Hepatectomy Combined with Diaphragmatic Resection for Hepatocellular Carcinoma with Diaphragmatic Involvement: A Propensity Score-Matched Analysis

Abstract

Purpose

We evaluated the short- and long-term surgical outcomes of hepatectomy combined with diaphragmatic resection for hepatocellular carcinoma (HCC) with diaphragmatic involvement.

Methods

We retrospectively reviewed the surgical outcomes of HCC patients with diaphragmatic resection (DR group) and HCC patients without diaphragmatic resection (non-DR group). We applied 1:1 propensity score matching (PSM) to these subjects.

Results

The study included 46 patients in DR group and 828 patients in non-DR group. The DR group cases were pathologically more advanced, and both overall and relapse-free survival among the patients in this group with pathological diaphragmatic invasion were similar to cases with pathological diaphragmatic fibrous adhesion. There were 40 patients from each group subjected to PSM. In these matched cohorts, there was no statistically significant difference between the two groups regarding perioperative outcomes, overall survival, and relapse-free survival. Multivariate analyses of our matched HCC patients revealed that alpha-fetoprotein expression and tumor size were independent prognostic factors for overall survival and poor differentiation for relapse-free survival, whereas neither diaphragmatic invasion nor diaphragmatic resection were prognostic indicators. The most frequent site of recurrence in non-DR group was the liver, whereas the most frequent site of recurrence in DR group was the lung before and after PSM.

Conclusions

The short- and long-term surgical outcomes of DR HCC cases are equivalent to their non-DR counterparts under a matched clinicopathological background. Hepatectomy combined with DR is an acceptable treatment for HCC with either diaphragmatic fibrous adhesion or diaphragmatic invasion.

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References

  1. 1.

    Forner A, Reig M, Bruix J. Hepatocellular carcinoma. Lancet. 2018;31:1301–14.

    Google Scholar 

  2. 2.

    Kokudo T, Hasegawa K, Matsuyama Y, et al. Survival benefit of liver resection for hepatocellular carcinoma associated with portal vein invasion. J Hepatol. 2016;65:938–43.

    PubMed  Google Scholar 

  3. 3.

    Wakayama K, Kamiyama T, Yokoo H, et al. Huge hepatocellular carcinoma greater than 10 cm in diameter worsens prognosis by causing distant recurrence after curative resection. J Surg Oncol. 2017;115:324–9.

    PubMed  Google Scholar 

  4. 4.

    Zheng J, Shen S, Jiang L, et al. Outcomes of anterior approach major hepatectomy with diaphragmatic resection for single huge right lobe HCC with diaphragmatic invasion. Medicine (Baltimore). 2018;97:e12194.

    PubMed  PubMed Central  Google Scholar 

  5. 5.

    Yamashita Y, Morita K, Iguchi T, et al. Surgical impacts of an en bloc resection of the diaphragm for hepatocellular carcinoma with gross diaphragmatic involvement. Surg Today. 2011;41:101–6.

    PubMed  Google Scholar 

  6. 6.

    Wakayama K, Kamiyama T, Yokoo H, et al. Our technique of preceding diaphragm resection and partial mobilization of the hepatic right lobe using a vessel sealing device (LigaSure™) for huge hepatic tumors with diaphragm invasion. Surg Today. 2016;46:1224–9.

    PubMed  Google Scholar 

  7. 7.

    Liu YC, Mao YZ, Wang JC, et al. Hepatocellular carcinoma with en bloc diaphragmatic resection: a single-center experience over 14 years. Int J Surg. 2018;53:93–7.

    PubMed  Google Scholar 

  8. 8.

    Kamiyama T, Nakanishi K, Yokoo H, et al. Perioperative management of hepatic resection toward zero mortality and morbidity: analysis of 793 consecutive cases in a single institution. J Am Coll Surg. 2010;211:443–9.

    PubMed  Google Scholar 

  9. 9.

    Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009;250:187–96.

    PubMed  Google Scholar 

  10. 10.

    Lau WY, Leung KL, Leung TW, Liew CT, Chan M, Li AK. Resection of hepatocellular carcinoma with diaphragmatic invasion. Br J Surg. 1995;82:264–6.

    CAS  PubMed  Google Scholar 

  11. 11.

    Yuki K, Hirohashi S, Sakamoto M, Kanai T, Shimosato Y. Growth and spread of hepatocellular carcinoma. A review of 240 consecutive autopsy cases. Cancer. 1990;66:2174–9.

  12. 12.

    Kamarajah SK, Frankel TL, Sonnenday C, Cho CS, Nathan H. Critical evaluation of the American Joint Commission on Cancer (AJCC) 8th edition staging system for patients with Hepatocellular Carcinoma (HCC): a Surveillance, Epidemiology, End Results (SEER) analysis. J Surg Oncol. 2018;117:644–50.

  13. 13.

    Sonohara F, Nomoto S, Inokawa Y, et al. Serosal invasion strongly associated with recurrence after curative hepatic resection of hepatocellular carcinoma: a retrospective study of 214 consecutive cases. Medicine (Baltimore). 2015;94:e602.

    PubMed  PubMed Central  Google Scholar 

  14. 14.

    Kato Y, Okamura Y, Sugiura T, et al. The impact of serosal invasion on prognosis after curative hepatectomy for hepatocellular carcinoma: invasion to adjacent organs and rupture of tumor were crucial tumor-related prognostic factors needed for survival. Dig Surg. 2018;35:155–63.

    PubMed  Google Scholar 

  15. 15.

    Sakamoto K, Ogawa K, Tohyama T, et al. Serosal invasion is a strong prognostic factor for hepatocellular carcinoma after hepatectomy. Hepatol Res. 2019;49:419–31.

    CAS  PubMed  Google Scholar 

  16. 16.

    Yang SL, Liu LP, Yang S, et al. Preoperative serum α-fetoprotein and prognosis after hepatectomy for hepatocellular carcinoma. Br J Surg. 2016;103:716-24.

    CAS  PubMed  Google Scholar 

  17. 17.

    Meguro M, Mizuguchi T, Nishidate T, et al. Prognostic roles of preoperative α-fetoprotein and des-γ-carboxy prothrombin in hepatocellular carcinoma patients. World J Gastroenterol. 2015;21(28):4933–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Han JH, Kim DG, Na GH, et al. Evaluation of prognostic factors on recurrence after curative resections for hepatocellular carcinoma. World J Gastroenterol. 2014;20:17132–40.

    PubMed  PubMed Central  Google Scholar 

  19. 19.

    Chang YJ, Chung KP, Chang YJ, Chen LJ. Long-term survival of patients undergoing liver resection for very large hepatocellular carcinomas. Br J Surg. 2016;103:1513–20.

    CAS  PubMed  Google Scholar 

  20. 20.

    Orimo T, Ojima H, Hiraoka N, Saito S, Kosuge T, Kakisaka T, Yokoo H, Nakanishi K, Kamiyama T, Todo S, Hirohashi S, Kondo T. Proteomic profiling reveals the prognostic value of adenomatous polyposis coli-end-binding protein 1 in hepatocellular carcinoma. Hepatology. 2008;48:1851–63.

    CAS  PubMed  Google Scholar 

  21. 21.

    Shen J, Liu J, Li C, Wen T, Yan L, Yang J. The impact of tumor differentiation on the prognosis of HBV-associated solitary hepatocellular carcinoma following hepatectomy: a propensity score matching analysis. Dig Dis Sci. 2018;63:1962–9.

    CAS  PubMed  Google Scholar 

  22. 22.

    Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology. 2005;42:1208–36.

    PubMed  Google Scholar 

  23. 23.

    Minagawa M, Makuuchi M, Takayama T, Ohtomo K. Selection criteria for hepatectomy in patients with hepatocellular carcinoma and portal vein tumor thrombus. Ann Surg. 2001;233:379–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Kamiyama T, Nakanishi K, Yokoo H, et al. Efficacy of preoperative radiotherapy to portal vein tumor thrombus in the main trunk or first branch in patients with hepatocellular carcinoma. Int J Clin Oncol. 2007;12:363–8.

    PubMed  Google Scholar 

  25. 25.

    Inoue Y, Hasegawa K, Ishizawa T, et al. Is there any difference in survival according to the portal tumor thrombectomy method in patients with hepatocellular carcinoma? Surgery. 2009;145:9–19.

    PubMed  Google Scholar 

  26. 26.

    Kokudo T, Hasegawa K, Yamamoto S, et al. Surgical treatment of hepatocellular carcinoma associated with hepatic vein tumor thrombosis. J Hepatol. 2014;61:583–8.

    PubMed  Google Scholar 

  27. 27.

    Poon RT, Fan ST, Wong J. Selection criteria for hepatic resection in patients with large hepatocellular carcinoma larger than 10 cm in diameter. J Am Coll Surg. 2002;194:592–602.

    PubMed  Google Scholar 

  28. 28.

    Matsukuma S, Sato K. Peritoneal seeding of hepatocellular carcinoma: clinicopathological characteristics of 17 autopsy cases. Pathol Int. 2011;61:356–62.

    PubMed  Google Scholar 

  29. 29.

    Xia F, Poon RT, Fan ST, Wong J. Thoracoabdominal approach for right-sided hepatic resection for hepatocellular carcinoma. J Am Coll Surg. 2003;196:418–27.

    PubMed  Google Scholar 

  30. 30.

    Bruix J, Takayama T, Mazzaferro V, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2015;16:1344–54.

    CAS  PubMed  Google Scholar 

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Correspondence to Tatsuya Orimo MD, PhD.

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Orimo, T., Kamiyama, T., Wakayama, K. et al. Hepatectomy Combined with Diaphragmatic Resection for Hepatocellular Carcinoma with Diaphragmatic Involvement: A Propensity Score-Matched Analysis. Ann Surg Oncol 27, 4153–4163 (2020). https://doi.org/10.1245/s10434-020-08754-6

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