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Laparoscopic versus open repeat liver resection for recurrent hepatocellular carcinoma in hepatectomy patients: inverse probability of treatment weighting

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Abstract

Repeat liver resection (RLR) is a good treatment option for recurrent hepatocellular carcinoma (HCC). However, laparoscopic repeat liver resection (LRLR) is more technically demanding than open repeat liver resection (ORLR). The purpose of our study is to compare the surgical outcomes of ORLR and LRLR and to carefully present LRLR guidelines for HCC. We performed RLR at a single institution from January 2017 to November 2019. We divided the patients into an ORLR group and an LRLR group. Inverse probability of treatment weighting (IPTW) was applied in this study to compare the ORLR group and the LRLR group. There was no difference between the two groups in patient characteristics, preoperative blood tests and pathological characteristics. After stabilized IPTW, the LRLR group had a shorter hospital stay (5.52 vs. 9.27 days, p = 0.001) and superior disease-free survival (p = 0.020). LRLR yielded better short-term outcomes than ORLR. And if a regular radiologic examination is performed, most of the recurrent tumors could be detected less than 3 cm. In conclusion, LRLR might be feasible and useful for recurrent HCC located contralateral to the previous tumor at a size of less than 3 cm.

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Abbreviations

HCC:

Hepatocellular carcinoma

RLR:

Repeat liver resection

LLR:

Laparoscopic liver resection

LPLR:

Laparoscopic primary liver resection

LRLR:

Laparoscopic repeat liver resection

ORLR:

Open repeat liver resection

BMI:

Body mass index

ASA:

American Society of Anesthesiologists

IPTW:

Inverse probability of treatment weighting

SMD:

Standardized mean differences

References

  1. European Association for the Study of the Liver (2018) EASL Clinical Practice Guidelines: management of hepatocellular carcinoma. J Hepatol 69:182–236. https://doi.org/10.1016/j.jhep.2018.03.019

    Article  Google Scholar 

  2. Meniconi RL, Komatsu S, Perdigao F, Boelle PY, Soubrane O, Scatton O (2015) Recurrent hepatocellular carcinoma: a Western strategy that emphasizes the impact of pathologic profile of the first resection. Surgery 157:454–462. https://doi.org/10.1016/j.surg.2014.10.011

    Article  PubMed  Google Scholar 

  3. Chan AC, Chan SC, Chok KS, Cheung TT, Chiu DW, Poon RT, Fan ST, Lo CM (2013) Treatment strategy for recurrent hepatocellular carcinoma: salvage transplantation, repeated resection, or radiofrequency ablation? Liver Transpl 19:411–419. https://doi.org/10.1002/lt.23605

    Article  PubMed  Google Scholar 

  4. Zhang XY, Li C, Wen TF, Yan LN, Li B, Yang JY, Wang WT, Xu MQ, Lu WS, Jiang L (2015) Appropriate treatment strategies for intrahepatic recurrence after curative resection of hepatocellular carcinoma initially within the Milan criteria: according to the recurrence pattern. Eur J Gastroenterol Hepatol 27:933–940. https://doi.org/10.1097/Meg.0000000000000383

    Article  PubMed  Google Scholar 

  5. Tralhao JG, Dagher I, Lino T, Roudie J, Franco D (2007) Treatment of tumour recurrence after resection of hepatocellular carcinoma. Analysis of 97 consecutive patients. Eur J Surg Oncol 33:746–751. https://doi.org/10.1016/j.ejso.2006.11.015

    Article  CAS  PubMed  Google Scholar 

  6. Roayaie S, Bassi D, Tarchi P, Labow D, Schwartz M (2011) Second hepatic resection for recurrent hepatocellular cancer: a Western experience. J Hepatol 55:346–350. https://doi.org/10.1016/j.jhep.2010.11.026

    Article  PubMed  Google Scholar 

  7. Gagner M (1992) Laparoscopic partial hepatectomy for liver tumor. Surg Endosc 6:97–98

    Google Scholar 

  8. Ome Y, Hashida K, Yokota M, Nagahisa Y, Yamaguchi K, Okabe M, Kawamoto K (2018) The feasibility and efficacy of pure laparoscopic repeat hepatectomy. Surg Endosc 32:3474–3479. https://doi.org/10.1007/s00464-018-6066-7

    Article  PubMed  Google Scholar 

  9. Goh BKP, Syn N, Teo JY, Guo YX, Lee SY, Cheow PC, Chow PKH, Ooi L, Chung AYF, Chan CY (2019) Perioperative outcomes of laparoscopic repeat liver resection for recurrent HCC: comparison with open repeat liver resection for recurrent HCC and laparoscopic resection for primary HCC. World J Surg 43:878–885. https://doi.org/10.1007/s00268-018-4828-y

    Article  PubMed  Google Scholar 

  10. Peng Y, Liu F, Wei Y, Li B (2019) Outcomes of laparoscopic repeat liver resection for recurrent liver cancer: a system review and meta-analysis. Medicine (Baltimore) 98:e17533. https://doi.org/10.1097/MD.0000000000017533

    Article  Google Scholar 

  11. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250:187–196. https://doi.org/10.1097/SLA.0b013e3181b13ca2

    Article  PubMed  Google Scholar 

  12. Rhu J, Kim SJ, Choi GS, Kim JM, Joh JW, Kwon CHD (2018) Laparoscopic versus open right posterior sectionectomy for hepatocellular carcinoma in a high-volume center: a propensity score matched analysis. World J Surg 42:2930–2937. https://doi.org/10.1007/s00268-018-4531-z

    Article  PubMed  Google Scholar 

  13. Kim JM, Kim S, Rhu J, Choi GS, Kwon CHD, Joh JW (2020) Elderly hepatocellular carcinoma patients: open or laparoscopic approach? Cancers (Basel). https://doi.org/10.3390/cancers12082281

    Article  PubMed Central  Google Scholar 

  14. Rhu J, Choi GS, Kim JM, Joh JW, Kwon CHD (2020) Feasibility of total laparoscopic living donor right hepatectomy compared with open surgery: comprehensive review of 100 cases of the initial stage. J Hepatobiliary Pancreat Sci 27:16–25. https://doi.org/10.1002/jhbp.653

    Article  PubMed  Google Scholar 

  15. Austin PC, Stuart EA (2015) Moving towards best practice when using inverse probability of treatment weighting (IPTW) using the propensity score to estimate causal treatment effects in observational studies. Stat Med 34:3661–3679. https://doi.org/10.1002/sim.6607

    Article  PubMed  PubMed Central  Google Scholar 

  16. Andrade C (2020) Mean difference, standardized mean difference (SMD), and their use in meta-analysis: as simple as it gets. J Clin Psychiatry. https://doi.org/10.4088/JCP.20f13681

    Article  PubMed  Google Scholar 

  17. Goh BK, Chow PK, Teo JY, Wong JS, Chan CY, Cheow PC, Chung AY, Ooi LL (2014) Number of nodules, Child-Pugh status, margin positivity, and microvascular invasion, but not tumor size, are prognostic factors of survival after liver resection for multifocal hepatocellular carcinoma. J Gastrointest Surg 18:1477–1485. https://doi.org/10.1007/s11605-014-2542-0

    Article  PubMed  Google Scholar 

  18. Noda T, Eguchi H, Wada H, Iwagami Y, Yamada D, Asaoka T, Gotoh K, Kawamoto K, Takeda Y, Tanemura M, Umeshita K, Doki Y, Mori M (2018) Short-term surgical outcomes of minimally invasive repeat hepatectomy for recurrent liver cancer. Surg Endosc 32:46–52. https://doi.org/10.1007/s00464-017-5632-8

    Article  PubMed  Google Scholar 

  19. Inoue Y, Fujii K, Ishii M, Kagota S, Tomioka A, Hamamoto H, Osumi W, Tsuchimoto Y, Terasawa T, Ogura T, Masubuchi S, Yamamoto M, Imoto A, Asai A, Komeda K, Fukunishi S, Hirokawa F, Goto M, Tanaka K, Okuda J, Higuchi K, Uchiyama K (2019) Laparoscopic repeat hepatic resection for the management of liver tumors. J Gastrointest Surg 23:2314–2321. https://doi.org/10.1007/s11605-019-04276-z

    Article  PubMed  Google Scholar 

  20. Morise Z, Aldrighetti L, Belli G, Ratti F, Belli A, Cherqui D, Tanabe M, Wakabayashi G (2020) Laparoscopic repeat liver resection for hepatocellular carcinoma: a multicentre propensity score-based study. Br J Surg 107:889–895. https://doi.org/10.1002/bjs.11436

    Article  CAS  PubMed  Google Scholar 

  21. Onoe T, Yamaguchi M, Irei T, Ishiyama K, Sudo T, Hadano N, Kojima M, Kubota H, Ide R, Tazawa H, Shimizu W, Suzuki T, Shimizu Y, Hinoi T, Tashiro H (2020) Feasibility and efficacy of repeat laparoscopic liver resection for recurrent hepatocellular carcinoma. Surg Endosc 34:4574–4581. https://doi.org/10.1007/s00464-019-07246-3

    Article  PubMed  Google Scholar 

  22. Belli G, Cioffi L, Fantini C, D’Agostino A, Russo G, Limongelli P, Belli A (2009) Laparoscopic redo surgery for recurrent hepatocellular carcinoma in cirrhotic patients: feasibility, safety, and results. Surg Endosc 23:1807–1811. https://doi.org/10.1007/s00464-009-0344-3

    Article  PubMed  Google Scholar 

  23. Hu M, Zhao G, Xu D, Liu R (2011) Laparoscopic repeat resection of recurrent hepatocellular carcinoma. World J Surg 35:648–655. https://doi.org/10.1007/s00268-010-0919-0

    Article  PubMed  Google Scholar 

  24. Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamamoto S, Yamazoe S, Ohira G, Nakajima T (2013) Laparoscopic liver resection for treating recurrent hepatocellular carcinoma. J Hepatobiliary Pancreat Sci 20:512–517. https://doi.org/10.1007/s00534-012-0592-9

    Article  PubMed  Google Scholar 

  25. Liu K, Chen Y, Wu X, Huang Z, Lin Z, Jiang J, Tan W, Zhang L (2017) Laparoscopic liver re-resection is feasible for patients with posthepatectomy hepatocellular carcinoma recurrence: a propensity score matching study. Surg Endosc 31:4790–4798. https://doi.org/10.1007/s00464-017-5556-3

    Article  PubMed  Google Scholar 

  26. Chan AC, Poon RT, Chok KS, Cheung TT, Chan SC, Lo CM (2014) Feasibility of laparoscopic re-resection for patients with recurrent hepatocellular carcinoma. World J Surg 38:1141–1146. https://doi.org/10.1007/s00268-013-2380-3

    Article  PubMed  Google Scholar 

  27. Zhang J, Zhou ZG, Huang ZX, Yang KL, Chen JC, Chen JB, Xu L, Chen MS, Zhang YJ (2016) Prospective, single-center cohort study analyzing the efficacy of complete laparoscopic resection on recurrent hepatocellular carcinoma. Chin J Cancer 35:25. https://doi.org/10.1186/s40880-016-0088-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors

Contributions

ESJ: acquisition of data, analysis and interpretation of data, and writing of the manuscript. JMK: design, analysis and interpretation of data, and writing of the manuscript. ML, JY, JEK, G-SC, and J-WJ: acquisition of data.

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Correspondence to Jong Man Kim.

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This study was approved by the Samsung Medical Center Institutional Review Board (IRB) (SMC-2020-01-071).

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Jeong, E.S., Kim, J.M., Lim, M. et al. Laparoscopic versus open repeat liver resection for recurrent hepatocellular carcinoma in hepatectomy patients: inverse probability of treatment weighting. Updates Surg 74, 527–534 (2022). https://doi.org/10.1007/s13304-022-01257-x

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  • DOI: https://doi.org/10.1007/s13304-022-01257-x

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