Ann Hepatobiliary Pancreat Surg.  2024 May;28(2):134-143. 10.14701/ahbps.24-048.

Surgical outcome and risk scoring to predict survival after hepatic resection for hepatocellular carcinoma with portal vein tumor thrombosis

• Kim TS
• Yang K
• Choi GH
• Yang HY
• Kim DS
• Jo HS
• Choi GS
• Kim KW
• Yoon YC
• Han J
• Kim DJ
• Hwang S
• Kang KJ

• KMID: 2555926
• DOI: http://doi.org/10.14701/ahbps.24-048

Abstract

Backgrounds/Aims
The hepatocellular carcinoma (HCC) with portal vein tumor thrombosis (PVTT) is classified as the advanced stage (BCLC stage C) with extremely poor prognosis, and in current guidelines is recommended for systemic therapy. This study aimed to evaluate the surgical outcomes and long-term prognosis after hepatic resection (HR) for patients who have HCC combined with PVTT.
Methods
We retrospectively analyzed 332 patients who underwent HR for HCC with PVTT at ten tertiary referral hospitals in South Korea.
Results
The median overall and recurrence-free survival after HR were 32.4 and 8.6 months, while the 1-, 3-, and 5-year overall survival rates were 75%, 48%, and 39%, respectively. In multivariate analysis, tumor number, tumor size, AFP, PIVKA−II, neutrophil-to-lymphocyte ratio, and albumin–bilirubin (ALBI) grade were significant prognostic factors. The risk scoring was developed using these seven factors–tumor, inflammation and hepatic function (TIF), to predict patient prognosis. The prognosis of the patients was well stratified according to the scores (log-rank test, p < 0.001).
Conclusions
HR for patients who have HCC combined with PVTT provided favorable survival outcomes. The risk scoring was useful in predicting prognosis, and determining the appropriate treatment strategy for those patients who have HCC with PVTT.

Keyword

Hepatocellular carcinoma; Tumor thrombosis; Portal vein; Hepatectomy; Prognosis

Figure

• 

  Fig. 1 OS and RFS curves of patients undergoing hepatic resection for hepatocellular carcinoma with portal vein tumor thrombosis. (A) OS curve. For the entire cohort of 332 patients, the 1-, 3-, and 5-year OS rates were 75%, 48%, and 39%, respectively. (B) The 1-, 3-, and 5-year RFS rates were 45%, 34%, and 28%, respectively. OS, overall survival; RFS, recurrence-free survival.

• 

  Fig. 2 RFS and OS curves of patients undergoing hepatic resection for hepatocellular carcinoma with portal vein tumor thrombosis according to the risk group by the TIF scoring system. (A) OS curve. The 1-, 3-, and 5-year OS in the low-risk group was 88%, 63%, and 54%; in the intermediate-risk group, 71%, 42%, and 35%; and in the high-risk group, 50%, 20%, and 15%, respectively (log-rank p < 0.05) for all comparisons. (B) RFS curve. The 1-, 3-, and 5-year RFS in the low-risk group was 60%, 48%, and 43%; in the intermediate-risk group, 40%, 28%, and 25%; and in the high-risk group, 11%, 6%, and 3%, respectively (log-rank p < 0.05, for all comparisons). OS, overall survival; RFS, recurrence-free survival.

• 

  Fig. 3 Overall and RFSs of patients undergoing hepatic resection for hepatocellular carcinoma with portal vein tumor thrombosis at different grades according to the risk group by the TIF scoring system. (A) The Vp1/2 subgroup showed better OS and RFS than the Vp3/4 subgroup. (B) The OS and RFS of the three different risk groups of patients with Vp1/2. In the Vp1/2 group, both OS and RFS were significantly different between the risk groups. (C) Significant differences in OS and RFS between the risk groups in the Vp3/4 group. The Vp3/4 group showed significant differences in OS among the risk groups. The RFS values in the low-risk and intermediate-risk groups were also significantly different from that in the high-risk group (p < 0.001), but the difference in RFS between the low-risk and intermediate-risk groups was not significant (p = 0.165). OS, overall survival; RFS, recurrence-free survival; Vp, portal vein tumor thrombosis.

Reference

References

1. Ikai I, Arii S, Kojiro M, Ichida T, Makuuchi M, Matsuyama Y, et al. 2004; Reevaluation of prognostic factors for survival after liver resection in patients with hepatocellular carcinoma in a japanese nationwide survey. Cancer. 101:796–802. DOI: 10.1002/cncr.20426. PMID: 15305412.

2. Minagawa M, Makuuchi M. 2006; Treatment of hepatocellular carcinoma accompanied by portal vein tumor thrombus. World J Gastroenterol. 12:7561–7567. DOI: 10.3748/wjg.v12.i47.7561. PMID: 17171782. PMCID: PMC4088035.

3. Reig M, Forner A, Rimola J, Ferrer-Fabrega J, Burrel M, Garcia-Criado Á, et al. 2022; Bclc strategy for prognosis prediction and treatment recommendation: the 2022 update. J Hepatol. 76:681–693. DOI: 10.1016/j.jhep.2021.11.018. PMID: 34801630. PMCID: PMC8866082.

4. Omata M, Lesmana LA, Tateishi R, Chen PJ, Lin SM, Yoshida H, et al. 2010; Asian Pacific Association for the Study of the Liver consensus recommendations on hepatocellular carcinoma. Hepatol Int. 4:439–474. DOI: 10.1007/s12072-010-9165-7. PMID: 20827404. PMCID: PMC2900561.

5. Peng ZW, Guo RP, Zhang YJ, Lin XJ, Chen MS, Lau WY. 2012; Hepatic resection versus transcatheter arterial chemoembolization for the treatment of hepatocellular carcinoma with portal vein tumor thrombus. Cancer. 118:4725–4736. DOI: 10.1002/cncr.26561. PMID: 22359112.

6. Kokudo T, Hasegawa K, Matsuyama Y, Takayama T, Izumi N, Kadoya M, et al. 2016; Survival benefit of liver resection for hepatocellular carcinoma associated with portal vein invasion. J Hepatol. 65:938–943. DOI: 10.1016/j.jhep.2016.05.044. PMID: 27266618.

7. Lee JM, Jang BK, Lee YJ, Choi WY, Choi SM, Chung WJ, et al. 2016; Survival outcomes of hepatic resection compared with transarterial chemoembolization or sorafenib for hepatocellular carcinoma with portal vein tumor thrombosis. Clin Mol Hepatol. 22:160–167. DOI: 10.3350/cmh.2016.22.1.160. PMID: 27044767. PMCID: PMC4825165.

8. Hatano E, Uemoto S, Yamaue H, Yamamoto M. Japanese Society of Hepato-Biliary-Pancreatic S. 2018; Significance of hepatic resection and adjuvant hepatic arterial infusion chemotherapy for hepatocellular carcinoma with portal vein tumor thrombus in the first branch of portal vein and the main portal trunk: a project study for hepatic surgery of the japanese society of hepato-biliary-pancreatic surgery. J Hepatobiliary Pancreat Sci. 25:395–402. DOI: 10.1002/jhbp.574. PMID: 30091239.

9. Zhang ZY, Dong KS, Zhang EL, Zhang LW, Chen XP, Dong HH. 2019; Resection might be a meaningful choice for hepatocellular carcinoma with portal vein thrombosis: a systematic review and meta-analysis. Medicine (Baltimore). 98:e18362. DOI: 10.1097/MD.0000000000018362. PMID: 31852141. PMCID: PMC6922393.

10. Chok KS, Cheung TT, Chan SC, Poon RT, Fan ST, Lo CM. 2014; Surgical outcomes in hepatocellular carcinoma patients with portal vein tumor thrombosis. World J Surg. 38:490–496. DOI: 10.1007/s00268-013-2290-4. PMID: 24132826.

11. Kudo M, Kitano M, Sakurai T, Nishida N. 2015; General rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: the outstanding achievements of the liver cancer study group of Japan. Dig Dis. 33:765–770. DOI: 10.1159/000439101. PMID: 26488173.

12. Malik HZ, Prasad KR, Halazun KJ, Aldoori A, Al-Mukhtar A, Gomez D, et al. 2007; Preoperative prognostic score for predicting survival after hepatic resection for colorectal liver metastases. Ann Surg. 246:806–814. DOI: 10.1097/SLA.0b013e318142d964. PMID: 17968173.

13. Halazun KJ, Najjar M, Abdelmessih RM, Samstein B, Griesemer AD, Guarrera JV, et al. 2017; Recurrence after liver transplantation for hepatocellular carcinoma: a new moral to the story. Ann Surg. 265:557–564. DOI: 10.1097/SLA.0000000000001966. PMID: 27611615.

14. Wei Z, Zhao J, Bi X, Zhang Y, Zhou J, Li Z, et al. 2022; Neoadjuvant radiotherapy for resectable hepatocellular carcinoma with portal vein tumor thrombus: a systematic review. Hepatobiliary Surg Nutr. 11:709–717. DOI: 10.21037/hbsn-20-854. PMID: 36268237. PMCID: PMC9577988.

15. Famularo S, Donadon M, Cipriani F, Giuliante F, Ferri S, Celsa C, et al. 2022; Hepatectomy versus sorafenib in advanced nonmetastatic hepatocellular carcinoma: a real-life multicentric weighted comparison. Ann Surg. 275:743–752. DOI: 10.1097/SLA.0000000000005373. PMID: 35081572.

16. Komatsu S, Ueshima K, Kido M, Kuramitsu K, Tsugawa D, Yanagimoto H, et al. 2023; Hepatectomy versus sorafenib for advanced hepatocellular carcinoma with macroscopic portal vein tumor thrombus: a bi-institutional propensity-matched cohort study. J Hepatobiliary Pancreat Sci. 30:303–314. DOI: 10.1002/jhbp.1236. PMID: 36047804.

17. Tsilimigras DI, Bagante F, Moris D, Hyer JM, Sahara K, Paredes AZ, et al. 2020; Recurrence patterns and outcomes after resection of hepatocellular carcinoma within and beyond the barcelona clinic liver cancer criteria. Ann Surg Oncol. 27:2321–2331. DOI: 10.1245/s10434-020-08452-3. PMID: 32285278.

18. Konishi M, Ryu M, Kinoshita T, Inoue K. 2001; Surgical treatment of hepatocellular carcinoma with direct removal of the tumor thrombus in the main portal vein. Hepatogastroenterology. 48:1421–1424.

19. Pawlik TM, Poon RT, Abdalla EK, Ikai I, Nagorney DM, Belghiti J, et al. 2005; Hepatectomy for hepatocellular carcinoma with major portal or hepatic vein invasion: results of a multicenter study. Surgery. 137:403–410. DOI: 10.1016/j.surg.2004.12.012. PMID: 15800485.

20. Kondo K, Chijiiwa K, Kai M, Otani K, Nagaike K, Ohuchida J, et al. 2009; Surgical strategy for hepatocellular carcinoma patients with portal vein tumor thrombus based on prognostic factors. J Gastrointest Surg. 13:1078–1083. DOI: 10.1007/s11605-009-0854-2. PMID: 19296182.

21. Ikai I, Hatano E, Hasegawa S, Fujii H, Taura K, Uyama N, et al. 2006; Prognostic index for patients with hepatocellular carcinoma combined with tumor thrombosis in the major portal vein. J Am Coll Surg. 202:431–438. DOI: 10.1016/j.jamcollsurg.2005.11.012. PMID: 16500247.

22. Le Treut YP, Hardwigsen J, Ananian P, Saïsse J, Grégoire E, Richa H, et al. 2006; Resection of hepatocellular carcinoma with tumor thrombus in the major vasculature. A European case-control series. J Gastrointest Surg. 10:855–862. DOI: 10.1016/j.gassur.2005.12.011. PMID: 16769542.

23. Cheng AL, Qin S, Ikeda M, Galle PR, Ducreux M, Kim TY, et al. 2022; Updated efficacy and safety data from IMbrave150: atezolizumab plus bevacizumab vs. sorafenib for unresectable hepatocellular carcinoma. J Hepatol. 76:862–873. DOI: 10.1016/j.jhep.2021.11.030. PMID: 34902530.

24. Abou-Alfa GK, Chan SL, Kudo M, Lau G, Kelley RK, Furuse J, et al. 2022; Phase 3 randomized, open-label, multicenter study of tremelimumab (T) and durvalumab (D) as first-line therapy in patients (PTS) with unresectable hepatocellular carcinoma (uHCC): Himalaya. JCO. 40:379. DOI: 10.1200/JCO.2022.40.4_suppl.379.

25. Hwang S, Lee YJ, Kim KH, Ahn CS, Moon DB, Ha TY, et al. 2015; Long-term outcome after resection of huge hepatocellular carcinoma ≥ 10 cm: single-institution experience with 471 patients. World J Surg. 39:2519–2528. DOI: 10.1007/s00268-015-3129-y. PMID: 26126423.

26. Jiang JF, Lao YC, Yuan BH, Yin J, Liu X, Chen L, et al. 2017; Treatment of hepatocellular carcinoma with portal vein tumor thrombus: advances and challenges. Oncotarget. 8:33911–33921. DOI: 10.18632/oncotarget.15411. PMID: 28430610. PMCID: PMC5464922.

27. Wang HL, Cucchetti A, Zhong JH, Ye XP, Gu JH, Ma L, et al. 2016; Should hepatic resection be recommended to patients with hepatocellular carcinoma and portal vein invasion? J Hepatol. 65:1057–1058. DOI: 10.1016/j.jhep.2016.07.022. PMID: 27475616.

28. Liang L, Chen TH, Li C, Xing H, Han J, Wang MD, et al. 2018; A systematic review comparing outcomes of surgical resection and non-surgical treatments for patients with hepatocellular carcinoma and portal vein tumor thrombus. HPB (Oxford). 20:1119–1129. DOI: 10.1016/j.hpb.2018.06.1804. PMID: 30056066.

29. Zhang XP, Wang K, Li N, Zhong CQ, Wei XB, Cheng YQ, et al. 2017; Survival benefit of hepatic resection versus transarterial chemoembolization for hepatocellular carcinoma with portal vein tumor thrombus: a systematic review and meta-analysis. BMC Cancer. 17:902. DOI: 10.1186/s12885-017-3895-z. PMID: 29282010. PMCID: PMC5746018.

30. Giannini EG, Bucci L, Garuti F, Brunacci M, Lenzi B, Valente M, et al. 2018; Patients with advanced hepatocellular carcinoma need a personalized management: a lesson from clinical practice. Hepatology. 67:1784–1796. DOI: 10.1002/hep.29668. PMID: 29159910.