507/1007-9424.201706024

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of magnetic resonance imaging (MRI) in evaluating microvascular invasion (MVI) of hepatocellular carcinoma (HCC) in order to provide information and evidence for therapy of HCC. Methods Papers published from May 1950 to May 2017, were retrieved in PubMed, OVID, CNKI database using the keywords on hepatocellular carcinoma, microvascular invasion, and magnetic resonance imaging. Sixty-seven papers were retrieved in English literatures and 13 in Chinese literatures. Criteria of paper adoption: ① the imaging method was MRI; ② the assessment content was MVI of HCC; ③ the golden standard was postoperative pathologic diagnosis. fifty-four papers were finally analyzed and reviewed. Results Currently there were various ways to evaluating the MVI of HCC using MRI, including morphology, texture analysis, diffusion-weighted imaging, dynamic-enhanced MRI, fat assessment, hepatocellular function and comprehensive evaluation. Conclusions Various methods perform differently in evaluating MVI. The use of multiparametric MRI techniques offers the potential for comprehensive assessment of MVI of HCC.

Citation： DUAN Ting, HUANG Zixing, SONG Bin. Research progress of magnetic resonance imaging in evaluating microvascular invasion of hepatocellular carcinoma. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2017, 24(7): 880-884. doi: 10.7507/1007-9424.201706024 Copy

1.	Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin, 2015, 65(2): 87-108.
2.	Sumie S, Kuromatsu R, Okuda K, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol, 2008, 15(5): 1375-1382.
3.	黄金球, 彭民浩, 邹全庆, 等. 原发性肝癌切除术后早期复发高危因素分析. 中国实用外科杂志, 2009, 29(5): 418-420.
4.	刘臻玉, 曾海锋, 武丹, 等. 微血管浸润对小肝癌患者预后的影响. 广东医学, 2013, 34(12): 1862-1864.
5.	Lee EC, Kim SH, Park H, et al. Survival analysis after liver resection for hepatocellular carcinoma: A consecutive cohort of 1002 patients. J Gastroenterol Hepatol, 2017, 32(5): 1055-1063.
6.	Sumie S, Nakashima O, Okuda K, et al. The significance of classifying microvascular invasion in patients with hepatocellular carcinoma. Ann Surg Oncol, 2014, 21(3): 1002-1009.
7.	Chou CT, Chen RC, Lin WC, et al. Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. Am J Roentgenol, 2014, 203(3): W253-W259.
8.	Zhao H, Hua Y, Dai T, et al. Development and validation of a novel predictive scoring model for microvascular invasion in patients with hepatocellular carcinoma. Eur J Radiol, 2017, 88: 32-40.
9.	张志敏, 谢冬敏, 许映斌, 等. 超声造影在肝细胞癌病理预后因素分析中的应用. 中国医学创新, 2016, 13(17): 66-69.
10.	郑丽荣, 沈俊颐, 陈卫霞, 等. CT 增强扫描预测肝细胞癌微血管侵犯、根治性切除术后早期复发. 中国普外基础与临床杂志, 2016, 23 (11): 1400-1406.
11.	Cho ES, Choi JY. MRI features of hepatocellular carcinoma related to biologic behavior. Korean J Radiol, 2015, 16(3): 449-464.
12.	Pomfret EA, Washburn K, Wald C, et al. Report of a national conference on liver allocation in patients with hepatocellular carcinoma in the United States. Liver Transplant, 2010, 16(3): 262-278.
13.	Kim KA, Kim MJ, Jeon HM, et al. Prediction of microvascular invasion of hepatocellular carcinoma: Usefulness of peritumoral hypointensity seen on gadoxetate disodium-enhanced hepatobiliary phase images. J Magn Reson Imaging, 2012, 35(3): 629-634.
14.	Kudo M, Kitano M, Sakurai T, et al. General rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: the outstanding achievements of the liver cancer study group of Japan. Digest Dis, 2015, 33(6): 765-770.
15.	Eguchi S, Takatsuki M, Hidaka M, et al. Predictor for histological microvascular invasion of hepatocellular carcinoma: a lesson from 229 consecutive cases of curative liver resection. World J Surg, 2010, 34(5): 1034-1038.
16.	Chandarana H, Robinson E, Hajdu CH, et al. Microvascular invasion in hepatocellular carcinoma: is it predictable with pretransplant MRI? AJR Am J Roentgenol, 2011, 196(5): 1083-1089.
17.	Renzulli M, Brocchi S, Cucchetti A, et al. Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology, 2016, 279(2): 432-442.
18.	徐萍, 黄梦琪, 廖冰, 等. Gd-EOB-DTPA MRI 动态增强预测孤立性肝细胞癌微血管侵犯的单因素及多因素回归分析. 影像诊断与介入放射学, 2017, 26(1): 31-36.
19.	Efremidis SC, Hytiroglou P, Matsui O. Enhancement patterns and signal-intensity characteristics of small hepatocellular carcinoma in cirrhosis: pathologic basis and diagnostic challenges. Eur Radiol, 2007, 17(11): 2969-2983.
20.	Roncalli M, Park YN, Di Tommaso L. Histopathological classification of hepatocellular carcinoma. Dig Liver Dis, 2010, 42 Suppl 3: S228-S234.
21.	Park YN. Update on precursor and early lesions of hepatocellular carcinomas. Arch Pathol Lab Med, 2011, 135(6): 704-715.
22.	International Consensus Group for Hepatocellular NeoplasiaThe International Consensus Group for Hepatocellular Neoplasia. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology, 2009, 49(2): 658-664.
23.	Rosenkrantz AB, Pinnamaneni N, Kierans AS, et al. Hypovascular hepatic nodules at gadoxetic acid-enhanced MRI: whole-lesion hepatobiliary phase histogram metrics for prediction of progression to arterial-enhancing hepatocellular carcinoma. Abdom Radiol, 2016, 41(1): 63-70.
24.	Kato H, Kanematsu M, Zhang XJ, et al. Computer-aided diagnosis of hepatic fibrosis: Preliminary evaluation of MRI texture analysis using the finite difference method and an artificial neural network. AJR Am J Roentgenol, 2007, 189(1): 117-122.
25.	Mayerhoefer ME, Schima W, Trattnig S, et al. Texture-based classification of focal liver lesions on MRI at 3.0 Tesla: a feasibility study in cysts and hemangiomas. J Magn Reson Imaging, 2010, 32(2): 352-359.
26.	Zhou W, Zhang LJ, Wang KX, et al. Malignancy characterization of hepatocellular carcinomas based on texture analysis of contrast-enhanced MR images. J Magn Reson Imaging, 2017, 45(5): 1476-1484.
27.	Choi JY, Kim H, Sun M, et al. Histogram analysis of hepatobiliary phase MR imaging as a quantitative value for liver cirrhosis: preliminary observations. Yonsei Med J, 2014, 55(3): 651-659.
28.	Huang YQ, Liang HY, Yang ZX, et al. Value of MR histogram analyses for prediction of microvascular invasion of hepatocellular carcinoma. Medicine, 2016, 95(26): e4034.
29.	Maier SE, Sun YP, Mulkern RV. Diffusion imaging of brain tumors. Nmr Biomed, 2010, 23(7): 849-864.
30.	Xu PJ, Yan FH, Wang JH, et al. Added value of breathhold diffusion-weighted MRI in detection of small hepatocellular carcinoma lesions compared with dynamic contrast-enhanced MRI alone using receiver operating characteristic curve analysis. J Magn Reson Imaging, 2009, 29(2): 341-349.
31.	Park MJ, Kim YK, Lee MW, et al. Small Hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns. Radiology, 2012, 264(3): 761-770.
32.	Mori Y, Tamai H, Shingaki N, et al. Hypointense hepatocellular carcinomas on apparent diffusion coefficient mapping: Pathological features and metastatic recurrence after hepatectomy. Hepatol Res, 2016, 46(7): 634-641.
33.	Xu PJ, Zeng MS, Liu K, et al. Microvascular invasion in small hepatocellular carcinoma: Is it predictable with preoperative diffusion-weighted imaging? J Gastroen Hepatol, 2014, 29(2): 330-336.
34.	Okamura S, Sumie S, Tonan T, et al. Diffusion-weighted magnetic resonance imaging predicts malignant potential in small hepatocellular carcinoma. Digest Liver Dis, 2016, 48(8): 945-952.
35.	Suh YJ, Kim MJ, Choi JY, et al. Preoperative prediction of the microvascular invasion of hepatocellular carcinoma with diffusion-weighted imaging. Liver Transpl, 2012, 18(10): 1171-1178.
36.	晏耀文, 饶圣祥, 俞梦勇. 扩散加权成像在预测肝细胞肝癌微血管浸润的价值. 临床放射学杂志, 2016, 35(1): 93-95.
37.	Yang C, Wang HQ, Sheng RF, et al. Microvascular invasion in hepatocellular carcinoma: is it predictable with a new, preoperative application of diffusion-weighted imaging? Clin Imag, 2017, 41: 101-105.
38.	李迎春, 宋彬, 徐隽, 等. 3.0T 磁共振薄层动态增强序列评价肝细胞性肝癌的临床应用研究. 中国普外基础与临床杂志, 2008, 15 (7): 536-540.
39.	Ahn SY, Lee JM, Joo I, et al. Prediction of microvascular invasion of hepatocellular carcinoma using gadoxetic acid-enhanced MR and F-18-FDG PET/CT. Abdom Imaging, 2015, 40(4): 843-851.
40.	Matsui O, Kobayashi S, Sanada J, et al. Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging, 2011, 36(3): 264-272.
41.	Witjes CD, Willemssen FE, Verheij J, et al. Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging, 2012, 36(3): 641-647.
42.	Shirabe K, Kajiyama K, Abe T, et al. Predictors of microscopic portal vein invasion by hepatocellular carcinoma: Measurement of portal perfusion defect area ratio. J Gastroenterol Hepatol, 2009, 24(8): 1431-1436.
43.	Eguchi A, Nakashima O, Okudaira S, et al. Adenomatous hyperplasia in the vicinity of small hepatocellular carcinoma. Hepatology, 1992, 15(5): 843-848.
44.	Terada T, Nakanuma Y, Hoso M, et al. Fatty macroregenerative nodule in non-steatotic liver cirrhosis. A morphologic study. Virchows Archiv A Pathol Anat Histopathol, 1989, 415(2): 131-136.
45.	Kutami R, Nakashima Y, Nakashima O, et al. Pathomorphologic study on the mechanism of fatty change in small hepatocellular carcinoma of humans. J Hepatol, 2000, 33(2): 282-289.
46.	Min JH, Kim YK, Lim S, et al. 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(6): 1036-1043.
47.	Van Beers BE, Pastor CM, Hussain HK. Primovist, Eovist: what to expect? J Hepatol, 2012, 57(2): 421-429.
48.	Motosugi U, Ichikawa T, Sou H, et al. Distinguishing hypervascular pseudolesions of the liver from hypervascular hepatocellular carcinomas with gadoxetic acid-enhanced MR imaging. Radiology, 2010, 256(1): 151-158.
49.	Kim JY, Kim MJ, Kim KA, et al. Hyperintense HCC on hepatobiliary phase images of gadoxetic acid-enhanced MRI: Correlation with clinical and pathological features. Eur J Radiol, 2012, 81(12): 3877-3882.
50.	Tsuda N, Matsui O. Cirrhotic rat liver: reference to transporter activity and morphologic changes in bile canaliculi-gadoxetic acid-enhanced MR imaging. Radiology, 2010, 256(3): 767-773.
51.	Tsuboyama T, Onishi H, Kim T, et al. Hepatocellular carcinoma: hepatocyte-selective enhancement at gadoxetic acid-enhanced MR imaging-correlation with expression of sinusoidal and canalicular transporters and bile accumulation. Radiology, 2010, 255(3): 824-833.
52.	Ariizumi S, Kitagawa K, Kotera Y, 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(4): 575-585.
53.	Lei ZQ, Li J, Wu D, et al. Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the Milan criteria. JAMA Surg, 2016, 151(4): 356-363.
54.	Zhao WC, Fan LF, Yang N, et al. Preoperative predictors of microvascular invasion in multinodular hepatocellular carcinoma. Eur J Surg Oncol, 2013, 39(8): 858-864.

1. Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin, 2015, 65(2): 87-108.
2. Sumie S, Kuromatsu R, Okuda K, et al. Microvascular invasion in patients with hepatocellular carcinoma and its predictable clinicopathological factors. Ann Surg Oncol, 2008, 15(5): 1375-1382.
3. 黄金球, 彭民浩, 邹全庆, 等. 原发性肝癌切除术后早期复发高危因素分析. 中国实用外科杂志, 2009, 29(5): 418-420.
4. 刘臻玉, 曾海锋, 武丹, 等. 微血管浸润对小肝癌患者预后的影响. 广东医学, 2013, 34(12): 1862-1864.
5. Lee EC, Kim SH, Park H, et al. Survival analysis after liver resection for hepatocellular carcinoma: A consecutive cohort of 1002 patients. J Gastroenterol Hepatol, 2017, 32(5): 1055-1063.
6. Sumie S, Nakashima O, Okuda K, et al. The significance of classifying microvascular invasion in patients with hepatocellular carcinoma. Ann Surg Oncol, 2014, 21(3): 1002-1009.
7. Chou CT, Chen RC, Lin WC, et al. Prediction of microvascular invasion of hepatocellular carcinoma: preoperative CT and histopathologic correlation. Am J Roentgenol, 2014, 203(3): W253-W259.
8. Zhao H, Hua Y, Dai T, et al. Development and validation of a novel predictive scoring model for microvascular invasion in patients with hepatocellular carcinoma. Eur J Radiol, 2017, 88: 32-40.
9. 张志敏, 谢冬敏, 许映斌, 等. 超声造影在肝细胞癌病理预后因素分析中的应用. 中国医学创新, 2016, 13(17): 66-69.
10. 郑丽荣, 沈俊颐, 陈卫霞, 等. CT 增强扫描预测肝细胞癌微血管侵犯、根治性切除术后早期复发. 中国普外基础与临床杂志, 2016, 23 (11): 1400-1406.
11. Cho ES, Choi JY. MRI features of hepatocellular carcinoma related to biologic behavior. Korean J Radiol, 2015, 16(3): 449-464.
12. Pomfret EA, Washburn K, Wald C, et al. Report of a national conference on liver allocation in patients with hepatocellular carcinoma in the United States. Liver Transplant, 2010, 16(3): 262-278.
13. Kim KA, Kim MJ, Jeon HM, et al. Prediction of microvascular invasion of hepatocellular carcinoma: Usefulness of peritumoral hypointensity seen on gadoxetate disodium-enhanced hepatobiliary phase images. J Magn Reson Imaging, 2012, 35(3): 629-634.
14. Kudo M, Kitano M, Sakurai T, et al. General rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: the outstanding achievements of the liver cancer study group of Japan. Digest Dis, 2015, 33(6): 765-770.
15. Eguchi S, Takatsuki M, Hidaka M, et al. Predictor for histological microvascular invasion of hepatocellular carcinoma: a lesson from 229 consecutive cases of curative liver resection. World J Surg, 2010, 34(5): 1034-1038.
16. Chandarana H, Robinson E, Hajdu CH, et al. Microvascular invasion in hepatocellular carcinoma: is it predictable with pretransplant MRI? AJR Am J Roentgenol, 2011, 196(5): 1083-1089.
17. Renzulli M, Brocchi S, Cucchetti A, et al. Can current preoperative imaging be used to detect microvascular invasion of hepatocellular carcinoma? Radiology, 2016, 279(2): 432-442.
18. 徐萍, 黄梦琪, 廖冰, 等. Gd-EOB-DTPA MRI 动态增强预测孤立性肝细胞癌微血管侵犯的单因素及多因素回归分析. 影像诊断与介入放射学, 2017, 26(1): 31-36.
19. Efremidis SC, Hytiroglou P, Matsui O. Enhancement patterns and signal-intensity characteristics of small hepatocellular carcinoma in cirrhosis: pathologic basis and diagnostic challenges. Eur Radiol, 2007, 17(11): 2969-2983.
20. Roncalli M, Park YN, Di Tommaso L. Histopathological classification of hepatocellular carcinoma. Dig Liver Dis, 2010, 42 Suppl 3: S228-S234.
21. Park YN. Update on precursor and early lesions of hepatocellular carcinomas. Arch Pathol Lab Med, 2011, 135(6): 704-715.
22. International Consensus Group for Hepatocellular NeoplasiaThe International Consensus Group for Hepatocellular Neoplasia. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology, 2009, 49(2): 658-664.
23. Rosenkrantz AB, Pinnamaneni N, Kierans AS, et al. Hypovascular hepatic nodules at gadoxetic acid-enhanced MRI: whole-lesion hepatobiliary phase histogram metrics for prediction of progression to arterial-enhancing hepatocellular carcinoma. Abdom Radiol, 2016, 41(1): 63-70.
24. Kato H, Kanematsu M, Zhang XJ, et al. Computer-aided diagnosis of hepatic fibrosis: Preliminary evaluation of MRI texture analysis using the finite difference method and an artificial neural network. AJR Am J Roentgenol, 2007, 189(1): 117-122.
25. Mayerhoefer ME, Schima W, Trattnig S, et al. Texture-based classification of focal liver lesions on MRI at 3.0 Tesla: a feasibility study in cysts and hemangiomas. J Magn Reson Imaging, 2010, 32(2): 352-359.
26. Zhou W, Zhang LJ, Wang KX, et al. Malignancy characterization of hepatocellular carcinomas based on texture analysis of contrast-enhanced MR images. J Magn Reson Imaging, 2017, 45(5): 1476-1484.
27. Choi JY, Kim H, Sun M, et al. Histogram analysis of hepatobiliary phase MR imaging as a quantitative value for liver cirrhosis: preliminary observations. Yonsei Med J, 2014, 55(3): 651-659.
28. Huang YQ, Liang HY, Yang ZX, et al. Value of MR histogram analyses for prediction of microvascular invasion of hepatocellular carcinoma. Medicine, 2016, 95(26): e4034.
29. Maier SE, Sun YP, Mulkern RV. Diffusion imaging of brain tumors. Nmr Biomed, 2010, 23(7): 849-864.
30. Xu PJ, Yan FH, Wang JH, et al. Added value of breathhold diffusion-weighted MRI in detection of small hepatocellular carcinoma lesions compared with dynamic contrast-enhanced MRI alone using receiver operating characteristic curve analysis. J Magn Reson Imaging, 2009, 29(2): 341-349.
31. Park MJ, Kim YK, Lee MW, et al. Small Hepatocellular carcinomas: improved sensitivity by combining gadoxetic acid-enhanced and diffusion-weighted MR imaging patterns. Radiology, 2012, 264(3): 761-770.
32. Mori Y, Tamai H, Shingaki N, et al. Hypointense hepatocellular carcinomas on apparent diffusion coefficient mapping: Pathological features and metastatic recurrence after hepatectomy. Hepatol Res, 2016, 46(7): 634-641.
33. Xu PJ, Zeng MS, Liu K, et al. Microvascular invasion in small hepatocellular carcinoma: Is it predictable with preoperative diffusion-weighted imaging? J Gastroen Hepatol, 2014, 29(2): 330-336.
34. Okamura S, Sumie S, Tonan T, et al. Diffusion-weighted magnetic resonance imaging predicts malignant potential in small hepatocellular carcinoma. Digest Liver Dis, 2016, 48(8): 945-952.
35. Suh YJ, Kim MJ, Choi JY, et al. Preoperative prediction of the microvascular invasion of hepatocellular carcinoma with diffusion-weighted imaging. Liver Transpl, 2012, 18(10): 1171-1178.
36. 晏耀文, 饶圣祥, 俞梦勇. 扩散加权成像在预测肝细胞肝癌微血管浸润的价值. 临床放射学杂志, 2016, 35(1): 93-95.
37. Yang C, Wang HQ, Sheng RF, et al. Microvascular invasion in hepatocellular carcinoma: is it predictable with a new, preoperative application of diffusion-weighted imaging? Clin Imag, 2017, 41: 101-105.
38. 李迎春, 宋彬, 徐隽, 等. 3.0T 磁共振薄层动态增强序列评价肝细胞性肝癌的临床应用研究. 中国普外基础与临床杂志, 2008, 15 (7): 536-540.
39. Ahn SY, Lee JM, Joo I, et al. Prediction of microvascular invasion of hepatocellular carcinoma using gadoxetic acid-enhanced MR and F-18-FDG PET/CT. Abdom Imaging, 2015, 40(4): 843-851.
40. Matsui O, Kobayashi S, Sanada J, et al. Hepatocelluar nodules in liver cirrhosis: hemodynamic evaluation (angiography-assisted CT) with special reference to multi-step hepatocarcinogenesis. Abdom Imaging, 2011, 36(3): 264-272.
41. Witjes CD, Willemssen FE, Verheij J, et al. Histological differentiation grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging, 2012, 36(3): 641-647.
42. Shirabe K, Kajiyama K, Abe T, et al. Predictors of microscopic portal vein invasion by hepatocellular carcinoma: Measurement of portal perfusion defect area ratio. J Gastroenterol Hepatol, 2009, 24(8): 1431-1436.
43. Eguchi A, Nakashima O, Okudaira S, et al. Adenomatous hyperplasia in the vicinity of small hepatocellular carcinoma. Hepatology, 1992, 15(5): 843-848.
44. Terada T, Nakanuma Y, Hoso M, et al. Fatty macroregenerative nodule in non-steatotic liver cirrhosis. A morphologic study. Virchows Archiv A Pathol Anat Histopathol, 1989, 415(2): 131-136.
45. Kutami R, Nakashima Y, Nakashima O, et al. Pathomorphologic study on the mechanism of fatty change in small hepatocellular carcinoma of humans. J Hepatol, 2000, 33(2): 282-289.
46. Min JH, Kim YK, Lim S, et al. 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(6): 1036-1043.
47. Van Beers BE, Pastor CM, Hussain HK. Primovist, Eovist: what to expect? J Hepatol, 2012, 57(2): 421-429.
48. Motosugi U, Ichikawa T, Sou H, et al. Distinguishing hypervascular pseudolesions of the liver from hypervascular hepatocellular carcinomas with gadoxetic acid-enhanced MR imaging. Radiology, 2010, 256(1): 151-158.
49. Kim JY, Kim MJ, Kim KA, et al. Hyperintense HCC on hepatobiliary phase images of gadoxetic acid-enhanced MRI: Correlation with clinical and pathological features. Eur J Radiol, 2012, 81(12): 3877-3882.
50. Tsuda N, Matsui O. Cirrhotic rat liver: reference to transporter activity and morphologic changes in bile canaliculi-gadoxetic acid-enhanced MR imaging. Radiology, 2010, 256(3): 767-773.
51. Tsuboyama T, Onishi H, Kim T, et al. Hepatocellular carcinoma: hepatocyte-selective enhancement at gadoxetic acid-enhanced MR imaging-correlation with expression of sinusoidal and canalicular transporters and bile accumulation. Radiology, 2010, 255(3): 824-833.
52. Ariizumi S, Kitagawa K, Kotera Y, 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(4): 575-585.
53. Lei ZQ, Li J, Wu D, et al. Nomogram for preoperative estimation of microvascular invasion risk in hepatitis B virus-related hepatocellular carcinoma within the Milan criteria. JAMA Surg, 2016, 151(4): 356-363.
54. Zhao WC, Fan LF, Yang N, et al. Preoperative predictors of microvascular invasion in multinodular hepatocellular carcinoma. Eur J Surg Oncol, 2013, 39(8): 858-864.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of magnetic resonance imaging in evaluating microvascular invasion of hepatocellular carcinoma

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