Prediction of Microvascular Invasion and Early Recurrence after Curative Resection of Hepatocellular Carcinoma with Enhanced CT Imaging_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

 ZHENGLi-rong ¹ , SHENJun-yi ² ,  CHENWei-xia ¹ , ZHAOYi-jun ³

1. Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China;
2. Department of Liver Surgery, West China Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China;
3. Department of Radiology, The Second Xiangya Hospital of Central South University, Changsha 410011, Hunan Province, China;

Corresponding author：

CHENWei-xia, Email: wxchen25@126.com

Keywords：

Hepatocellular carcinoma; CT enhanced imaging; Curative tumor resection; Microvascular invasion; Early recurrence; Risk factors

DOI：

10.7507/1007-9424.20160359

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To assess value of preoperative clinical data and enhanced CT imaging features in predic-tion of microvascular invasion (MVI) and early recurrence (recurrence in one year) after curative resection for hepatoce-llular carcinoma (HCC). Methods A retrospective analysis was conducted for 150 patients with HCC who underwent curative tumor resection in West China Hospital of Sichuan University from April 2014 to May 2015. The roles of preoperative CT characteristics and clinical data on MVI and early recurrence after curative tumor resection were evaluated by univariate and multivariate analyses. Results compared with HCC with no MVI and no early recurrence after curative resection, univariate analysis results showed that HCC with MVI and early recurrence had larger tumor size (P=0.002, P=0.005), a higher proportion of non-smooth tumor margin (P<0.001, P<0.001), and tumor multifocality (P=0.005, P=0.038), HCC with MVI had a higher proportion of incomplete tumor capsule (P=0.032), HCC with early recurrence had a higher proportion of incomplete and absence tumor capsules (P=0.038) and a faster washout on portal venous phase-the percentage attenuation ratio on the portal venous phase (P=0.049) and relative washout ratio on the portal venous phase (P=0.020) were higher. A multivariate logistic regression analysis results showed that non-smooth tumor margin (OR=7.075, P<0.001; OR=4.125, P<0.001) and tumor multifocality (OR=3.290, P=0.008; OR=2.354, P=0.047) were the independent predictors for MVI and early recurrence after curative tumor resection, HCC with early recurrence also had a faster washout on the portal venous phase (OR=1.023, P=0.017). Conclusion Non-smooth tumor margin and tumor multifocality are independent risk factors for MVI and early recurrence after curative tumor resection, and HCC with early recurrence has a faster washout on portal venous phase. Preoperative enhanced CT imaging could predict MVI and early recurrence after curative tumor resection and CT imaging findings are helpful to choose reasonable treatment and predict prognosis.

Citation： ZHENGLi-rong, SHENJun-yi, CHENWei-xia, ZHAOYi-jun. Prediction of Microvascular Invasion and Early Recurrence after Curative Resection of Hepatocellular Carcinoma with Enhanced CT Imaging. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2016, 23(11): 1400-1406. doi: 10.7507/1007-9424.20160359 Copy

1.	Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin, 2015, 65(2):87-108.
2.	Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2):115-132.
3.	Tsai TJ, Chau GY, Lui WY, et al. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery, 2000, 127(6):603-608.
4.	Lauwers GY, Terris B, Balis UJ, et al. Prognostic histologic indica-tors of curatively resected hepatocellular carcinomas:a multi-institu-tional analysis of 425 patients with definition of a histologic progno-stic index. Am J Surg Pathol, 2002, 26(1):25-34.
5.	Chou CT, Chen RC, Lee CW, et al. Prediction of microvascular invasion of hepatocellular carcinoma by preoperative CT imaging. Br J Radiol, 2012, 85(1014):778-783.
6.	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.
7.	Wu TH, Hatano E, Yamanaka K, et al. A non-smooth tumor margin on preoperative imaging predicts microvascular invasion of hepatocellular carcinoma. Surg Today, 2016, 46(11):1275-1281.
8.	Chou CT, Chen RC, Lin WC, et al. Prediction of microvascular inva-sion of hepatocellular carcinoma:preoperative CT and histopatho-logic correlation. AJR Am J Roentgenol, 2014, 203(3):W253-W259.
9.	Chandarana H, Robinson E, Hajdu CH, et al. Microvascular inva-sion in hepatocellular carcinoma:is it predictable with pretransplant MRI? AJR Am J Roentgenol, 2011, 196(5):1083-1089.
10.	An C, Kim DW, Park YN, et al. Single hepatocellular carcinoma:preoperative MR imaging to predict early recurrence after curative resection. Radiology, 2015, 276(2):433-443.
11.	Shimoda M, Tago K, Shiraki T, et al. Risk factors for early recurrence of single lesion hepatocellular carcinoma after curative resection. World J Surg, 2016, 40(10):2466-2471.
12.	Japan LCSGO. The general rules for the clinical and pathological study of primary liver cancer. Jpn J Surg, 1989, 19(1):98-129.
13.	Chandarana H, Lee VS, Hecht E, et al. Comparison of biexponential and monoexponential model of diffusion weighted imaging in evaluation of renal lesions:preliminary experience. Invest Radiol, 2011, 46(5):285-291.
14.	Liu YI, Shin LK, Jeffrey RB, et al. Quantitatively defining washout in hepatocellular carcinoma. AJR Am J Roentgenol, 2013, 200(1):84-89.
15.	Iwatsuki S, Dvorchik I, Marsh JW, et al. Liver transplantation for hepatocellular carcinoma:a proposal of a prognostic scoring system. J Am Coll Surg, 2000, 191(4):389-394.
16.	Nakashima Y, Nakashima O, Tanaka M, et al. Portal vein invasion and intrahepatic micrometastasis in small hepatocellular carcinoma by gross type. Hepatol Res, 2003, 26(2):142-147.
17.	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.
18.	Nagano Y, Shimada H, Takeda K, et al. Predictive factors of micro-vascular invasionin patients with hepatocellular carcinoma larger than 5 cm. World J Surg, 2008, 32(10):2218-2222.
19.	He J, Shi J, Fu X, et al. The clinicopathologic and prognostic signifi-cance of gross classification on solitary hepatocellular carcinoma after hepatectomy. Medicine (Baltimore), 2015, 94(32):e1331.
20.	伏旭, 何健, 史炯, 等. 肝细胞癌大体形态分型的临床意义. 中华消化外科杂志, 2015, 14(2):120-126.
21.	Kono M, Inoue T, Kudo M, et al. Radiofrequency ablation for hepa-tocellular carcinoma measuring 2 cm or smaller:results and risk factors for local recurrence. Dig Dis, 2014, 32(6):670-677.
22.	Zhu WJ, Huang CY, Li C, et al. Risk factors for early recurrence of HBV-related hepatocellular carcinoma meeting milan criteria after curative resection. Asian Pac J Cancer Prev, 2013, 14(12):7101-7106.
23.	Lu X, Zhao HT, Yang HY, et al. A prospective clinical study on early recurrence of hepatocellular carcinoma after hepatectomy. J Surg Oncol, 2009, 100(6):488-493.
24.	Kim BK, Han KH, Park YN, et al. Prediction of microvascular invasion before curative resection of hepatocellular carcinoma. J Surg Oncol, 2008, 97(3):246-252.
25.	Cheng ZJ, Yang PH, Qu SP, et al. Risk factors and management for early and late intrahepatic recurrence of solitary hepatocellular carcinoma after curative resection. HBP(Oxford), 2015, 17(5):422-427.
26.	Kim SJ, Lee KK, Kim DG. Tumor size predicts the biological behavior and influence of operative modalities in hepatocellular carcinoma. Hepatogastroenterology, 2010, 57(97):121-126.
27.	Kim H, Park MS, Choi JY, et al. Can microvessel invasion of hepa-tocellular carcinoma be predicted by pre-operative MRI? Eur Radio, 2009, 19(7):1744-1751.
28.	Miyata R, Tanimoto A, Wakabayashi G, et al. Accuracy of preoper-ative prediction of microinvasion of portal vein in hepatocellular carcinoma using superparamagnetic iron oxide-enhanced magnetic resonance imaging and computed tomography during hepatic angio-graphy. J Gastroenterol, 2006, 41(10):987-995.
29.	Nishie A, Yoshimitsu K, Asayama Y, et al. Radiologic detectability of minute portal venous invasion in hepatocellular carcinoma. AJR Am J Roentgenol, 2008, 190(1):81-87.
30.	Ng IO, Lai EC, Ng MM, et al. Tumor encapsulation in hepatocellular carcinoma:a pathologic study of 189 cases. Cancer, 1992, 70(1):45-49.
31.	Ishizaki M, Ashida K, Higashi T, et al. The formation of capsule and septum in human hepatocellular carcinoma. Virchows Arch, 2001, 438(6):574-580.
32.	Torimura T, Ueno T, Inuzuka S, et al. Mechanism of fibrous capsule formation surrounding hepatocellular carcinoma:immunohisto-chemical study. Arch Pathol Lab Med, 1991, 115(4):365-371.
33.	张雪辉, 孙其勤, 王钦习. 动态增强CT预测原发性肝癌微血管的侵犯. 临床放射学杂志, 2014, 33(5):730-733.
34.	Adachi E, Maeda T, Kajiyama K, et al. Factors correlated with portal venous invasion by hepatocellular carcinoma:univariate and multivariate analyses of 232 resected cases without preoperative treatments. Cancer, 1996, 77(10):2022-2031.
35.	Wang Y, Liao J, Qi W, et al. Predictive value of conventional ultra-sound and contrast-enhanced ultrasound in early recurrence of hepatocellular carcinoma after surgical resection. Ultrasound Med Biol, 2016, 42(5):1042-1048.
36.	Okamoto D, Yoshimitsu K, Nishie A, et al. Enhancement pattern analysis of hypervascular hepatocellular carcinoma on dynamic MR imaging with histopathological correlation:validity of portal phase imaging for predicting tumor grade. Eur J Radiol, 2012, 81(6):1116-1121.
37.	Nishie A, Yoshimitsu K, Okamoto D, et al. CT prediction of histo-logical grade of hypervascular hepatocellular carcinoma:utility of the portal phase. Jpn J Radiol, 2013, 31(2):89-98.
38.	Asayama Y, Yoshimitsu K, Nishihara Y, et al. Arterial blood supply of hepatocellular carcinoma and histologic grading:radiologic-pathologic correlation. AJR Am J Roentgenol, 2008, 190(1):W28-W34.
39.	Choi BI, Takayasu K, Han MC. Small hepatocellular carcinomas and associated nodularlesions of the liver:pathology, pathogenesis, and imaging findings. AJR Am J Roentgenol, 1993, 160(6):1177-1187.
40.	Matsui O, Kadoya M, Kameyama T, et al. Benign and malignant nodules in cirrhotic livers:distinction based on blood supply. Radiology, 1991, 178(2):493-497.
41.	Nakashima Y, Nakashima O, Hsia CC, et al. Vascularization of small lhepatocellular carcinomas:correlation with differentiation. Liver, 1999, 19(1):12-18.
42.	Jang HJ, Kim TK, Burns PN, et al. Enhancement patterns of hepa-tocellular carcinoma at contrast-enhanced US:comparison with histologic differentiation. Radiology, 2007, 244(3):898-906.
43.	Witjes CD, Willemssen FE, Verheij J, et al. Histological differentia-tion grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging, 2012, 36(3):641-647.
44.	Kim MJ, Leea M, Choia JY, et al. Imaging features of small hepato-cellular carcinomas with microvascular invasion on gadoxetic acid-enhanced MR imaging. Eur J Radiol, 2012, 81(10):2507-2512.
45.	Wu D, Tan M, Zhou M, et al. Liver computed tomographic perfu-sion in the assessment of microvascular invasion in patients with small hepatocellular carcinoma. Invest Radiol, 2015, 50(4):188-194.
46.	McHugh PP, Gilbert J, Vera S, et al. Alpha-fetoprotein and tumour size are associated with microvascular invasion in explanted livers of patients undergoing transplantation with hepatocellular carcinoma. HPB (Oxford), 2010, 12(1):56-61.
47.	Zhou YM, Yang JM, Li B, et al. Risk factors for early recurrence of small hepatocellular carcinoma after curative resection. Hepatobiliary Pancreat Dis Int, 2010, 9(1):33-37.

1. Torre LA, Bray F, Siegel RL, et al. Global cancer statistics, 2012. CA Cancer J Clin, 2015, 65(2):87-108.
2. Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2):115-132.
3. Tsai TJ, Chau GY, Lui WY, et al. Clinical significance of microscopic tumor venous invasion in patients with resectable hepatocellular carcinoma. Surgery, 2000, 127(6):603-608.
4. Lauwers GY, Terris B, Balis UJ, et al. Prognostic histologic indica-tors of curatively resected hepatocellular carcinomas:a multi-institu-tional analysis of 425 patients with definition of a histologic progno-stic index. Am J Surg Pathol, 2002, 26(1):25-34.
5. Chou CT, Chen RC, Lee CW, et al. Prediction of microvascular invasion of hepatocellular carcinoma by preoperative CT imaging. Br J Radiol, 2012, 85(1014):778-783.
6. 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.
7. Wu TH, Hatano E, Yamanaka K, et al. A non-smooth tumor margin on preoperative imaging predicts microvascular invasion of hepatocellular carcinoma. Surg Today, 2016, 46(11):1275-1281.
8. Chou CT, Chen RC, Lin WC, et al. Prediction of microvascular inva-sion of hepatocellular carcinoma:preoperative CT and histopatho-logic correlation. AJR Am J Roentgenol, 2014, 203(3):W253-W259.
9. Chandarana H, Robinson E, Hajdu CH, et al. Microvascular inva-sion in hepatocellular carcinoma:is it predictable with pretransplant MRI? AJR Am J Roentgenol, 2011, 196(5):1083-1089.
10. An C, Kim DW, Park YN, et al. Single hepatocellular carcinoma:preoperative MR imaging to predict early recurrence after curative resection. Radiology, 2015, 276(2):433-443.
11. Shimoda M, Tago K, Shiraki T, et al. Risk factors for early recurrence of single lesion hepatocellular carcinoma after curative resection. World J Surg, 2016, 40(10):2466-2471.
12. Japan LCSGO. The general rules for the clinical and pathological study of primary liver cancer. Jpn J Surg, 1989, 19(1):98-129.
13. Chandarana H, Lee VS, Hecht E, et al. Comparison of biexponential and monoexponential model of diffusion weighted imaging in evaluation of renal lesions:preliminary experience. Invest Radiol, 2011, 46(5):285-291.
14. Liu YI, Shin LK, Jeffrey RB, et al. Quantitatively defining washout in hepatocellular carcinoma. AJR Am J Roentgenol, 2013, 200(1):84-89.
15. Iwatsuki S, Dvorchik I, Marsh JW, et al. Liver transplantation for hepatocellular carcinoma:a proposal of a prognostic scoring system. J Am Coll Surg, 2000, 191(4):389-394.
16. Nakashima Y, Nakashima O, Tanaka M, et al. Portal vein invasion and intrahepatic micrometastasis in small hepatocellular carcinoma by gross type. Hepatol Res, 2003, 26(2):142-147.
17. 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.
18. Nagano Y, Shimada H, Takeda K, et al. Predictive factors of micro-vascular invasionin patients with hepatocellular carcinoma larger than 5 cm. World J Surg, 2008, 32(10):2218-2222.
19. He J, Shi J, Fu X, et al. The clinicopathologic and prognostic signifi-cance of gross classification on solitary hepatocellular carcinoma after hepatectomy. Medicine (Baltimore), 2015, 94(32):e1331.
20. 伏旭, 何健, 史炯, 等. 肝细胞癌大体形态分型的临床意义. 中华消化外科杂志, 2015, 14(2):120-126.
21. Kono M, Inoue T, Kudo M, et al. Radiofrequency ablation for hepa-tocellular carcinoma measuring 2 cm or smaller:results and risk factors for local recurrence. Dig Dis, 2014, 32(6):670-677.
22. Zhu WJ, Huang CY, Li C, et al. Risk factors for early recurrence of HBV-related hepatocellular carcinoma meeting milan criteria after curative resection. Asian Pac J Cancer Prev, 2013, 14(12):7101-7106.
23. Lu X, Zhao HT, Yang HY, et al. A prospective clinical study on early recurrence of hepatocellular carcinoma after hepatectomy. J Surg Oncol, 2009, 100(6):488-493.
24. Kim BK, Han KH, Park YN, et al. Prediction of microvascular invasion before curative resection of hepatocellular carcinoma. J Surg Oncol, 2008, 97(3):246-252.
25. Cheng ZJ, Yang PH, Qu SP, et al. Risk factors and management for early and late intrahepatic recurrence of solitary hepatocellular carcinoma after curative resection. HBP(Oxford), 2015, 17(5):422-427.
26. Kim SJ, Lee KK, Kim DG. Tumor size predicts the biological behavior and influence of operative modalities in hepatocellular carcinoma. Hepatogastroenterology, 2010, 57(97):121-126.
27. Kim H, Park MS, Choi JY, et al. Can microvessel invasion of hepa-tocellular carcinoma be predicted by pre-operative MRI? Eur Radio, 2009, 19(7):1744-1751.
28. Miyata R, Tanimoto A, Wakabayashi G, et al. Accuracy of preoper-ative prediction of microinvasion of portal vein in hepatocellular carcinoma using superparamagnetic iron oxide-enhanced magnetic resonance imaging and computed tomography during hepatic angio-graphy. J Gastroenterol, 2006, 41(10):987-995.
29. Nishie A, Yoshimitsu K, Asayama Y, et al. Radiologic detectability of minute portal venous invasion in hepatocellular carcinoma. AJR Am J Roentgenol, 2008, 190(1):81-87.
30. Ng IO, Lai EC, Ng MM, et al. Tumor encapsulation in hepatocellular carcinoma:a pathologic study of 189 cases. Cancer, 1992, 70(1):45-49.
31. Ishizaki M, Ashida K, Higashi T, et al. The formation of capsule and septum in human hepatocellular carcinoma. Virchows Arch, 2001, 438(6):574-580.
32. Torimura T, Ueno T, Inuzuka S, et al. Mechanism of fibrous capsule formation surrounding hepatocellular carcinoma:immunohisto-chemical study. Arch Pathol Lab Med, 1991, 115(4):365-371.
33. 张雪辉, 孙其勤, 王钦习. 动态增强CT预测原发性肝癌微血管的侵犯. 临床放射学杂志, 2014, 33(5):730-733.
34. Adachi E, Maeda T, Kajiyama K, et al. Factors correlated with portal venous invasion by hepatocellular carcinoma:univariate and multivariate analyses of 232 resected cases without preoperative treatments. Cancer, 1996, 77(10):2022-2031.
35. Wang Y, Liao J, Qi W, et al. Predictive value of conventional ultra-sound and contrast-enhanced ultrasound in early recurrence of hepatocellular carcinoma after surgical resection. Ultrasound Med Biol, 2016, 42(5):1042-1048.
36. Okamoto D, Yoshimitsu K, Nishie A, et al. Enhancement pattern analysis of hypervascular hepatocellular carcinoma on dynamic MR imaging with histopathological correlation:validity of portal phase imaging for predicting tumor grade. Eur J Radiol, 2012, 81(6):1116-1121.
37. Nishie A, Yoshimitsu K, Okamoto D, et al. CT prediction of histo-logical grade of hypervascular hepatocellular carcinoma:utility of the portal phase. Jpn J Radiol, 2013, 31(2):89-98.
38. Asayama Y, Yoshimitsu K, Nishihara Y, et al. Arterial blood supply of hepatocellular carcinoma and histologic grading:radiologic-pathologic correlation. AJR Am J Roentgenol, 2008, 190(1):W28-W34.
39. Choi BI, Takayasu K, Han MC. Small hepatocellular carcinomas and associated nodularlesions of the liver:pathology, pathogenesis, and imaging findings. AJR Am J Roentgenol, 1993, 160(6):1177-1187.
40. Matsui O, Kadoya M, Kameyama T, et al. Benign and malignant nodules in cirrhotic livers:distinction based on blood supply. Radiology, 1991, 178(2):493-497.
41. Nakashima Y, Nakashima O, Hsia CC, et al. Vascularization of small lhepatocellular carcinomas:correlation with differentiation. Liver, 1999, 19(1):12-18.
42. Jang HJ, Kim TK, Burns PN, et al. Enhancement patterns of hepa-tocellular carcinoma at contrast-enhanced US:comparison with histologic differentiation. Radiology, 2007, 244(3):898-906.
43. Witjes CD, Willemssen FE, Verheij J, et al. Histological differentia-tion grade and microvascular invasion of hepatocellular carcinoma predicted by dynamic contrast-enhanced MRI. J Magn Reson Imaging, 2012, 36(3):641-647.
44. Kim MJ, Leea M, Choia JY, et al. Imaging features of small hepato-cellular carcinomas with microvascular invasion on gadoxetic acid-enhanced MR imaging. Eur J Radiol, 2012, 81(10):2507-2512.
45. Wu D, Tan M, Zhou M, et al. Liver computed tomographic perfu-sion in the assessment of microvascular invasion in patients with small hepatocellular carcinoma. Invest Radiol, 2015, 50(4):188-194.
46. McHugh PP, Gilbert J, Vera S, et al. Alpha-fetoprotein and tumour size are associated with microvascular invasion in explanted livers of patients undergoing transplantation with hepatocellular carcinoma. HPB (Oxford), 2010, 12(1):56-61.
47. Zhou YM, Yang JM, Li B, et al. Risk factors for early recurrence of small hepatocellular carcinoma after curative resection. Hepatobiliary Pancreat Dis Int, 2010, 9(1):33-37.

Previous Article
Dubin-Jonhson综合征合并胆囊结石1例报道
Next Article
Current Status and Progress of Vagus Nerve-Preserving Radical Gastrectomy

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Prediction of Microvascular Invasion and Early Recurrence after Curative Resection of Hepatocellular Carcinoma with Enhanced CT Imaging

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content