Skip to main content
Top
Published in: Hepatology International 6/2020

01-12-2020 | Hepatocellular Carcinoma | Original Article

A standardized pathological proposal for evaluating microvascular invasion of hepatocellular carcinoma: a multicenter study by LCPGC

Authors: Xia Sheng, Yuan Ji, Guo-Ping Ren, Chang-Li Lu, Jing-Ping Yun, Li-Hong Chen, Bin Meng, Li-Juan Qu, Guang-Jie Duan, Qing Sun, Xin-Qing Ye, Shan-Shan Li, Jing Yang, Bing Liao, Zhan-Bo Wang, Jian-Hua Zhou, Yu Sun, Xue-Shan Qiu, Lei Wang, Zeng-Shan Li, Jun Chen, Chun-Yan Xia, Song He, Chuan-Ying Li, En-Wei Xu, Jing-Shu Geng, Chao Pan, Dong Kuang, Rong Qin, Hong-Wei Guan, Zhan-Dong Wang, Li-Xing Li, Xi Zhang, Han Wang, Qian Zhao, Bo Wei, Wu-Jian Zhang, Shao-Ping Ling, Xiang Du, Wen-Ming Cong, for the Liver Cancer Pathology Group of China (LCPGC)

Published in: Hepatology International | Issue 6/2020

Login to get access

Abstract

Background and aims

Microvascular invasion (MVI) is a key pathological factor that severely affects the postoperative prognosis of patients with hepatocellular carcinoma (HCC). However, no MVI classification schemes based on standardized gross sampling protocols of HCC are available at present.

Methods

119 HCC specimens were sampled at multiple sites (3-, 7-, and 13 points) for the optimum MVI detection rate. 16,144 resected HCCs were graded as M0, M1 or M2 by adopting three-tiered MVI grading (MVI-TTG) scheme based on the seven-point sampling protocol (SPSP). Survival analyses were performed on 2573 patients to explore the advantages of MVI-TTG.

Results

The MVI detection rate determined by SPSP was significantly higher than that determined by the 3-point sampling method (34.5% vs. 47.1%, p = 0.048), but was similar to that determined by the 13-point sampling method (47.1% vs. 51.3%, p = 0.517). Among 16,144 resected HCCs, the proportions of M0, M1 and M2 specimens according to SPSP were 53.4%, 26.2% and 20.4%, respectively. Postoperative survival analysis in 2573 HCC patients showed that the 3-year recurrence rates in M0, M1 and M2 MVI groups were 62.5%, 71.6% and 86.1%, respectively (p < 0.001), and the corresponding 3-year overall survival (OS) rates were 94.1%, 87.5% and 67.0%, respectively (p < 0.001). M1 grade was associated with early recurrence, while M2 grade was associated with both early and late recurrence. MVI-TTG had a larger area under the curve and net benefit rate than the two-tiered MVI grading scheme for predicting time to recurrence and OS.

Conclusions

SPSP is a practical method to balance the efficacy of sampling numbers and MVI detection rates. MVI-TTG based on SPSP is a better prognostic predictor than the two-tiered MVI scheme. The combined use of SPSP and MVI-TTG is recommended for the routine pathological diagnosis of HCC.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRefPubMed Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424.CrossRefPubMed
2.
go back to reference Zhou M, Wang H, Zeng X, Yin P, Zhu J, Chen W, et al. Mortality, morbidity, and risk factors in China and its provinces, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet (London, England). 2019;394:1145–1158.CrossRef Zhou M, Wang H, Zeng X, Yin P, Zhu J, Chen W, et al. Mortality, morbidity, and risk factors in China and its provinces, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet (London, England). 2019;394:1145–1158.CrossRef
3.
go back to reference Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–132.PubMedCrossRef Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–132.PubMedCrossRef
4.
go back to reference Zheng R, Qu C, Zhang S, Zeng H, Sun K, Gu X, et al. Liver cancer incidence and mortality in China: Temporal trends and projections to 2030. Chin J Cancer Res. 2018;30:571–579.PubMedPubMedCentralCrossRef Zheng R, Qu C, Zhang S, Zeng H, Sun K, Gu X, et al. Liver cancer incidence and mortality in China: Temporal trends and projections to 2030. Chin J Cancer Res. 2018;30:571–579.PubMedPubMedCentralCrossRef
5.
go back to reference Islami F, Miller KD, Siegel RL, Fedewa SA, Ward EM, Jemal A. Disparities in liver cancer occurrence in the United States by race/ethnicity and state. CA Cancer J Clin. 2017;67:273–289.PubMedCrossRef Islami F, Miller KD, Siegel RL, Fedewa SA, Ward EM, Jemal A. Disparities in liver cancer occurrence in the United States by race/ethnicity and state. CA Cancer J Clin. 2017;67:273–289.PubMedCrossRef
7.
go back to reference Chan AWH, Zhong J, Berhane S, Toyoda H, Cucchetti A, Shi K, et al. Development of pre and post-operative models to predict early recurrence of hepatocellular carcinoma after surgical resection. J Hepatol. 2018;69:1284–1293.PubMedCrossRef Chan AWH, Zhong J, Berhane S, Toyoda H, Cucchetti A, Shi K, et al. Development of pre and post-operative models to predict early recurrence of hepatocellular carcinoma after surgical resection. J Hepatol. 2018;69:1284–1293.PubMedCrossRef
8.
go back to reference Njei B, Rotman Y, Ditah I, Lim JK. Emerging trends in hepatocellular carcinoma incidence and mortality. Hepatology (Baltimore, MD). 2015;61:191–199.CrossRef Njei B, Rotman Y, Ditah I, Lim JK. Emerging trends in hepatocellular carcinoma incidence and mortality. Hepatology (Baltimore, MD). 2015;61:191–199.CrossRef
9.
10.
go back to reference Wang H, Qian YW, Wu MC, Cong WM. Liver resection is justified in patients with BCLC intermediate stage hepatocellular carcinoma without microvascular invasion. J. Gastrointest. Surg. 2020;24(12):2737–47. Wang H, Qian YW, Wu MC, Cong WM. Liver resection is justified in patients with BCLC intermediate stage hepatocellular carcinoma without microvascular invasion. J. Gastrointest. Surg. 2020;24(12):2737–47.
11.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
12.
go back to reference Imai K, Yamashita YI, Yusa T, Nakao Y, Itoyama R, Nakagawa S, et al. Microvascular invasion in small-sized hepatocellular carcinoma: significance for outcomes following hepatectomy and radiofrequency ablation. Anticancer Res. 2018;38(2):1053–1060.PubMed Imai K, Yamashita YI, Yusa T, Nakao Y, Itoyama R, Nakagawa S, et al. Microvascular invasion in small-sized hepatocellular carcinoma: significance for outcomes following hepatectomy and radiofrequency ablation. Anticancer Res. 2018;38(2):1053–1060.PubMed
13.
go back to reference Xiao H, Chen ZB, Jin HL, Li B, Xu LX, Guo Y, et al. Treatment selection of recurrent hepatocellular carcinoma with microvascular invasion at the initial hepatectomy. Am J Transl Res. 2019;11:1864–1875.PubMedPubMedCentral Xiao H, Chen ZB, Jin HL, Li B, Xu LX, Guo Y, et al. Treatment selection of recurrent hepatocellular carcinoma with microvascular invasion at the initial hepatectomy. Am J Transl Res. 2019;11:1864–1875.PubMedPubMedCentral
14.
go back to reference Hu HT, Wang Z, Kuang M, Wang W. Need for normalization: the non-standard reference standard for microvascular invasion diagnosis in hepatocellular carcinoma. World J Surg Oncol. 2018;16:50.PubMedPubMedCentralCrossRef Hu HT, Wang Z, Kuang M, Wang W. Need for normalization: the non-standard reference standard for microvascular invasion diagnosis in hepatocellular carcinoma. World J Surg Oncol. 2018;16:50.PubMedPubMedCentralCrossRef
15.
go back to reference Ratziu V, Bugianesi E, Dixon J, Fassio E, Ekstedt M, Charlotte F, et al. Histological progression of non-alcoholic fatty liver disease: a critical reassessment based on liver sampling variability. Aliment Pharmacol Ther. 2007;26:821–830.PubMedCrossRef Ratziu V, Bugianesi E, Dixon J, Fassio E, Ekstedt M, Charlotte F, et al. Histological progression of non-alcoholic fatty liver disease: a critical reassessment based on liver sampling variability. Aliment Pharmacol Ther. 2007;26:821–830.PubMedCrossRef
16.
go back to reference Gill US, Pallett LJ, Kennedy PTF, Maini MK. Liver sampling: a vital window into HBV pathogenesis on the path to functional cure. Gut. 2018;67:767–775.PubMed Gill US, Pallett LJ, Kennedy PTF, Maini MK. Liver sampling: a vital window into HBV pathogenesis on the path to functional cure. Gut. 2018;67:767–775.PubMed
17.
go back to reference Pons E, Braun LM, Hunink MG, Kors JA. Natural language processing in radiology: a systematic review. Radiology. 2016;279:329–343.PubMedCrossRef Pons E, Braun LM, Hunink MG, Kors JA. Natural language processing in radiology: a systematic review. Radiology. 2016;279:329–343.PubMedCrossRef
18.
go back to reference Murff HJ, FitzHenry F, Matheny ME, Gentry N, Kotter KL, Crimin K, et al. Automated identification of postoperative complications within an electronic medical record using natural language processing. JAMA. 2011;306:848–855.PubMed Murff HJ, FitzHenry F, Matheny ME, Gentry N, Kotter KL, Crimin K, et al. Automated identification of postoperative complications within an electronic medical record using natural language processing. JAMA. 2011;306:848–855.PubMed
20.
go back to reference Yim W, Yetisgen M, Harris WP, Kwan SW. Natural language processing in oncology: a review. JAMA Oncol. 2016;2:797–804.PubMedCrossRef Yim W, Yetisgen M, Harris WP, Kwan SW. Natural language processing in oncology: a review. JAMA Oncol. 2016;2:797–804.PubMedCrossRef
21.
go back to reference Torbenson MS. Liver. In. Westra WH, Phelps TH, Hruban RH, Isacson C. Surgical Pathology Dissection. An Illustrated Guide. 2nd Ed, Springer-Verlag New York Inc, 2003;76–81. Torbenson MS. Liver. In. Westra WH, Phelps TH, Hruban RH, Isacson C. Surgical Pathology Dissection. An Illustrated Guide. 2nd Ed, Springer-Verlag New York Inc, 2003;76–81.
22.
go back to reference Cong WM, Bu H, Chen J, Dong H, Zhu YY, Feng LH, et al. Practice guidelines for the pathological diagnosis of primary liver cancer: 2015 update. World J Gastroenterol. 2016;22:9279–9287.PubMedPubMedCentralCrossRef Cong WM, Bu H, Chen J, Dong H, Zhu YY, Feng LH, et al. Practice guidelines for the pathological diagnosis of primary liver cancer: 2015 update. World J Gastroenterol. 2016;22:9279–9287.PubMedPubMedCentralCrossRef
24.
go back to reference Zhou XD, Tang ZY, Ma ZC, Fan J, Wu ZQ, Qin LX, et al. Twenty-year survivors after resection for hepatocellular carcinoma-analysis of 53 cases. J Cancer Res Clin Oncol. 2009;135:1067–1072.PubMedCrossRef Zhou XD, Tang ZY, Ma ZC, Fan J, Wu ZQ, Qin LX, et al. Twenty-year survivors after resection for hepatocellular carcinoma-analysis of 53 cases. J Cancer Res Clin Oncol. 2009;135:1067–1072.PubMedCrossRef
25.
go back to reference Lim KC, Chow PK, Allen JC, Chia GS, Lim M, Cheow PC, et al. Microvascular invasion is a better predictor of tumor recurrence and overall survival following surgical resection for hepatocellular carcinoma compared to the Milan criteria. Ann Surg. 2011;254:108–113.PubMedCrossRef Lim KC, Chow PK, Allen JC, Chia GS, Lim M, Cheow PC, et al. Microvascular invasion is a better predictor of tumor recurrence and overall survival following surgical resection for hepatocellular carcinoma compared to the Milan criteria. Ann Surg. 2011;254:108–113.PubMedCrossRef
26.
go back to reference Du M, Chen L, Zhao J, Tian F, Zeng H, Tan Y, et al. Microvascular invasion (MVI) is a poorer prognostic predictor for small hepatocellular carcinoma. BMC Cancer. 2014;14:38.PubMedPubMedCentralCrossRef Du M, Chen L, Zhao J, Tian F, Zeng H, Tan Y, et al. Microvascular invasion (MVI) is a poorer prognostic predictor for small hepatocellular carcinoma. BMC Cancer. 2014;14:38.PubMedPubMedCentralCrossRef
27.
go back to reference Wang H, Wu MC, Cong WM. Microvascular invasion predicts a poor prognosis of solitary hepatocellular carcinoma up to 2 cm based on propensity score matching analysis. Hepatol Res. 2019;49:344–354.PubMedCrossRef Wang H, Wu MC, Cong WM. Microvascular invasion predicts a poor prognosis of solitary hepatocellular carcinoma up to 2 cm based on propensity score matching analysis. Hepatol Res. 2019;49:344–354.PubMedCrossRef
28.
go back to reference Wang Z, Ren Z, Chen Y, Hu J, Yang G, Yu L, et al. Adjuvant transarterial chemoembolization for HBV-related hepatocellular carcinoma after resection: a randomized controlled study. Clin Cancer Res. 2018;24:2074–2081.PubMedCrossRef Wang Z, Ren Z, Chen Y, Hu J, Yang G, Yu L, et al. Adjuvant transarterial chemoembolization for HBV-related hepatocellular carcinoma after resection: a randomized controlled study. Clin Cancer Res. 2018;24:2074–2081.PubMedCrossRef
29.
go back to reference Wei W, Jian PE, Li SH, Guo ZX, Zhang YF, Ling YH, et al. Adjuvant transcatheter arterial chemoembolization after curative resection for hepatocellular carcinoma patients with solitary tumor and microvascular invasion: a randomized clinical trial of efficacy and safety. Cancer Commun (London). 2018;38(1):61.CrossRef Wei W, Jian PE, Li SH, Guo ZX, Zhang YF, Ling YH, et al. Adjuvant transcatheter arterial chemoembolization after curative resection for hepatocellular carcinoma patients with solitary tumor and microvascular invasion: a randomized clinical trial of efficacy and safety. Cancer Commun (London). 2018;38(1):61.CrossRef
30.
go back to reference EASL Clinical Practice Guidelines. Management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236.CrossRef EASL Clinical Practice Guidelines. Management of hepatocellular carcinoma. J Hepatol. 2018;69:182–236.CrossRef
31.
go back to reference Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology (Baltimore, MD). 2018;67:358–380.CrossRef Heimbach JK, Kulik LM, Finn RS, Sirlin CB, Abecassis MM, Roberts LR, et al. AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology (Baltimore, MD). 2018;67:358–380.CrossRef
32.
go back to reference Omata M, Cheng AL, Kokudo N, Kudo M, Lee JM, Jia J, et al. Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatol Int. 2017;11:317–370.PubMedCrossRef Omata M, Cheng AL, Kokudo N, Kudo M, Lee JM, Jia J, et al. Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatol Int. 2017;11:317–370.PubMedCrossRef
33.
go back to reference Chen ZH, Zhang XP, Wang H, Chai ZT, Sun JX, Guo WX, et al. Effect of microvascular invasion on the postoperative long-term prognosis of solitary small HCC: a systematic review and meta-analysis. HPB. 2019;21:935–944.PubMedCrossRef Chen ZH, Zhang XP, Wang H, Chai ZT, Sun JX, Guo WX, et al. Effect of microvascular invasion on the postoperative long-term prognosis of solitary small HCC: a systematic review and meta-analysis. HPB. 2019;21:935–944.PubMedCrossRef
34.
go back to reference Huo TI, Liu PH, Hsu CY. Detecting microvascular invasion in HCC with contrast-enhanced MRI: is it a good idea? J Hepatol. 2018;68:862–263.PubMedCrossRef Huo TI, Liu PH, Hsu CY. Detecting microvascular invasion in HCC with contrast-enhanced MRI: is it a good idea? J Hepatol. 2018;68:862–263.PubMedCrossRef
35.
go back to reference Cong WM, Dong H, Zhu YY, et al. Malignant tumors of the liver and intrahepatic bile ducts. In: Cong WM. Surgical pathology of hepatobiliary tumors. 1st ed. Springer Nature Singapore Pte Ltd. and People’s Medical Publishing House; 2017:145–282 Cong WM, Dong H, Zhu YY, et al. Malignant tumors of the liver and intrahepatic bile ducts. In: Cong WM. Surgical pathology of hepatobiliary tumors. 1st ed. Springer Nature Singapore Pte Ltd. and People’s Medical Publishing House; 2017:145–282
36.
go back to reference Fujita N, Aishima S, Iguchi T, Mano Y, Taketomi A, Shirabe K, et al. Histologic classification of microscopic portal venous invasion to predict prognosis in hepatocellular carcinoma. Hum Pathol. 2011;42:1531–1538.PubMedCrossRef Fujita N, Aishima S, Iguchi T, Mano Y, Taketomi A, Shirabe K, et al. Histologic classification of microscopic portal venous invasion to predict prognosis in hepatocellular carcinoma. Hum Pathol. 2011;42:1531–1538.PubMedCrossRef
37.
go back to reference Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S, et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009;137:850–855.PubMedCrossRef Roayaie S, Blume IN, Thung SN, Guido M, Fiel MI, Hiotis S, et al. A system of classifying microvascular invasion to predict outcome after resection in patients with hepatocellular carcinoma. Gastroenterology. 2009;137:850–855.PubMedCrossRef
38.
go back to reference Sumie S, Nakashima O, Okuda K, Kuromatsu R, Kawaguchi A, Nakano M, et al. The significance of classifying microvascular invasion in patients with hepatocellular carcinoma. Ann Surg Oncol. 2014;21:1002–1009.PubMedCrossRef Sumie S, Nakashima O, Okuda K, Kuromatsu R, Kawaguchi A, Nakano M, et al. The significance of classifying microvascular invasion in patients with hepatocellular carcinoma. Ann Surg Oncol. 2014;21:1002–1009.PubMedCrossRef
39.
go back to reference Hidaka M, Eguchi S, Okuda K, Beppu T, Shirabe K, Kondo K, et al. Impact of anatomical resection for hepatocellular carcinoma with microportal invasion (vp1): a multi-institutional study by the kyushu study group of liver surgery. Ann Surg. 2020;271(2):339–346.PubMedCrossRef Hidaka M, Eguchi S, Okuda K, Beppu T, Shirabe K, Kondo K, et al. Impact of anatomical resection for hepatocellular carcinoma with microportal invasion (vp1): a multi-institutional study by the kyushu study group of liver surgery. Ann Surg. 2020;271(2):339–346.PubMedCrossRef
40.
go back to reference Toyosaka A, Okamoto E, Mitsunobu M, Oriyama T, Nakao N, Miura K. Pathologic and radiographic studies of intrahepatic metastasis in hepatocellular carcinoma; the role of efferent vessels. Hepato-Pancreato-Biliary Surg. 1996;10(2):97–103.CrossRef Toyosaka A, Okamoto E, Mitsunobu M, Oriyama T, Nakao N, Miura K. Pathologic and radiographic studies of intrahepatic metastasis in hepatocellular carcinoma; the role of efferent vessels. Hepato-Pancreato-Biliary Surg. 1996;10(2):97–103.CrossRef
41.
go back to reference Park NH, Chung YH, Youn KH, Song BC, Yang SH, Kim JA, et al. Close correlation of p53 mutation to microvascular invasion in hepatocellular carcinoma. J Clin Gastroenterol. 2001;33:397–401.PubMedCrossRef Park NH, Chung YH, Youn KH, Song BC, Yang SH, Kim JA, et al. Close correlation of p53 mutation to microvascular invasion in hepatocellular carcinoma. J Clin Gastroenterol. 2001;33:397–401.PubMedCrossRef
42.
go back to reference Erstad DJ, Tanabe KK. Prognostic and therapeutic implications of microvascular invasion in hepatocellular carcinoma. Ann Surg Oncol. 2019;26:1474–1493.PubMedCrossRef Erstad DJ, Tanabe KK. Prognostic and therapeutic implications of microvascular invasion in hepatocellular carcinoma. Ann Surg Oncol. 2019;26:1474–1493.PubMedCrossRef
43.
go back to reference Feng LH, Dong H, Lau WY, Yu H, Zhu YY, Zhao Y, et al. Novel microvascular invasion-based prognostic nomograms to predict survival outcomes in patients after R0 resection for hepatocellular carcinoma. J Cancer Res Clin Oncol. 2017;143:293–303.PubMedCrossRef Feng LH, Dong H, Lau WY, Yu H, Zhu YY, Zhao Y, et al. Novel microvascular invasion-based prognostic nomograms to predict survival outcomes in patients after R0 resection for hepatocellular carcinoma. J Cancer Res Clin Oncol. 2017;143:293–303.PubMedCrossRef
44.
go back to reference Li Z, Lei Z, Xia Y, Li J, Wang K, Zhang H, et al. Association of preoperative antiviral treatment with incidences of microvascular invasion and early tumor recurrence in hepatitis B virus-related hepatocellular carcinoma. JAMA Surg. 2018;153(10):e182721.PubMedPubMedCentralCrossRef Li Z, Lei Z, Xia Y, Li J, Wang K, Zhang H, et al. Association of preoperative antiviral treatment with incidences of microvascular invasion and early tumor recurrence in hepatitis B virus-related hepatocellular carcinoma. JAMA Surg. 2018;153(10):e182721.PubMedPubMedCentralCrossRef
45.
go back to reference Wang B, Xia CY, Lau WY, Lu XY, Dong H, Yu WL, et al. Determination of clonal origin of recurrent hepatocellular carcinoma for personalized therapy and outcomes evaluation: a new strategy for hepatic surgery. J Am Coll Surg. 2013;217:1054–1062.PubMedCrossRef Wang B, Xia CY, Lau WY, Lu XY, Dong H, Yu WL, et al. Determination of clonal origin of recurrent hepatocellular carcinoma for personalized therapy and outcomes evaluation: a new strategy for hepatic surgery. J Am Coll Surg. 2013;217:1054–1062.PubMedCrossRef
46.
go back to reference Wang H, Feng LH, Qian YW, Cao ZY, Wu MC, Cong WM. Does microvascular invasion in Barcelona Clinic Liver Cancer stage A multinodular hepatocellular carcinoma indicate early-stage behavior? Ann Transl Med. 2019;7(18):428.PubMedPubMedCentralCrossRef Wang H, Feng LH, Qian YW, Cao ZY, Wu MC, Cong WM. Does microvascular invasion in Barcelona Clinic Liver Cancer stage A multinodular hepatocellular carcinoma indicate early-stage behavior? Ann Transl Med. 2019;7(18):428.PubMedPubMedCentralCrossRef
47.
go back to reference Wang H, Du PC, Wu MC, Cong WM. Postoperative adjuvant transarterial chemoembolization for multinodular hepatocellular carcinoma within the Barcelona Clinic Liver Cancer early stage and microvascular invasion. Hepatobiliary Surg Nutr. 2018;7:418–428.PubMedPubMedCentralCrossRef Wang H, Du PC, Wu MC, Cong WM. Postoperative adjuvant transarterial chemoembolization for multinodular hepatocellular carcinoma within the Barcelona Clinic Liver Cancer early stage and microvascular invasion. Hepatobiliary Surg Nutr. 2018;7:418–428.PubMedPubMedCentralCrossRef
48.
go back to reference Yang P, Si A, Yang J, Cheng Z, Wang K, Li J, et al. A wide-margin liver resection improves long-term outcomes for patients with HBV-related hepatocellular carcinoma with microvascular invasion. Surgery. 2019;165:721–730.PubMedCrossRef Yang P, Si A, Yang J, Cheng Z, Wang K, Li J, et al. A wide-margin liver resection improves long-term outcomes for patients with HBV-related hepatocellular carcinoma with microvascular invasion. Surgery. 2019;165:721–730.PubMedCrossRef
49.
go back to reference Wang H, Yu H, Qian YW, Cao ZY, Wu MC, Cong WM. Impact of surgical margin on the prognosis of early hepatocellular carcinoma (≤5 cm): a propensity score matching analysis. Front Med 2020;7(139). Wang H, Yu H, Qian YW, Cao ZY, Wu MC, Cong WM. Impact of surgical margin on the prognosis of early hepatocellular carcinoma (≤5 cm): a propensity score matching analysis. Front Med 2020;7(139).
50.
go back to reference Wang L, Wang W, Yao X, Rong W, Wu F, Chen B, et al. Postoperative adjuvant radiotherapy is associated with improved survival in hepatocellular carcinoma with microvascular invasion. Oncotarget. 2017;8:79971–79981.PubMedPubMedCentralCrossRef Wang L, Wang W, Yao X, Rong W, Wu F, Chen B, et al. Postoperative adjuvant radiotherapy is associated with improved survival in hepatocellular carcinoma with microvascular invasion. Oncotarget. 2017;8:79971–79981.PubMedPubMedCentralCrossRef
Metadata
Title
A standardized pathological proposal for evaluating microvascular invasion of hepatocellular carcinoma: a multicenter study by LCPGC
Authors
Xia Sheng
Yuan Ji
Guo-Ping Ren
Chang-Li Lu
Jing-Ping Yun
Li-Hong Chen
Bin Meng
Li-Juan Qu
Guang-Jie Duan
Qing Sun
Xin-Qing Ye
Shan-Shan Li
Jing Yang
Bing Liao
Zhan-Bo Wang
Jian-Hua Zhou
Yu Sun
Xue-Shan Qiu
Lei Wang
Zeng-Shan Li
Jun Chen
Chun-Yan Xia
Song He
Chuan-Ying Li
En-Wei Xu
Jing-Shu Geng
Chao Pan
Dong Kuang
Rong Qin
Hong-Wei Guan
Zhan-Dong Wang
Li-Xing Li
Xi Zhang
Han Wang
Qian Zhao
Bo Wei
Wu-Jian Zhang
Shao-Ping Ling
Xiang Du
Wen-Ming Cong
for the Liver Cancer Pathology Group of China (LCPGC)
Publication date
01-12-2020
Publisher
Springer India
Published in
Hepatology International / Issue 6/2020
Print ISSN: 1936-0533
Electronic ISSN: 1936-0541
DOI
https://doi.org/10.1007/s12072-020-10111-4

Other articles of this Issue 6/2020

Hepatology International 6/2020 Go to the issue