Annals of Surgical Oncology

, Volume 26, Issue 5, pp 1465–1473 | Cite as

Postoperative Adjuvant Transarterial Chemoembolization Improves Outcomes of Hepatocellular Carcinoma Associated with Hepatic Vein Invasion: A Propensity Score Matching Analysis

  • Xiu-Ping Zhang
  • Yan-Chen Liu
  • Zhen-Hua Chen
  • Ju-Xian Sun
  • Kang Wang
  • Zong-Tao Chai
  • Jie Shi
  • Wei-Xing Guo
  • Meng-Chao Wu
  • Wan Yee Lau
  • Shu-Qun ChengEmail author
Hepatobiliary Tumors



Vascular invasion is a major determinant of survival outcomes after curative resection for hepatocellular carcinoma (HCC) patients. This study was designed to investigate the efficacy of postoperative adjuvant transarterial chemoembolization (PA-TACE) in patients with HCC with hepatic vein tumor thrombus (HVTT).


Data from patients who underwent LR for HCC with HVTT at the Eastern Hepatobiliary Surgery Hospital were retrospectively analyzed. The survival outcomes for patients who underwent PA-TACE after LR were compared with those who underwent LR alone. Propensity score matching (PSM) analysis was performed to match patients in a ratio of 1:1.


All included 319 patients who underwent LR for HCC with HVTT, 134 underwent LR alone (the LR group), and 185 patients underwent in adjuvant TACE (the PA-TACE group). PSM matched 107 patients in two groups. The overall survival (OS) and recurrence-free survival (RFS) were significantly better for patients in the PA-TACE group than the LR group (for OS: before PSM, P < 0.001; after PSM, P = 0.004; for RFS: before PSM, P < 0.001; after PSM, P = 0.013), respectively. On subgroup analysis, equivalent acceptable results were obtained in patients with peripheral HVTT (pHVTT) and major HVTT (mHVTT). However, PA-TACE resulted in no survival benefits for patients when the HVTT had extended to the inferior vena cava (IVCTT).


PA-TACE was associated with significantly better survival outcomes than LR alone for patients with HCC and HVTT (pHVTT and mHVTT). There was no survival benefits in patients whose HVTT had extended to form IVCTT.


Authors contributions

Conception and design: Shu-Qun Cheng, Wan Yee Lau, Xiu-Ping Zhang; Financial support: Shu-Qun Cheng; Provision of study materials or patients: Ju-Xian Sun, Kang Wang, Zong-Tao Chai, Jie Shi, Wei-Xing Guo, Meng-Chao Wu; Collection and assembly of data: Xiu-Ping Zhang, Yan-Chen Liu, Zhen-Hua Chen; Data analysis and interpretation: Xiu-Ping Zhang, Yan-Chen Liu, Zhen-Hua Chen; Manuscript writing: Xiu-Ping Zhang, Wan Yee Lau; Final approval of manuscript: All authors.


This work was supported by the Key Project of the Natural Science Foundation of China (No: 81730097); grants from the Science Fund for Creative Research Groups (No: 81521091); the Chang Jiang Scholars Programme (2013) of China Ministry of Education; the National Key Basic Research Programme “973 project” (No: 2015CB554000); the National Natural Science Foundation of China (No: 81602523), Shanghai Municipal Health Bureau (No: SHDC12015106); and Shanghai Science and Technology Committee (No: 134119a0200).


No potential conflicts of interest.

Supplementary material

10434_2019_7223_MOESM1_ESM.doc (1 mb)
Supplementary material 1 (DOC 1056 kb)


  1. 1.
    Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Can J Clin. 2015;65(2):87–108.CrossRefGoogle Scholar
  2. 2.
    Marrero JA, Kulik LM, Sirlin C, et al. Diagnosis, staging and management of hepatocellular carcinoma: 2018 Practice Guidance by the American Association for the Study of Liver Diseases. Hepatology. 2018;68(2):723–750.CrossRefGoogle Scholar
  3. 3.
    Bruix J, Reig M, Sherman M. Evidence-based diagnosis, staging, and treatment of patients with hepatocellular carcinoma. Gastroenterology. 2016;150(4):835–53.CrossRefGoogle Scholar
  4. 4.
    Aldrighetti L, Pulitano C, Catena M, et al. Liver resection with portal vein thrombectomy for hepatocellular carcinoma with vascular invasion. Ann Surg Oncol. 2009;16(5):1254.CrossRefGoogle Scholar
  5. 5.
    Lu XJ, Dong J, Ji LJ, et al. Safety and efficacy of TACE and gamma knife on hepatocellular carcinoma with portal vein invasion. Gut. 2016;65(4):715–6.CrossRefGoogle Scholar
  6. 6.
    Forner A, Llovet JM, Bruix J. Hepatocellular carcinoma. Lancet. 2012;379(9822):1245–55.CrossRefGoogle Scholar
  7. 7.
    Kokudo T, Hasegawa K, Yamamoto S, et al. Surgical treatment of hepatocellular carcinoma associated with hepatic vein tumor thrombosis. J Hepatol. 2014;61(3):583–8.CrossRefGoogle Scholar
  8. 8.
    Kokudo T, Hasegawa K, Matsuyama Y, et al. Liver resection for hepatocellular carcinoma associated with hepatic vein invasion: a Japanese nationwide survey. Hepatology. 2017;66(2):510–7.CrossRefGoogle Scholar
  9. 9.
    Kokudo T, Hasegawa K, Matsuyama Y, et al. Survival benefit of liver resection for hepatocellular carcinoma associated with portal vein invasion. J Hepatol. 2016;65(5):938–43.CrossRefGoogle Scholar
  10. 10.
    Wang K, Guo WX, Chen MS, et al. Multimodality treatment for hepatocellular carcinoma with portal vein tumor thrombus: a large-scale, multicenter, propensity mathching score analysis. Medicine. 2016;95(11):e3015.CrossRefGoogle Scholar
  11. 11.
    Zhang XP, Wang K, Chen ZH, Cheng SQ. Hepatocellular carcinoma with hepatic vein invasion should not be considered a contraindication for liver resection. Hepatology. 2017;67(2):804–805.CrossRefGoogle Scholar
  12. 12.
    Lee JM, Jang BK, Lee YJ, et al. Survival outcomes of hepatic resection compared with transarterial chemoembolization or sorafenib for hepatocellular carcinoma with portal vein tumor thrombosis. Clin Mol Hepatol. 2016;22(1):160–7.CrossRefGoogle Scholar
  13. 13.
    Shaohua L, Qiaoxuan W, Peng S, et al. Surgical strategy for hepatocellular carcinoma patients with portal/hepatic vein tumor thrombosis. PloS ONE. 2015;10(6):e0130021.CrossRefGoogle Scholar
  14. 14.
    Itoh A, Sadamori H, Yabushita K, et al. Advanced hepatocellular carcinoma with hepatic vein tumor thrombosis and renal dysfunction after hepatic arterial infusion chemotherapy effectively treated by liver resection with active veno-venous bypass: report of a case. BMC Cancer 2016;16:705.CrossRefGoogle Scholar
  15. 15.
    Hyun MH, Lee YS, Kim JH, et al. Hepatic resection compared to chemoembolization in intermediate- to advanced-stage hepatocellular carcinoma: a meta-analysis of high-quality studies. Hepatology. 2018;68(3):977–993.CrossRefGoogle Scholar
  16. 16.
    Tong Y, Li Z, Liang Y, et al. Postoperative adjuvant TACE for patients of hepatocellular carcinoma in AJCC stage I: friend or foe? a propensity score analysis. Oncotarget. 2017;8(16):26671–8.CrossRefGoogle Scholar
  17. 17.
    Wang Z, Ren Z, Chen Y, et al. Adjuvant transarterial chemoembolization for hbv-related hepatocellular carcinoma after resection: a randomized controlled study. Clin Cancer Res. 2018;24(9):2074–81.CrossRefGoogle Scholar
  18. 18.
    Liu S, Guo L, Li H, et al. Postoperative adjuvant trans-arterial chemoembolization for patients with hepatocellular carcinoma and portal vein tumor thrombus. Ann Surg Oncol. 2018;25(7):2098–104.CrossRefGoogle Scholar
  19. 19.
    Peng ZW, Guo RP, Zhang YJ, Lin XJ, Chen MS, Lau WY. Hepatic resection versus transcatheter arterial chemoembolization for the treatment of hepatocellular carcinoma with portal vein tumor thrombus. Cancer. 2012;118(19):4725–36.CrossRefGoogle Scholar
  20. 20.
    Zhang YF, Wei W, Guo ZX, Wang JH, Shi M, Guo RP. Hepatic resection versus transcatheter arterial chemoembolization for the treatment of hepatocellular carcinoma with hepatic vein tumor thrombus. Japanese J Clin Oncol. 2015;45(9):837–43.CrossRefGoogle Scholar
  21. 21.
    Wang Y, Yuan L, Ge RL, Sun Y, Wei G. Survival benefit of surgical treatment for hepatocellular carcinoma with inferior vena cava/right atrium tumor thrombus: results of a retrospective cohort study. Ann Surg Oncol. 2013;20(3):914–22.CrossRefGoogle Scholar
  22. 22.
    Sun JJ, Wang K, Zhang CZ, et al. Postoperative adjuvant transcatheter arterial chemoembolization after R0 hepatectomy improves outcomes of patients who have hepatocellular carcinoma with microvascular invasion. Ann Surg Oncol. 2016;23(4):1344–51.CrossRefGoogle Scholar
  23. 23.
    Wang K, Guo W, Li N, et al. Alpha-1-fucosidase as a prognostic indicator for hepatocellular carcinoma following hepatectomy: a large-scale, long-term study. Br J Cancer. 2014;110(7):1811–19.CrossRefGoogle Scholar
  24. 24.
    Zhang YF, Wei W, Wang JH, et al. Transarterial chemoembolization combined with sorafenib for the treatment of hepatocellular carcinoma with hepatic vein tumor thrombus. OncoTargets Ther. 2016;9:4239–46.CrossRefGoogle Scholar
  25. 25.
    Fleming CJ, Andrews JC, Wiseman GA, Gansen DN, Roberts LR. Hepatic vein tumor thrombus as a risk factor for excessive pulmonary deposition of microspheres during TheraSphere therapy for unresectable hepatocellular carcinoma. J Vasc Interv Radiol. 2009;20(11):1460–3.CrossRefGoogle Scholar
  26. 26.
    Kim HC, Lee JH, Chung JW, et al. Transarterial chemoembolization with additional cisplatin infusion for hepatocellular carcinoma invading the hepatic vein. J Vasc Interv Radiol. 2013;24(2):274–83.CrossRefGoogle Scholar
  27. 27.
    Jiang C, Wang Z, Xu Q, Wu X, Ding Y. Inferior right hepatic vein-preserving major right hepatectomy for hepatocellular carcinoma in patients with significant fibrosis or cirrhosis. World J Surg. 2014;38(1):159–67.CrossRefGoogle Scholar
  28. 28.
    Zhang T, Huang JW, Bai YN, Wu H, Zeng Y. Recurrence and survivals following hepatic resection for hepatocellular carcinoma with major portal/hepatic vein tumor thrombus. Hepatol Res. 2014;44(7):761–8.CrossRefGoogle Scholar
  29. 29.
    Ye JZ, Chen JZ, Li ZH, et al. Efficacy of postoperative adjuvant transcatheter arterial chemoembolization in hepatocellular carcinoma patients with microvascular invasion. World J Gastroenterol. 2017;23(41):7415–24.CrossRefGoogle Scholar
  30. 30.
    Pesi B, Ferrero A, Grazi GL, et al. Liver resection with thrombectomy as a treatment of hepatocellular carcinoma with major vascular invasion: results from a retrospective multicentric study. Am J Surg. 2015;210(1):35–44.CrossRefGoogle Scholar
  31. 31.
    Biolato M, Marrone G, Racco S, et al. Transarterial chemoembolization (TACE) for unresectable HCC: a new life begins? Eur Rev Med Pharm Sci. 2010;14(4):356–62.Google Scholar
  32. 32.
    Ke-Wei L, Tian-Fu W, Xi L, et al. The effect of postoperative TACE on prognosis of HCC with microscopic venous invasion. Hepato-gastroenterology. 2012;59(118):1944–6.Google Scholar
  33. 33.
    Lencioni R, Llovet JM, Han G, et al. Sorafenib or placebo plus TACE with doxorubicin-eluting beads for intermediate stage HCC: The SPACE trial. J Hepatol. 2016;64(5):1090–8.CrossRefGoogle Scholar
  34. 34.
    Roayaie S. TACE vs. surgical resection for BCLC stage B HCC. J Hepatol. 2014;61(1):3–4.CrossRefGoogle Scholar
  35. 35.
    Klompenhouwer EG, Dresen RC, Verslype C, et al. Transarterial radioembolization following chemoembolization for unresectable hepatocellular carcinoma: response based on apparent diffusion coefficient change is an independent predictor for survival. Cardiovasc Interv Radiol. 2018.Google Scholar
  36. 36.
    Guo T, Wu P, Liu P, et al. Identifying the best anticancer agent combination in TACE for HCC patients: a network meta-analysis. J Cancer. 2018;9(15):2640–9.CrossRefGoogle Scholar
  37. 37.
    Weiss KE, Sze DY, Rangaswami AA, et al. Transarterial chemoembolization in children to treat unresectable hepatocellular carcinoma. Pediatric Transpl. 2018;22(4):e13187.CrossRefGoogle Scholar
  38. 38.
    Kirstein MM, Voigtlander T, Schweitzer N, et al. Transarterial chemoembolization versus sorafenib in patients with hepatocellular carcinoma and extrahepatic disease. United Eur Gastroenterol J. 2018;6(2):238–46.CrossRefGoogle Scholar
  39. 39.
    Leng JJ, Xu YZ, Dong JH. Efficacy of transarterial chemoembolization for hepatocellular carcinoma with portal vein thrombosis: a meta-analysis. ANZ J Surg. 2016;86(10):816–20.CrossRefGoogle Scholar
  40. 40.
    Zhao Y, Duran R, Chapiro J, et al. Transarterial chemoembolization for the treatment of advanced-stage hepatocellular carcinoma. J Gastrointest Surg. 2016;20(12):2002–9.CrossRefGoogle Scholar
  41. 41.
    Zhang XP, Wang K, Li N, et al. Survival benefit of hepatic resection versus transarterial chemoembolization for hepatocellular carcinoma with portal vein tumor thrombus: a systematic review and meta-analysis. BMC Cancer. 2017;17(1):902.CrossRefGoogle Scholar
  42. 42.
    Takano M, Kokudo T, Miyazaki Y, et al. Complete response with sorafenib and transcatheter arterial chemoembolization in unresectable hepatocellular carcinoma. World J Gastroenterol. 2016;22(42):9445–50.CrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2019

Authors and Affiliations

  • Xiu-Ping Zhang
    • 1
  • Yan-Chen Liu
    • 1
    • 3
  • Zhen-Hua Chen
    • 1
  • Ju-Xian Sun
    • 1
  • Kang Wang
    • 1
  • Zong-Tao Chai
    • 1
  • Jie Shi
    • 1
  • Wei-Xing Guo
    • 1
  • Meng-Chao Wu
    • 1
  • Wan Yee Lau
    • 1
    • 2
  • Shu-Qun Cheng
    • 1
    Email author
  1. 1.Department of Hepatic Surgery VI, Eastern Hepatobiliary Surgery HospitalSecond Military Medical UniversityShanghaiChina
  2. 2.Faculty of MedicineThe Chinese University of Hong KongShatinChina
  3. 3.Basic Medical CollegeSecond Military Medical UniversityShanghaiChina

Personalised recommendations