Research progress of hepatocellular carcinoma with lung metastasis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

LI Zhengshi ^1,2 , WU Hong ³ ,  LIU Chang ^1,2

1. Division of Liver Surgery, Department of General Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;
2. Department of Minimal Invasive Surgery, Shangjin Nanfu Hospital, Chengdu 610037, P. R. China;
3. Liver Transplant Center, Transplant Center, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

LIU Chang, Email: drliuchang@wchscu.cn

Keywords：

hepatocellular carcinoma; lung metastasis; transfer mechanism; treatment

DOI：

10.7507/1007-9424.202304017

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the recent progress in the research on the mechanism and treatment of lung metastasis of hepatocellular carcinoma, in order to provide reference for clinical workers to systematically treat patients with lung metastasis of hepatocellular carcinoma, guarantee their survival and improve their quality of life. Method The literatures about mechanism and clinical treatment of lung metastasis of hepatocellular carcinoma in recent years were reviewed. Results At home and abroad, there was no unified treatment standard for patients with lung metastasis of hepatocellular carcinoma. For patients with early metastasis, some scholars proposed resection of the metastasis, or ablation, radiotherapy and other methods for the metastatic site. For patients with advanced lung metastasis, systematic therapy was used. Conclusions The treatment effect is not ideal due to the limitations of few clinical studies, low level of evidence and complex disease mechanism, and there is no unified treatment standard. Therefore, in view of the differences between patients and the specific reality in clinical treatment, personalized treatment is implemented.

Citation： LI Zhengshi, WU Hong, LIU Chang. Research progress of hepatocellular carcinoma with lung metastasis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(8): 1001-1007. doi: 10.7507/1007-9424.202304017 Copy

1.	Uchino K, Tateishi R, Shiina S, et al. Hepatocellular carcinoma with extrahepatic metastasis: clinical features and prognostic factors. Cancer, 2011, 117(19): 4475-4483.
2.	Katyal S, Oliver JH 3rd, Peterson MS, et al. Extrahepatic metastases of hepatocellular carcinoma. Radiology, 2000, 216(3): 698-703.
3.	Wu C, Ren X, Zhang Q. Incidence, risk factors, and prognosis in patients with primary hepatocellular carcinoma and lung metastasis: a population-based study. Cancer Manag Res, 2019, 11: 2759-2768.
4.	Guo X, Xu Y, Wang X, et al. Advanced hepatocellular carcinoma with bone metastases: prevalence, associated factors, and survival estimation. Med Sci Monit, 2019, 25: 1105-1112.
5.	Alshahrani AA, Ha SM, Hwang S, et al. Clinical features and surveillance of very late hepatocellular carcinoma recurrence after liver transplantation. Ann Transplant, 2018, 23: 659-665.
6.	He Y, Lin Y, He F, et al. Role for calcium-activated potassium channels (BK) in migration control of human hepatocellular carcinoma cells. J Cell Mol Med, 2021, 25(20): 9685-9696.
7.	Kaczynski J, Hansson G, Wallerstedt S. Metastases in cases with hepatocellular carcinoma in relation to clinicopathologic features of the tumor. An autopsy study from a low endemic area. Acta Oncol, 1995, 34(1): 43-48.
8.	方东升. 肺转移癌189例临床分析. 河北医学, 2001, 7(11): 1011-1012.
9.	Yuki K, Hirohashi S, Sakamoto M, et al. Growth and spread of hepatocellular carcinoma. A review of 240 consecutive autopsy cases. Cancer, 1990, 66(10): 2174-2179.
10.	Yang JC, Hu JJ, Li YX, et al. Clinical applications of liquid biopsy in hepatocellular carcinoma. Front Oncol, 2022, 12: 781820. doi: 10.3389/fonc.2022.781820.
11.	Ye L, Zhang Q, Cheng Y, et al. Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1⁺ regulatory B cell expansion. J Immunother Cancer, 2018, 6(1): 145. doi: 10.1186/s40425-018-0451-6.
12.	Pu Z, Duda DG, Zhu Y, et al. VCP interaction with HMGB1 promotes hepatocellular carcinoma progression by activating the PI3K/AKT/mTOR pathway. J Transl Med, 2022, 20(1): 212. doi: 10.1186/s12967-022-03416-5.
13.	Chen L, Guo P, He Y, et al. HCC-derived exosomes elicit HCC progression and recurrence by epithelial-mesenchymal transition through MAPK/ERK signalling pathway. Cell Death Dis, 2018, 9(5): 513. doi: 10.1038/s41419-018-0534-9.
14.	Qu Z, Feng J, Pan H, et al. Exosomes derived from HCC cells with different invasion characteristics mediated EMT through TGF-β/Smad signaling pathway. Onco Targets Ther, 2019, 12: 6897-6905.
15.	Peng Z, Hao M, Tong H, et al. The interactions between integrin α5β1 of liver cancer cells and fibronectin of fibroblasts promote tumor growth and angiogenesis. Int J Biol Sci, 2022, 18(13): 5019-5037.
16.	Sun YF, Guo W, Xu Y, et al. Circulating tumor cells from different vascular sites exhibit spatial heterogeneity in epithelial and mesenchymal composition and distinct clinical significance in hepatocellular carcinoma. Clin Cancer Res, 2018, 24(3): 547-559.
17.	Li J, King MR. Adhesion receptors as therapeutic targets for circulating tumor cells. Front Oncol, 2012, 2: 79. doi: 10.3389/fonc.2012.00079.
18.	Liu H, Xu L, He H, et al. Hepatitis B virus X protein promotes hepatoma cell invasion and metastasis by stabilizing Snail protein. Cancer Sci, 2012, 103(12): 2072-2081.
19.	Chen S, Dong Z, Yang P, et al. Hepatitis B virus X protein stimulates high mobility group box 1 secretion and enhances hepatocellular carcinoma metastasis. Cancer Lett, 2017, 394: 22-32.
20.	Xia L, Huang W, Tian D, et al. Upregulated FoxM1 expression induced by hepatitis B virus X protein promotes tumor metastasis and indicates poor prognosis in hepatitis B virus-related hepatocellular carcinoma. J Hepatol, 2012, 57(3): 600-612.
21.	Zhou D, Luan J, Huang C, et al. Tumor-associated macrophages in hepatocellular carcinoma: friend or foe?. Gut Liver, 2021, 15(4): 500-516.
22.	Graham N, Pollard JW. An acid trip activates protumoral macrophages to promote hepatocellular carcinoma malignancy. J Clin Invest, 2022, 132(7): e158562. doi: 10.1172/JCI158562.
23.	Yuan LT, Chang JH, Lee HL, et al. Genetic variants of lncRNA MALAT1 exert diverse impacts on the risk and clinicopathologic characteristics of patients with hepatocellular carcinoma. J Clin Med, 2019, 8(9): 1406. doi: 10.3390/jcm8091406.
24.	Wu S, Zheng Q, Xing X, et al. Matrix stiffness-upregulated LOXL2 promotes fibronectin production, MMP9 and CXCL12 expression and BMDCs recruitment to assist pre-metastatic niche formation. J Exp Clin Cancer Res, 2018, 37(1): 99. doi: 10.1186/s13046-018-0761-z.
25.	Liu G, Sun J, Yang ZF, et al. Cancer-associated fibroblast-derived CXCL11 modulates hepatocellular carcinoma cell migration and tumor metastasis through the circUBAP2/miR-4756/IFIT1/3 axis. Cell Death Dis, 2021, 12(3): 260. doi: 10.1038/s41419-021-03545-7.
26.	Xiang ZW, Sun L, Li GH, et al. Progress in the treatment of pulmonary metastases after liver transplantation for hepatocellular carcinoma. World J Hepatol, 2015, 7(20): 2309-2314.
27.	Lee CY, Bae MK, Park IK, et al. Surgical resection for pulmonary metastasis from hepatocellular carcinoma: analysis of prognosis in relation to primary control. J Surg Oncol, 2010, 101(3): 239-243.
28.	周恺乾, 孙云帆, 杨欣荣, 等. 肝细胞癌 (HCC) 肺转移切除术 (PME) 的预后影响因素分析. 复旦学报 (医学版), 2019, 46(5): 569-575.
29.	Jeong YH, Hwang S, Lee GD, et al. Surgical outcome of pulmonary metastasectomy for hepatocellular carcinoma recurrence in liver transplant patients. Ann Transplant, 2021, 26: e930383. doi: 10.12659/AOT.930383.
30.	Lam CM, Lo CM, Yuen WK, et al. Prolonged survival in selected patients following surgical resection for pulmonary metastasis from hepatocellular carcinoma. Br J Surg, 1998, 85(9): 1198-1200.
31.	张峥, 毛燕君. 多学科团队护理模式在肺癌患者行CT引导下射频消融术围术期的应用效果. 2022SINC第五届上海国际护理大会, 2022.
32.	Lassandro G, Picchi SG, Bianco A, et al. Effectiveness and safety in radiofrequency ablation of pulmonary metastases from HCC: a five years study. Med Oncol, 2020, 37(4): 25. doi: 10.1007/s12032-020-01352-2.
33.	Zuo T, Lin W, Liu F, et al. Artificial pneumothorax improves radiofrequency ablation of pulmonary metastases of hepatocellular carcinoma close to mediastinum. BMC Cancer, 2021, 21(1): 505. doi: 10.1186/s12885-021-08223-7.
34.	Hori A, Ohira R, Nakamura T, et al. Transarterial chemoembolization for pulmonary or mediastinal metastases from hepatocellular carcinoma. Br J Radiol, 2020, 93(1110): 20190407. doi: 10.1259/bjr.20190407.
35.	Zhou TY, Tao GF, Chen SQ, et al. Complete response of hepatocellular carcinoma with macroscopic vascular invasion and pulmonary metastasis to the combination of drug-eluting beads transarterial chemoembolization and huaier granule: a case report. Onco Targets Ther, 2021, 14: 3873-3880.
36.	Fang LJ, Chen LY, Sun JH, et al. Clinical characteristics and outcomes of acute lung injury caused by transcatheter arterial chemoembolization for hepatocellular carcinoma: a retrospective cohort study from a single institution in China. Anal Cell Pathol (Amst), 2019, 2019: 4307651. doi: 10.1155/2019/4307651.
37.	Jiang W, Zeng ZC, Zhang JY, et al. Palliative radiation therapy for pulmonary metastases from hepatocellular carcinoma. Clin Exp Metastasis, 2012, 29(3): 197-205.
38.	Zhang L, Chen LH, Wang J, et al. CT-guided radioactive ¹²⁵I seed implantation treatment of multiple pulmonary metastases of hepatocellular carcinoma. Clin Radiol, 2014, 69(6): 624-629.
39.	Okabe T, Kimura T, Nagata Y. Stereotactic body radiotherapy. Gan To Kagaku Ryoho, 2014, 41(13): 2543-2545.
40.	Xiang Z, Bai M, Li G, et al. Safety and efficacy of ¹²⁵I brachytherapy for bilateral lung recurrences from hepatocellular carcinoma after resection or ablation. J Cancer Res Clin Oncol, 2019, 145(7): 1907-1916.
41.	Yuan Q, Ma Y, Wu L, et al. Clinical outcome of CT-guided iodine-125 radioactive seed implantation for intrahepatic recurrent hepatocellular carcinoma: a retrospective, multicenter study. Front Oncol, 2022, 12: 819934. doi: 10.3389/fonc.2022.819934.
42.	Wang Z, Yang F, Zhao X, et al. Outcome of near-infrared fluorescence-navigated pulmonary metastasectomy for hepatocellular carcinoma. Eur J Cardiothorac Surg, 2022, 62(5): ezac270. doi: 10.1093/ejcts/ezac270.
43.	Lee HP, Yun JK, Jung HS, et al. Surgical outcomes of pulmonary metastasectomy in hepatocellular carcinoma patients according to approach method: thoracoscopic versus open approach. World J Surg Oncol, 2021, 19(1): 33. doi: 10.1186/s12957-021-02138-0.
44.	Oh YJ, Park YM, Kim BH, et al. A case of hepatocellular carcinoma with pulmonary metastases treated successfully with a combination of repeated hepatic arterial infusion epirubicin and Cisplatin chemotherapy and systemic low-dose infusion of 5-Fluorouracil. Gut Liver, 2009, 3(4): 343-348.
45.	Qin S, Kruger E, Tan SC, et al. Cost-effectiveness analysis of FOLFOX4 and sorafenib for the treatment of advanced hepatocellular carcinoma in China. Cost Eff Resour Alloc, 2018, 16: 29. doi: 10.1186/s12962-018-0112-0.
46.	Hasegawa H, Kawakubo E, Kitagawa D, et al. Combined modality therapy for giant hepatocellular carcinoma and multiple lung metastases-a case study. Gan To Kagaku Ryoho, 2020, 47(13): 2251-2253.
47.	Shi J, Sun J, Liu C, et al. All-trans-retinoic acid (ATRA) plus oxaliplatin plus 5-fluorouracil/leucovorin (FOLFOX) versus FOLFOX alone as palliative chemotherapy in patients with advanced hepatocellular carcinoma and extrahepatic metastasis: study protocol for a randomized controlled trial. Trials, 2019, 20(1): 245. doi: 10.1186/s13063-019-3349-9.
48.	Sun J, Liu C, Wang N, et al. All-trans-retinoic acid plus oxaliplatin/fluorouracil/leucovorin for advanced hepatocellular carcinoma with pulmonary metastasis: a multicenter retrospective study. Cancer Manag Res, 2022, 14: 1663-1670.
49.	Takuma K, Fujihara S, Fujita K, et al. Antitumor effect of regorafenib on microRNA expression in hepatocellular carcinoma cell lines. Int J Mol Sci, 2022, 23(3): 1667. doi: 10.3390/ijms23031667.
50.	冯跃, 郑家平, 邵国良. 索拉非尼治疗肝细胞癌肺转移39例预后分析. 肿瘤学杂志, 2018, 24(10): 987-991.
51.	Wada Y, Takami Y, Matsushima H, et al. The safety and efficacy of combination therapy of sorafenib and radiotherapy for advanced hepatocellular carcinoma: a retrospective study. Intern Med, 2018, 57(10): 1345-1353.
52.	尹小兰, 许青. 索拉非尼联合立体定向精确放疗治疗肝癌肺转移疗效观察. 中国临床医学, 2016, 23(5): 618-624.
53.	Yi Y, Han J, Fang Y, et al. Sorafenib and a novel immune therapy in lung metastasis from hepatocellular carcinoma following hepatectomy: a case report. Mol Clin Oncol, 2016, 5(2): 337-341.
54.	Kim HS, Kim CG, Hong JY, et al. The presence and size of intrahepatic tumors determine the therapeutic efficacy of nivolumab in advanced hepatocellular carcinoma. Ther Adv Med Oncol, 2022, 14: 17588359221113266. doi: 10.1177/ 17588359221113266.
55.	Li J, Chen T, Bi F, et al. Efficacy of lenvatinib plus pembrolizumab in hepatocellular carcinoma with metachronous lung metastasis: a report of two cases. Tumori, 2021, 107(6): NP114-NP119.
56.	He X, Peng Y, Zhou Z, et al. Immune checkpoint inhibitor-based systemic therapy shows remarkable curative effect in a hepatocellular carcinoma patient with intractable postoperative recurrence and metastases: a case report and literature review. Front Oncol, 2022, 12: 784224. doi: 10.3389/fonc.2022.784224.
57.	Liu M, Xie L, Zhang Y, et al. Inhibition of CEMIP potentiates the effect of sorafenib on metastatic hepatocellular carcinoma by reducing the stiffness of lung metastases. Cell Death Dis, 2023, 14(1): 25. doi: 10.1038/s41419-023-05550-4.
58.	Sun H, Xing C, Jiang S, et al. Long term complete response of advanced hepatocellular carcinoma to glypican-3 specific chimeric antigen receptor T-Cells plus sorafenib, a case report. Front Immunol, 2022, 13: 963031. doi: 10.3389/fimmu.2022.963031.
59.	Wen J, Huang Z, Wei Y, et al. Hsa-microRNA-27b-3p inhibits hepatocellular carcinoma progression by inactivating transforming growth factor-activated kinase-binding protein 3/nuclear factor kappa B signalling. Cell Mol Biol Lett, 2022, 27(1): 79. doi: 10.1186/s11658-022-00370-4.

1. Uchino K, Tateishi R, Shiina S, et al. Hepatocellular carcinoma with extrahepatic metastasis: clinical features and prognostic factors. Cancer, 2011, 117(19): 4475-4483.
2. Katyal S, Oliver JH 3rd, Peterson MS, et al. Extrahepatic metastases of hepatocellular carcinoma. Radiology, 2000, 216(3): 698-703.
3. Wu C, Ren X, Zhang Q. Incidence, risk factors, and prognosis in patients with primary hepatocellular carcinoma and lung metastasis: a population-based study. Cancer Manag Res, 2019, 11: 2759-2768.
4. Guo X, Xu Y, Wang X, et al. Advanced hepatocellular carcinoma with bone metastases: prevalence, associated factors, and survival estimation. Med Sci Monit, 2019, 25: 1105-1112.
5. Alshahrani AA, Ha SM, Hwang S, et al. Clinical features and surveillance of very late hepatocellular carcinoma recurrence after liver transplantation. Ann Transplant, 2018, 23: 659-665.
6. He Y, Lin Y, He F, et al. Role for calcium-activated potassium channels (BK) in migration control of human hepatocellular carcinoma cells. J Cell Mol Med, 2021, 25(20): 9685-9696.
7. Kaczynski J, Hansson G, Wallerstedt S. Metastases in cases with hepatocellular carcinoma in relation to clinicopathologic features of the tumor. An autopsy study from a low endemic area. Acta Oncol, 1995, 34(1): 43-48.
8. 方东升. 肺转移癌189例临床分析. 河北医学, 2001, 7(11): 1011-1012.
9. Yuki K, Hirohashi S, Sakamoto M, et al. Growth and spread of hepatocellular carcinoma. A review of 240 consecutive autopsy cases. Cancer, 1990, 66(10): 2174-2179.
10. Yang JC, Hu JJ, Li YX, et al. Clinical applications of liquid biopsy in hepatocellular carcinoma. Front Oncol, 2022, 12: 781820. doi: 10.3389/fonc.2022.781820.
11. Ye L, Zhang Q, Cheng Y, et al. Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1⁺ regulatory B cell expansion. J Immunother Cancer, 2018, 6(1): 145. doi: 10.1186/s40425-018-0451-6.
12. Pu Z, Duda DG, Zhu Y, et al. VCP interaction with HMGB1 promotes hepatocellular carcinoma progression by activating the PI3K/AKT/mTOR pathway. J Transl Med, 2022, 20(1): 212. doi: 10.1186/s12967-022-03416-5.
13. Chen L, Guo P, He Y, et al. HCC-derived exosomes elicit HCC progression and recurrence by epithelial-mesenchymal transition through MAPK/ERK signalling pathway. Cell Death Dis, 2018, 9(5): 513. doi: 10.1038/s41419-018-0534-9.
14. Qu Z, Feng J, Pan H, et al. Exosomes derived from HCC cells with different invasion characteristics mediated EMT through TGF-β/Smad signaling pathway. Onco Targets Ther, 2019, 12: 6897-6905.
15. Peng Z, Hao M, Tong H, et al. The interactions between integrin α5β1 of liver cancer cells and fibronectin of fibroblasts promote tumor growth and angiogenesis. Int J Biol Sci, 2022, 18(13): 5019-5037.
16. Sun YF, Guo W, Xu Y, et al. Circulating tumor cells from different vascular sites exhibit spatial heterogeneity in epithelial and mesenchymal composition and distinct clinical significance in hepatocellular carcinoma. Clin Cancer Res, 2018, 24(3): 547-559.
17. Li J, King MR. Adhesion receptors as therapeutic targets for circulating tumor cells. Front Oncol, 2012, 2: 79. doi: 10.3389/fonc.2012.00079.
18. Liu H, Xu L, He H, et al. Hepatitis B virus X protein promotes hepatoma cell invasion and metastasis by stabilizing Snail protein. Cancer Sci, 2012, 103(12): 2072-2081.
19. Chen S, Dong Z, Yang P, et al. Hepatitis B virus X protein stimulates high mobility group box 1 secretion and enhances hepatocellular carcinoma metastasis. Cancer Lett, 2017, 394: 22-32.
20. Xia L, Huang W, Tian D, et al. Upregulated FoxM1 expression induced by hepatitis B virus X protein promotes tumor metastasis and indicates poor prognosis in hepatitis B virus-related hepatocellular carcinoma. J Hepatol, 2012, 57(3): 600-612.
21. Zhou D, Luan J, Huang C, et al. Tumor-associated macrophages in hepatocellular carcinoma: friend or foe?. Gut Liver, 2021, 15(4): 500-516.
22. Graham N, Pollard JW. An acid trip activates protumoral macrophages to promote hepatocellular carcinoma malignancy. J Clin Invest, 2022, 132(7): e158562. doi: 10.1172/JCI158562.
23. Yuan LT, Chang JH, Lee HL, et al. Genetic variants of lncRNA MALAT1 exert diverse impacts on the risk and clinicopathologic characteristics of patients with hepatocellular carcinoma. J Clin Med, 2019, 8(9): 1406. doi: 10.3390/jcm8091406.
24. Wu S, Zheng Q, Xing X, et al. Matrix stiffness-upregulated LOXL2 promotes fibronectin production, MMP9 and CXCL12 expression and BMDCs recruitment to assist pre-metastatic niche formation. J Exp Clin Cancer Res, 2018, 37(1): 99. doi: 10.1186/s13046-018-0761-z.
25. Liu G, Sun J, Yang ZF, et al. Cancer-associated fibroblast-derived CXCL11 modulates hepatocellular carcinoma cell migration and tumor metastasis through the circUBAP2/miR-4756/IFIT1/3 axis. Cell Death Dis, 2021, 12(3): 260. doi: 10.1038/s41419-021-03545-7.
26. Xiang ZW, Sun L, Li GH, et al. Progress in the treatment of pulmonary metastases after liver transplantation for hepatocellular carcinoma. World J Hepatol, 2015, 7(20): 2309-2314.
27. Lee CY, Bae MK, Park IK, et al. Surgical resection for pulmonary metastasis from hepatocellular carcinoma: analysis of prognosis in relation to primary control. J Surg Oncol, 2010, 101(3): 239-243.
28. 周恺乾, 孙云帆, 杨欣荣, 等. 肝细胞癌 (HCC) 肺转移切除术 (PME) 的预后影响因素分析. 复旦学报 (医学版), 2019, 46(5): 569-575.
29. Jeong YH, Hwang S, Lee GD, et al. Surgical outcome of pulmonary metastasectomy for hepatocellular carcinoma recurrence in liver transplant patients. Ann Transplant, 2021, 26: e930383. doi: 10.12659/AOT.930383.
30. Lam CM, Lo CM, Yuen WK, et al. Prolonged survival in selected patients following surgical resection for pulmonary metastasis from hepatocellular carcinoma. Br J Surg, 1998, 85(9): 1198-1200.
31. 张峥, 毛燕君. 多学科团队护理模式在肺癌患者行CT引导下射频消融术围术期的应用效果. 2022SINC第五届上海国际护理大会, 2022.
32. Lassandro G, Picchi SG, Bianco A, et al. Effectiveness and safety in radiofrequency ablation of pulmonary metastases from HCC: a five years study. Med Oncol, 2020, 37(4): 25. doi: 10.1007/s12032-020-01352-2.
33. Zuo T, Lin W, Liu F, et al. Artificial pneumothorax improves radiofrequency ablation of pulmonary metastases of hepatocellular carcinoma close to mediastinum. BMC Cancer, 2021, 21(1): 505. doi: 10.1186/s12885-021-08223-7.
34. Hori A, Ohira R, Nakamura T, et al. Transarterial chemoembolization for pulmonary or mediastinal metastases from hepatocellular carcinoma. Br J Radiol, 2020, 93(1110): 20190407. doi: 10.1259/bjr.20190407.
35. Zhou TY, Tao GF, Chen SQ, et al. Complete response of hepatocellular carcinoma with macroscopic vascular invasion and pulmonary metastasis to the combination of drug-eluting beads transarterial chemoembolization and huaier granule: a case report. Onco Targets Ther, 2021, 14: 3873-3880.
36. Fang LJ, Chen LY, Sun JH, et al. Clinical characteristics and outcomes of acute lung injury caused by transcatheter arterial chemoembolization for hepatocellular carcinoma: a retrospective cohort study from a single institution in China. Anal Cell Pathol (Amst), 2019, 2019: 4307651. doi: 10.1155/2019/4307651.
37. Jiang W, Zeng ZC, Zhang JY, et al. Palliative radiation therapy for pulmonary metastases from hepatocellular carcinoma. Clin Exp Metastasis, 2012, 29(3): 197-205.
38. Zhang L, Chen LH, Wang J, et al. CT-guided radioactive ¹²⁵I seed implantation treatment of multiple pulmonary metastases of hepatocellular carcinoma. Clin Radiol, 2014, 69(6): 624-629.
39. Okabe T, Kimura T, Nagata Y. Stereotactic body radiotherapy. Gan To Kagaku Ryoho, 2014, 41(13): 2543-2545.
40. Xiang Z, Bai M, Li G, et al. Safety and efficacy of ¹²⁵I brachytherapy for bilateral lung recurrences from hepatocellular carcinoma after resection or ablation. J Cancer Res Clin Oncol, 2019, 145(7): 1907-1916.
41. Yuan Q, Ma Y, Wu L, et al. Clinical outcome of CT-guided iodine-125 radioactive seed implantation for intrahepatic recurrent hepatocellular carcinoma: a retrospective, multicenter study. Front Oncol, 2022, 12: 819934. doi: 10.3389/fonc.2022.819934.
42. Wang Z, Yang F, Zhao X, et al. Outcome of near-infrared fluorescence-navigated pulmonary metastasectomy for hepatocellular carcinoma. Eur J Cardiothorac Surg, 2022, 62(5): ezac270. doi: 10.1093/ejcts/ezac270.
43. Lee HP, Yun JK, Jung HS, et al. Surgical outcomes of pulmonary metastasectomy in hepatocellular carcinoma patients according to approach method: thoracoscopic versus open approach. World J Surg Oncol, 2021, 19(1): 33. doi: 10.1186/s12957-021-02138-0.
44. Oh YJ, Park YM, Kim BH, et al. A case of hepatocellular carcinoma with pulmonary metastases treated successfully with a combination of repeated hepatic arterial infusion epirubicin and Cisplatin chemotherapy and systemic low-dose infusion of 5-Fluorouracil. Gut Liver, 2009, 3(4): 343-348.
45. Qin S, Kruger E, Tan SC, et al. Cost-effectiveness analysis of FOLFOX4 and sorafenib for the treatment of advanced hepatocellular carcinoma in China. Cost Eff Resour Alloc, 2018, 16: 29. doi: 10.1186/s12962-018-0112-0.
46. Hasegawa H, Kawakubo E, Kitagawa D, et al. Combined modality therapy for giant hepatocellular carcinoma and multiple lung metastases-a case study. Gan To Kagaku Ryoho, 2020, 47(13): 2251-2253.
47. Shi J, Sun J, Liu C, et al. All-trans-retinoic acid (ATRA) plus oxaliplatin plus 5-fluorouracil/leucovorin (FOLFOX) versus FOLFOX alone as palliative chemotherapy in patients with advanced hepatocellular carcinoma and extrahepatic metastasis: study protocol for a randomized controlled trial. Trials, 2019, 20(1): 245. doi: 10.1186/s13063-019-3349-9.
48. Sun J, Liu C, Wang N, et al. All-trans-retinoic acid plus oxaliplatin/fluorouracil/leucovorin for advanced hepatocellular carcinoma with pulmonary metastasis: a multicenter retrospective study. Cancer Manag Res, 2022, 14: 1663-1670.
49. Takuma K, Fujihara S, Fujita K, et al. Antitumor effect of regorafenib on microRNA expression in hepatocellular carcinoma cell lines. Int J Mol Sci, 2022, 23(3): 1667. doi: 10.3390/ijms23031667.
50. 冯跃, 郑家平, 邵国良. 索拉非尼治疗肝细胞癌肺转移39例预后分析. 肿瘤学杂志, 2018, 24(10): 987-991.
51. Wada Y, Takami Y, Matsushima H, et al. The safety and efficacy of combination therapy of sorafenib and radiotherapy for advanced hepatocellular carcinoma: a retrospective study. Intern Med, 2018, 57(10): 1345-1353.
52. 尹小兰, 许青. 索拉非尼联合立体定向精确放疗治疗肝癌肺转移疗效观察. 中国临床医学, 2016, 23(5): 618-624.
53. Yi Y, Han J, Fang Y, et al. Sorafenib and a novel immune therapy in lung metastasis from hepatocellular carcinoma following hepatectomy: a case report. Mol Clin Oncol, 2016, 5(2): 337-341.
54. Kim HS, Kim CG, Hong JY, et al. The presence and size of intrahepatic tumors determine the therapeutic efficacy of nivolumab in advanced hepatocellular carcinoma. Ther Adv Med Oncol, 2022, 14: 17588359221113266. doi: 10.1177/ 17588359221113266.
55. Li J, Chen T, Bi F, et al. Efficacy of lenvatinib plus pembrolizumab in hepatocellular carcinoma with metachronous lung metastasis: a report of two cases. Tumori, 2021, 107(6): NP114-NP119.
56. He X, Peng Y, Zhou Z, et al. Immune checkpoint inhibitor-based systemic therapy shows remarkable curative effect in a hepatocellular carcinoma patient with intractable postoperative recurrence and metastases: a case report and literature review. Front Oncol, 2022, 12: 784224. doi: 10.3389/fonc.2022.784224.
57. Liu M, Xie L, Zhang Y, et al. Inhibition of CEMIP potentiates the effect of sorafenib on metastatic hepatocellular carcinoma by reducing the stiffness of lung metastases. Cell Death Dis, 2023, 14(1): 25. doi: 10.1038/s41419-023-05550-4.
58. Sun H, Xing C, Jiang S, et al. Long term complete response of advanced hepatocellular carcinoma to glypican-3 specific chimeric antigen receptor T-Cells plus sorafenib, a case report. Front Immunol, 2022, 13: 963031. doi: 10.3389/fimmu.2022.963031.
59. Wen J, Huang Z, Wei Y, et al. Hsa-microRNA-27b-3p inhibits hepatocellular carcinoma progression by inactivating transforming growth factor-activated kinase-binding protein 3/nuclear factor kappa B signalling. Cell Mol Biol Lett, 2022, 27(1): 79. doi: 10.1186/s11658-022-00370-4.

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Research progress of hepatocellular carcinoma with lung metastasis

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