Research advances in early postoperative recurrence of hepatocellular carcinoma with microvascular invasion_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

WANG Kaiti ¹ , BADENGCAIREN Anrui ¹ , CONG Yun ¹ , ZHANG Ruiqing ¹ ,  SHAO Yingmei ^1,2 , TUERGANAILI Aji ^1,2

1. Department of Hepatobiliary Hydatid Disease Surgery, the First Affiliated Hospital of Xinjiang Medical University, Urumqi 830054, P. R. China;
2. State Key Laboratory of Central Asian High-Prevalence Disease Etiology and Prevention, Xinjiang Medical University, Urumqi 830054, P. R. China;

Corresponding author：

SHAO Yingmei, Email: syingmei1@163.com

Keywords：

hepatocellular carcinoma; microvascular invasion; recurrence and metastasis; treatment; radical hepatectomy

DOI：

10.7507/1007-9424.202406037

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To explore the impact of microvascular invasion (MVI) on the survival prognosis of patients after radical hepatectomy for hepatocellular carcinoma, to analyze its related risk factors and preoperative prediction methods, and to provide reference and support for the treatment of early postoperative recurrence. Methods By searching domestic and international medical literature databases, we screened studies related to MVI in hepatocellular carcinoma, focusing on the definition, grading, risk factors, preoperative prediction methods, and postoperative treatment strategies of MVI, and summarized the results of the existing studies. Results MVI was a well-established risk factor for the intrahepatic metastasis and early postoperative recurrence of hepatocellular carcinoma. Currently, various methods were employed to predict MVI, including laboratory indicators, imaging genomics, and genomics. The laboratory indicators used for prediction included alpha-fetoprotein, protein induced by vitamin K absence or antagonist-Ⅱ, hepatitis B virus, tumor diameter, vascular endothelial growth factor A, and circulating tumor cells. Imaging genomics involved preoperative MRI with irregular tumor shape and intra-voxel incoherent motion diffusion-weighted imaging D value < 1.16 × 10^-3 mm²/S, CT enhancement imaging features with irregular tumor margins, multiple foci, and contrast-enhanced ultrasound portal venous and delayed phase scores. Genomics included the maximum variant allele frequency of circulating tumor DNA. In cases where MVI was detected after surgery, adjuvant therapy options had gained attention, such as transcatheter arterial chemoembolization, hepatic arterial infusion chemotherapy, targeted therapy, immunotherapy, radiation therapy, antiviral therapy, and local treatment combined with systemic treatment. Conclusions The study of MVI and its targeted treatment strategies are important for reducing the postoperative recurrence rate of hepatocellular carcinoma and improving patient survival. The preoperative prediction model and postoperative treatment plan should be optimized in the future to provide more effective treatment reference for patients.

Citation： WANG Kaiti, BADENGCAIREN Anrui, CONG Yun, ZHANG Ruiqing, SHAO Yingmei, TUERGANAILI Aji. Research advances in early postoperative recurrence of hepatocellular carcinoma with microvascular invasion. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(11): 1399-1405. doi: 10.7507/1007-9424.202406037 Copy

1.	Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2024, 74(3): 229-263.
2.	郝运, 李川, 文天夫, 等. 全球及中国的肝癌流行病学特征: 基于《2022全球癌症统计报告》解读. 中国普外基础与临床杂志, 2024, 31(7): 781-789.
3.	Lu C, Rong D, Zhang B, et al. Current perspectives on the immunosuppressive tumor microenvironment in hepatocellular carcinoma: challenges and opportunities. Mol Cancer, 2019, 18(1): 130. doi: 10.1186/s12943-019-1047-6.
4.	中国医师协会肝癌专业委员会. 肝细胞癌伴微血管侵犯诊断和治疗中国专家共识 (2024版). 中华消化外科杂志, 2024, 23(2): 153-164.
5.	Calderaro J, Petitprez F, Becht E, et al. Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma. J Hepatol, 2019, 70(1): 58-65.
6.	Tabrizian P, Jibara G, Shrager B, et al. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg, 2015, 261(5): 947-955.
7.	Feng LH, Dong H, Lau WY, 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(2): 293-303.
8.	Xu XF, Diao YK, Zeng YY, et al. Association of severity in the grading of microvascular invasion with long-term oncological prognosis after liver resection for early-stage hepatocellular carcinoma: a multicenter retrospective cohort study from a hepatitis B virus-endemic area. Int J Surg, 2023, 109(4): 841-849.
9.	Lei Z, 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.
10.	Wang H, Liu R, Mo H, et al. A novel nomogram predicting the early recurrence of hepatocellular carcinoma patients after R0 resection. Front Oncol, 2023, 13: 1133807. doi: 10.3389/fonc.2023.1133807.
11.	Ryu T, Takami Y, Wada Y, et al. A clinical scoring system for predicting microvascular invasion in patients with hepatocellular carcinoma within the Milan Criteria. J Gastrointest Surg, 2019, 23(4): 779-787.
12.	Yamashita YI, Imai K, Yusa T, et al. Microvascular invasion of single small hepatocellular carcinoma ≤3 cm: predictors and optimal treatments. Ann Gastroenterol Surg, 2018, 2(3): 197-203.
13.	Kim DY, Toan BN, Tan CK, et al. Utility of combining PIVKA-Ⅱ and AFP in the surveillance and monitoring of hepatocellular carcinoma in the Asia-Pacific region. Clin Mol Hepatol, 2023, 29(2): 277-292.
14.	Hong YM, Cho M, Yoon KT, et al. Risk factors of early recurrence after curative hepatectomy in hepatocellular carcinoma. Tumour Biol, 2017, 39(10): 1010428317720863.
15.	Yang J, Qian J, Wu Z, et al. Exploring the factors affecting the occurrence of postoperative MVI and the prognosis of hepatocellular carcinoma patients treated with hepatectomy: a multicenter retrospective study. Cancer Med, 2024, 13(3): e6933. doi: 10.1002/cam4.6933.
16.	Apte RS, Chen DS, Ferrara N. VEGF in signaling and disease: beyond discovery and development. Cell, 2019, 176(6): 1248-1264.
17.	Wang H, Lu Y, Liu R, et al. A non-invasive nomogram for preoperative prediction of microvascular invasion risk in hepatocellular carcinoma. Front Oncol, 2021, 11: 745085. doi: 10.3389/fonc.2021.745085.
18.	Ha Y, Kim TH, Shim JE, et al. Circulating tumor cells are associated with poor outcomes in early-stage hepatocellular carcinoma: a prospective study. Hepatol Int, 2019, 13(6): 726-735.
19.	Zhou J, Zhang Z, Zhou H, et al. Preoperative circulating tumor cells to predict microvascular invasion and dynamical detection indicate the prognosis of hepatocellular carcinoma. BMC Cancer, 2020, 20(1): 1047. doi: 10.1186/s12885-020-07488-8.
20.	Zheng X, Xu YJ, Huang J, et al. Predictive value of radiomics analysis of enhanced CT for three-tiered microvascular invasion grading in hepatocellular carcinoma. Med Phys, 2023, 50(10): 6079-6095.
21.	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.
22.	Meng XP, Wang YC, Zhou JY, et al. Comparison of MRI and CT for the prediction of microvascular invasion in solitary hepatocellular carcinoma based on a non-radiomics and radiomics method: which imaging modality is better? J Magn Reson Imaging, 2021, 54(2): 526-536.
23.	瞿成名, 李昆, 蔡萍, 等. 基于MRI影像组学的特征模型预测肝细胞癌微血管侵犯的研究. 中国普外基础与临床杂志, 2021, 28(2): 175-180.
24.	Zhao W, Liu W, Liu H, et al. Preoperative prediction of microvascular invasion of hepatocellular carcinoma with IVIM diffusion-weighted MR imaging and Gd-EOB-DTPA-enhanced MR imaging. PLoS One, 2018, 13(5): e0197488. doi: 10.1371/journal.pone.0197488.
25.	Zhang D, Wei Q, Wu GG, et al. Preoperative prediction of microvascular invasion in patients with hepatocellular carcinoma based on radiomics nomogram using contrast-enhanced ultrasound. Front Oncol, 2021, 11: 709339. doi: 10.3389/fonc.2021.709339.
26.	Xin Z, Li J, Zhang H, et al. Cancer genomic alterations can be potential biomarkers predicting microvascular invasion and early recurrence of hepatocellular carcinoma. Front Oncol, 2022, 12: 783109. doi: 10.3389/fonc.2022.783109.
27.	Wang J, Ding ZW, Chen K, et al. A predictive and prognostic model for hepatocellular carcinoma with microvascular invasion based TCGA database genomics. BMC Cancer, 2021, 21(1): 1337. doi: 10.1186/s12885-021-09047-1.
28.	Zhang Y, Wei Q, Huang Y, et al. Deep learning of liver contrast-enhanced ultrasound to predict microvascular invasion and prognosis in hepatocellular carcinoma. Front Oncol, 2022, 12: 878061. doi: 10.3389/fonc.2022.878061.
29.	Song D, Wang Y, Wang W, et al. Using deep learning to predict microvascular invasion in hepatocellular carcinoma based on dynamic contrast-enhanced MRI combined with clinical parameters. J Cancer Res Clin Oncol, 2021, 147(12): 3757-3767.
30.	Yang Y, Zhou Y, Zhou C, et al. Deep learning radiomics based on contrast enhanced computed tomography predicts microvascular invasion and survival outcome in early stage hepatocellular carcinoma. Eur J Surg Oncol, 2022, 48(5): 1068-1077.
31.	Li SH, Mei J, Cheng Y, et al. Postoperative adjuvant hepatic arterial infusion chemotherapy with FOLFOX in hepatocellular carcinoma with microvascular invasion: a multicenter, phase Ⅲ, randomized study. J Clin Oncol, 2023, 41(10): 1898-1908.
32.	Bai S, Hu L, Liu J, et al. Prognostic nomograms combined adjuvant lenvatinib for hepatitis B virus-related hepatocellular carcinoma with microvascular invasion after radical resection. Front Oncol, 2022, 12: 919824. doi: 10.3389/fonc.2022.919824.
33.	Zhang W, Zhang B, Chen XP. Adjuvant treatment strategy after curative resection for hepatocellular carcinoma. Front Med, 2021, 15(2): 155-169.
34.	Wei W, Jian PE, Li SH, 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 (Lond), 2018, 38(1): 61.
35.	Gai X, Zhou P, Xu M, et al. Hyperactivation of IL-6/STAT3 pathway leaded to the poor prognosis of post-TACE HCCs by HIF-1α/SNAI1 axis-induced epithelial to mesenchymal transition. J Cancer, 2020, 11(3): 570-582.
36.	Qi W, Peng W, Qi X, et al. TIDE: adjuvant tislelizumab plus donafenib combined with transarterial chemoembolization for high-risk hepatocellular carcinoma after surgery: protocol for a prospective, single-arm, phase Ⅱ trial. Front Oncol, 2023, 13: 1138570. doi: 10.3389/fonc.2023.1138570.
37.	Peng Z, Fan W, Liu Z, et al. Adjuvant transarterial chemoembolization with sorafenib for portal vein tumor thrombus: a randomized clinical trial. JAMA Surg, 2024, 159(6): 616-624.
38.	Tang Y, Zhang J, Chen G, et al. Efficacy of adjuvant transarterial chemoembolization combined antiviral therapy for HBV-related HCC with MVI after hepatic resection: a multicenter study. Asian Pac J Cancer Prev, 2022, 23(8): 2695-2703.
39.	He M, Li Q, Zou R, et al. Sorafenib plus hepatic arterial infusion of oxaliplatin, fluorouracil, and leucovorin vs sorafenib alone for hepatocellular carcinoma with portal vein invasion: a randomized clinical trial. JAMA Oncol, 2019, 5(7): 953-960.
40.	Mei J, Li SH, Li QJ, et al. Anti-PD-1 immunotherapy improves the efficacy of hepatic artery infusion chemotherapy in advanced hepatocellular carcinoma. J Hepatocell Carcinoma, 2021, 8: 167-176.
41.	Wang L, Wang W, Rong W, et al. Postoperative adjuvant treatment strategy for hepatocellular carcinoma with microvascular invasion: a non-randomized interventional clinical study. BMC Cancer, 2020, 20(1): 614. doi: 10.1186/s12885-020-07087-7.
42.	Chen J, He K, Han Y, et al. Clinical efficacy and safety of external radiotherapy combined with sorafenib in the treatment of hepatocellular carcinoma: a systematic review and meta-analysis. Ann Hepatol, 2022, 27(4): 100710. doi: 10.1016/j.aohep.2022.100710.
43.	Li H, Wu Z, Chen J, et al. External radiotherapy combined with sorafenib has better efficacy in unresectable hepatocellular carcinoma: a systematic review and meta-analysis. Clin Exp Med, 2023, 23(5): 1537-1549.
44.	Zhang XP, Chai ZT, Gao YZ, et al. Postoperative adjuvant sorafenib improves survival outcomes in hepatocellular carcinoma patients with microvascular invasion after R0 liver resection: a propensity score matching analysis. HPB (Oxford), 2019, 21(12): 1687-1696.
45.	Li J, Wang WQ, Zhu RH, et al. Postoperative adjuvant tyrosine kinase inhibitors combined with anti-PD-1 antibodies improves surgical outcomes for hepatocellular carcinoma with high-risk recurrent factors. Front Immunol, 2023, 14: 1202039. doi: 10.3389/fimmu.2023.1202039.
46.	Qin S, Chen M, Cheng AL, et al. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial. Lancet, 2023, 402(10415): 1835-1847.
47.	You H, Wang F, Li T, et al. Guidelines for the prevention and treatment of chronic hepatitis B (version 2022). J Clin Transl Hepatol, 2023, 11(6): 1425-1442.
48.	Liu K, Duan J, Liu H, et al. Precancer antiviral treatment reduces microvascular invasion of early-stage hepatitis B-related hepatocellular carcinoma. Sci Rep, 2019, 9(1): 2220. doi: 10.1038/s41598-019-39440-7.
49.	Li Z, Lei Z, Xia Y, 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. doi: 10.1001/jamasurg.2018.2721.
50.	Huang S, Xia Y, Lei Z, et al. Antiviral therapy inhibits viral reactivation and improves survival after repeat hepatectomy for hepatitis B virus-related recurrent hepatocellular carcinoma. J Am Coll Surg, 2017, 224(3): 283-293.e4.

1. Bray F, Laversanne M, Sung H, et al. Global cancer statistics 2022: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2024, 74(3): 229-263.
2. 郝运, 李川, 文天夫, 等. 全球及中国的肝癌流行病学特征: 基于《2022全球癌症统计报告》解读. 中国普外基础与临床杂志, 2024, 31(7): 781-789.
3. Lu C, Rong D, Zhang B, et al. Current perspectives on the immunosuppressive tumor microenvironment in hepatocellular carcinoma: challenges and opportunities. Mol Cancer, 2019, 18(1): 130. doi: 10.1186/s12943-019-1047-6.
4. 中国医师协会肝癌专业委员会. 肝细胞癌伴微血管侵犯诊断和治疗中国专家共识 (2024版). 中华消化外科杂志, 2024, 23(2): 153-164.
5. Calderaro J, Petitprez F, Becht E, et al. Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma. J Hepatol, 2019, 70(1): 58-65.
6. Tabrizian P, Jibara G, Shrager B, et al. Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg, 2015, 261(5): 947-955.
7. Feng LH, Dong H, Lau WY, 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(2): 293-303.
8. Xu XF, Diao YK, Zeng YY, et al. Association of severity in the grading of microvascular invasion with long-term oncological prognosis after liver resection for early-stage hepatocellular carcinoma: a multicenter retrospective cohort study from a hepatitis B virus-endemic area. Int J Surg, 2023, 109(4): 841-849.
9. Lei Z, 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.
10. Wang H, Liu R, Mo H, et al. A novel nomogram predicting the early recurrence of hepatocellular carcinoma patients after R0 resection. Front Oncol, 2023, 13: 1133807. doi: 10.3389/fonc.2023.1133807.
11. Ryu T, Takami Y, Wada Y, et al. A clinical scoring system for predicting microvascular invasion in patients with hepatocellular carcinoma within the Milan Criteria. J Gastrointest Surg, 2019, 23(4): 779-787.
12. Yamashita YI, Imai K, Yusa T, et al. Microvascular invasion of single small hepatocellular carcinoma ≤3 cm: predictors and optimal treatments. Ann Gastroenterol Surg, 2018, 2(3): 197-203.
13. Kim DY, Toan BN, Tan CK, et al. Utility of combining PIVKA-Ⅱ and AFP in the surveillance and monitoring of hepatocellular carcinoma in the Asia-Pacific region. Clin Mol Hepatol, 2023, 29(2): 277-292.
14. Hong YM, Cho M, Yoon KT, et al. Risk factors of early recurrence after curative hepatectomy in hepatocellular carcinoma. Tumour Biol, 2017, 39(10): 1010428317720863.
15. Yang J, Qian J, Wu Z, et al. Exploring the factors affecting the occurrence of postoperative MVI and the prognosis of hepatocellular carcinoma patients treated with hepatectomy: a multicenter retrospective study. Cancer Med, 2024, 13(3): e6933. doi: 10.1002/cam4.6933.
16. Apte RS, Chen DS, Ferrara N. VEGF in signaling and disease: beyond discovery and development. Cell, 2019, 176(6): 1248-1264.
17. Wang H, Lu Y, Liu R, et al. A non-invasive nomogram for preoperative prediction of microvascular invasion risk in hepatocellular carcinoma. Front Oncol, 2021, 11: 745085. doi: 10.3389/fonc.2021.745085.
18. Ha Y, Kim TH, Shim JE, et al. Circulating tumor cells are associated with poor outcomes in early-stage hepatocellular carcinoma: a prospective study. Hepatol Int, 2019, 13(6): 726-735.
19. Zhou J, Zhang Z, Zhou H, et al. Preoperative circulating tumor cells to predict microvascular invasion and dynamical detection indicate the prognosis of hepatocellular carcinoma. BMC Cancer, 2020, 20(1): 1047. doi: 10.1186/s12885-020-07488-8.
20. Zheng X, Xu YJ, Huang J, et al. Predictive value of radiomics analysis of enhanced CT for three-tiered microvascular invasion grading in hepatocellular carcinoma. Med Phys, 2023, 50(10): 6079-6095.
21. 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.
22. Meng XP, Wang YC, Zhou JY, et al. Comparison of MRI and CT for the prediction of microvascular invasion in solitary hepatocellular carcinoma based on a non-radiomics and radiomics method: which imaging modality is better? J Magn Reson Imaging, 2021, 54(2): 526-536.
23. 瞿成名, 李昆, 蔡萍, 等. 基于MRI影像组学的特征模型预测肝细胞癌微血管侵犯的研究. 中国普外基础与临床杂志, 2021, 28(2): 175-180.
24. Zhao W, Liu W, Liu H, et al. Preoperative prediction of microvascular invasion of hepatocellular carcinoma with IVIM diffusion-weighted MR imaging and Gd-EOB-DTPA-enhanced MR imaging. PLoS One, 2018, 13(5): e0197488. doi: 10.1371/journal.pone.0197488.
25. Zhang D, Wei Q, Wu GG, et al. Preoperative prediction of microvascular invasion in patients with hepatocellular carcinoma based on radiomics nomogram using contrast-enhanced ultrasound. Front Oncol, 2021, 11: 709339. doi: 10.3389/fonc.2021.709339.
26. Xin Z, Li J, Zhang H, et al. Cancer genomic alterations can be potential biomarkers predicting microvascular invasion and early recurrence of hepatocellular carcinoma. Front Oncol, 2022, 12: 783109. doi: 10.3389/fonc.2022.783109.
27. Wang J, Ding ZW, Chen K, et al. A predictive and prognostic model for hepatocellular carcinoma with microvascular invasion based TCGA database genomics. BMC Cancer, 2021, 21(1): 1337. doi: 10.1186/s12885-021-09047-1.
28. Zhang Y, Wei Q, Huang Y, et al. Deep learning of liver contrast-enhanced ultrasound to predict microvascular invasion and prognosis in hepatocellular carcinoma. Front Oncol, 2022, 12: 878061. doi: 10.3389/fonc.2022.878061.
29. Song D, Wang Y, Wang W, et al. Using deep learning to predict microvascular invasion in hepatocellular carcinoma based on dynamic contrast-enhanced MRI combined with clinical parameters. J Cancer Res Clin Oncol, 2021, 147(12): 3757-3767.
30. Yang Y, Zhou Y, Zhou C, et al. Deep learning radiomics based on contrast enhanced computed tomography predicts microvascular invasion and survival outcome in early stage hepatocellular carcinoma. Eur J Surg Oncol, 2022, 48(5): 1068-1077.
31. Li SH, Mei J, Cheng Y, et al. Postoperative adjuvant hepatic arterial infusion chemotherapy with FOLFOX in hepatocellular carcinoma with microvascular invasion: a multicenter, phase Ⅲ, randomized study. J Clin Oncol, 2023, 41(10): 1898-1908.
32. Bai S, Hu L, Liu J, et al. Prognostic nomograms combined adjuvant lenvatinib for hepatitis B virus-related hepatocellular carcinoma with microvascular invasion after radical resection. Front Oncol, 2022, 12: 919824. doi: 10.3389/fonc.2022.919824.
33. Zhang W, Zhang B, Chen XP. Adjuvant treatment strategy after curative resection for hepatocellular carcinoma. Front Med, 2021, 15(2): 155-169.
34. Wei W, Jian PE, Li SH, 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 (Lond), 2018, 38(1): 61.
35. Gai X, Zhou P, Xu M, et al. Hyperactivation of IL-6/STAT3 pathway leaded to the poor prognosis of post-TACE HCCs by HIF-1α/SNAI1 axis-induced epithelial to mesenchymal transition. J Cancer, 2020, 11(3): 570-582.
36. Qi W, Peng W, Qi X, et al. TIDE: adjuvant tislelizumab plus donafenib combined with transarterial chemoembolization for high-risk hepatocellular carcinoma after surgery: protocol for a prospective, single-arm, phase Ⅱ trial. Front Oncol, 2023, 13: 1138570. doi: 10.3389/fonc.2023.1138570.
37. Peng Z, Fan W, Liu Z, et al. Adjuvant transarterial chemoembolization with sorafenib for portal vein tumor thrombus: a randomized clinical trial. JAMA Surg, 2024, 159(6): 616-624.
38. Tang Y, Zhang J, Chen G, et al. Efficacy of adjuvant transarterial chemoembolization combined antiviral therapy for HBV-related HCC with MVI after hepatic resection: a multicenter study. Asian Pac J Cancer Prev, 2022, 23(8): 2695-2703.
39. He M, Li Q, Zou R, et al. Sorafenib plus hepatic arterial infusion of oxaliplatin, fluorouracil, and leucovorin vs sorafenib alone for hepatocellular carcinoma with portal vein invasion: a randomized clinical trial. JAMA Oncol, 2019, 5(7): 953-960.
40. Mei J, Li SH, Li QJ, et al. Anti-PD-1 immunotherapy improves the efficacy of hepatic artery infusion chemotherapy in advanced hepatocellular carcinoma. J Hepatocell Carcinoma, 2021, 8: 167-176.
41. Wang L, Wang W, Rong W, et al. Postoperative adjuvant treatment strategy for hepatocellular carcinoma with microvascular invasion: a non-randomized interventional clinical study. BMC Cancer, 2020, 20(1): 614. doi: 10.1186/s12885-020-07087-7.
42. Chen J, He K, Han Y, et al. Clinical efficacy and safety of external radiotherapy combined with sorafenib in the treatment of hepatocellular carcinoma: a systematic review and meta-analysis. Ann Hepatol, 2022, 27(4): 100710. doi: 10.1016/j.aohep.2022.100710.
43. Li H, Wu Z, Chen J, et al. External radiotherapy combined with sorafenib has better efficacy in unresectable hepatocellular carcinoma: a systematic review and meta-analysis. Clin Exp Med, 2023, 23(5): 1537-1549.
44. Zhang XP, Chai ZT, Gao YZ, et al. Postoperative adjuvant sorafenib improves survival outcomes in hepatocellular carcinoma patients with microvascular invasion after R0 liver resection: a propensity score matching analysis. HPB (Oxford), 2019, 21(12): 1687-1696.
45. Li J, Wang WQ, Zhu RH, et al. Postoperative adjuvant tyrosine kinase inhibitors combined with anti-PD-1 antibodies improves surgical outcomes for hepatocellular carcinoma with high-risk recurrent factors. Front Immunol, 2023, 14: 1202039. doi: 10.3389/fimmu.2023.1202039.
46. Qin S, Chen M, Cheng AL, et al. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): a randomised, open-label, multicentre, phase 3 trial. Lancet, 2023, 402(10415): 1835-1847.
47. You H, Wang F, Li T, et al. Guidelines for the prevention and treatment of chronic hepatitis B (version 2022). J Clin Transl Hepatol, 2023, 11(6): 1425-1442.
48. Liu K, Duan J, Liu H, et al. Precancer antiviral treatment reduces microvascular invasion of early-stage hepatitis B-related hepatocellular carcinoma. Sci Rep, 2019, 9(1): 2220. doi: 10.1038/s41598-019-39440-7.
49. Li Z, Lei Z, Xia Y, 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. doi: 10.1001/jamasurg.2018.2721.
50. Huang S, Xia Y, Lei Z, et al. Antiviral therapy inhibits viral reactivation and improves survival after repeat hepatectomy for hepatitis B virus-related recurrent hepatocellular carcinoma. J Am Coll Surg, 2017, 224(3): 283-293.e4.

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Research advances in early postoperative recurrence of hepatocellular carcinoma with microvascular invasion

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