Skip to main content
SpringerLink
Log in

Feasibility and efficacy of repeat laparoscopic liver resection for recurrent hepatocellular carcinoma

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Repeat hepatectomy is an acceptable treatment for recurrent hepatocellular carcinoma (HCC). However, repeat laparoscopic liver resection (LLR) has not been widely adopted due to its technical difficulty. This study aimed to assess the feasibility and efficacy of repeat LLR compared with repeat open liver resection (OLR) for recurrent HCC.

Methods

We performed 42 repeat OLR and 30 repeat LLR for cases of recurrent HCC between January 2007 and March 2018. This study retrospectively compared the patients’ clinicopathological characteristics and operative and short-term outcomes including surgical time, intraoperative blood loss, duration of hospital stay, and postoperative complications between the two groups.

Results

There were no significant differences in patient characteristics between the two groups except in terms of Child–Pugh grade. The repeat LLR group had lower median intraoperative blood loss (100 mL vs. 435 mL; P = 0.001) and shorter median postoperative hospital stay (10 days vs. 14.5 days; P = 0.002). The other results including postoperative complications were comparable between the two groups. Further, comparison of two subpopulations of the repeat LLR group stratified by previous hepatectomy type (open or laparoscopic) or tumor location (segments 7 and 8 or other) revealed no significant differences in the postoperative clinical characteristics between them, although the morbidity rate tended to be higher in patients who underwent open hepatectomy for primary HCC than in patients who underwent laparoscopic hepatectomy.

Conclusions

Repeat LLR for recurrent HCC is feasible and useful with good short-term outcomes although an appropriate patient selection seems to be necessary.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Minagawa M, Makuuchi M, Takayama T, Kokudo N (2003) Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 238:703–710

    Article  PubMed  PubMed Central  Google Scholar 

  2. Itamoto T, Nakahara H, Amano H, Kohashi T, Ohdan H, Tashiro H, Asahara T (2007) Repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 141:589–597

    Article  PubMed  Google Scholar 

  3. 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

    Article  PubMed  Google Scholar 

  4. Gagner M, Rheault M, Dubuc J (1992) Laparoscopic partial hepatectomy for liver tumor. Surg Endosc 6:97–98

    Google Scholar 

  5. Kaneko H, Takagi S, Shiba T (1996) Laparoscopic partial hepatectomy and left lateral segmentectomy: technique and results of a clinical series. Surgery 120:468–475

    Article  CAS  PubMed  Google Scholar 

  6. Koffron AJ, Kung RD, Auffenberg GB, Abecassis MM (2007) Laparoscopic liver surgery for everyone: the hybrid method. Surgery 142:463–468 (Discussion 468.e461–462)

    Article  PubMed  Google Scholar 

  7. Nitta H, Sasaki A, Fujita T, Itabashi H, Hoshikawa K, Takahara T, Takahashi M, Nishizuka S, Wakabayashi G (2010) Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 251:450–453

    Article  PubMed  Google Scholar 

  8. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS, World Consensus Conference on Laparoscopic Study (2009) The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg 250:825–830

    Article  PubMed  Google Scholar 

  9. Beppu T, Wakabayashi G, Hasegawa K, Gotohda N, Mizuguchi T, Takahashi Y, Hirokawa F, Taniai N, Watanabe M, Katou M, Nagano H, Honda G, Baba H, Kokudo N, Konishi M, Hirata K, Yamamoto M, Uchiyama K, Uchida E, Kusachi S, Kubota K, Mori M, Takahashi K, Kikuchi K, Miyata H, Takahara T, Nakamura M, Kaneko H, Yamaue H, Miyazaki M, Takada T (2015) Long-term and perioperative outcomes of laparoscopic versus open liver resection for colorectal liver metastases with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci 22:711–720

    Article  PubMed  Google Scholar 

  10. Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N, Hatano E, Tanahashi Y, Mizuguchi T, Kamiyama T, Ikeda T, Tanaka S, Taniai N, Baba H, Tanabe M, Kokudo N, Konishi M, Uemoto S, Sugioka A, Hirata K, Taketomi A, Maehara Y, Kubo S, Uchida E, Miyata H, Nakamura M, Kaneko H, Yamaue H, Miyazaki M, Takada T (2015) Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci 22:721–727

    Article  PubMed  Google Scholar 

  11. Fretland AA, Dagenborg VJ, Bjornelv GMW, Kazaryan AM, Kristiansen R, Fagerland MW, Hausken J, Tonnessen TI, Abildgaard A, Barkhatov L, Yaqub S, Rosok BI, Bjornbeth BA, Andersen MH, Flatmark K, Aas E, Edwin B (2018) Laparoscopic versus open resection for colorectal liver metastases: the OSLO-COMET randomized controlled trial. Ann Surg 267:199–207

    Article  PubMed  Google Scholar 

  12. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, O’Rourke N, Tanabe M, Koffron AJ, Tsung A, Soubrane O, Machado MA, Gayet B, Troisi RI, Pessaux P, Van Dam RM, Scatton O, Abu Hilal M, Belli G, Kwon CH, Edwin B, Choi GH, Aldrighetti LA, Cai X, Cleary S, Chen KH, Schon MR, Sugioka A, Tang CN, Herman P, Pekolj J, Chen XP, Dagher I, Jarnagin W, Yamamoto M, Strong R, Jagannath P, Lo CM, Clavien PA, Kokudo N, Barkun J, Strasberg SM (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261:619–629

    PubMed  Google Scholar 

  13. Ciria R, Cherqui D, Geller DA, Briceno J, Wakabayashi G (2016) comparative short-term benefits of laparoscopic liver resection: 9000 cases and climbing. Ann Surg 263:761–777

    Article  PubMed  Google Scholar 

  14. Isetani M, Morise Z, Kawabe N, Tomishige H, Nagata H, Kawase J, Arakawa S (2015) Pure laparoscopic hepatectomy as repeat surgery and repeat hepatectomy. World J Gastroenterol 21:961–968

    Article  PubMed  PubMed Central  Google Scholar 

  15. Shafaee Z, Kazaryan AM, Marvin MR, Cannon R, Buell JF, Edwin B, Gayet B (2011) Is laparoscopic repeat hepatectomy feasible? A tri-institutional analysis. J Am Coll Surg 212:171–179

    Article  PubMed  Google Scholar 

  16. Hallet J, SaCunha A, Cherqui D, Gayet B, Goere D, Bachellier P, Laurent A, Fuks D, Navarro F, Pessaux P, French Colorectal Liver Metastases Working Group AFdC (2017) Laparoscopic compared to open repeat hepatectomy for colorectal liver metastases: a multi-institutional propensity-matched analysis of short- and long-term outcomes. World J Surg 41:3189–3198

    Article  PubMed  Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. Hu M, Zhao G, Xu D, Liu R (2011) Laparoscopic repeat resection of recurrent hepatocellular carcinoma. World J Surg 35:648–655

    Article  PubMed  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. Arii S, Yamaoka Y, Futagawa S, Inoue K, Kobayashi K, Kojiro M, Makuuchi M, Nakamura Y, Okita K, Yamada R (2000) Results of surgical and nonsurgical treatment for small-sized hepatocellular carcinomas: a retrospective and nationwide survey in Japan. The Liver Cancer Study Group of Japan. Hepatology 32:1224–1229

    Article  CAS  PubMed  Google Scholar 

  21. Hasegawa K, Makuuchi M, Takayama T, Kokudo N, Arii S, Okazaki M, Okita K, Omata M, Kudo M, Kojiro M, Nakanuma Y, Takayasu K, Monden M, Matsuyama Y, Ikai I (2008) Surgical resection vs. percutaneous ablation for hepatocellular carcinoma: a preliminary report of the Japanese nationwide survey. J Hepatol 49:589–594

    Article  PubMed  Google Scholar 

  22. Llovet JM, Real MI, Montana X, Planas R, Coll S, Aponte J, Ayuso C, Sala M, Muchart J, Sola R, Rodes J, Bruix J, Barcelona Liver Cancer Group (2002) Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet 359:1734–1739

    Article  PubMed  Google Scholar 

  23. Sumie S, Yamashita F, Ando E, Tanaka M, Yano Y, Fukumori K, Sata M (2003) Interventional radiology for advanced hepatocellular carcinoma: comparison of hepatic artery infusion chemotherapy and transcatheter arterial lipiodol chemoembolization. Am J Roentgenol 181:1327–1334

    Article  Google Scholar 

  24. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, Schwartz M, Porta C, Zeuzem S, Bolondi L, Greten TF, Galle PR, Seitz JF, Borbath I, Haussinger D, Giannaris T, Shan M, Moscovici M, Voliotis D, Bruix J, Group SIS (2008) Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359:378–390

    Article  CAS  PubMed  Google Scholar 

  25. Chan AC, Poon RT, Cheung TT, Chok KS, Chan SC, Fan ST, Lo CM (2012) Survival analysis of re-resection versus radiofrequency ablation for intrahepatic recurrence after hepatectomy for hepatocellular carcinoma. World J Surg 36:151–156

    Article  PubMed  Google Scholar 

  26. Song KD, Lim HK, Rhim H, Lee MW, Kim YS, Lee WJ, Paik YH, Gwak GY, Kim JM, Kwon CH, Joh JW (2015) Repeated hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma after hepatic resection: a propensity score matching study. Radiology 275:599–608

    Article  PubMed  Google Scholar 

  27. Ho CM, Lee PH, Shau WY, Ho MC, Wu YM, Hu RH (2012) Survival in patients with recurrent hepatocellular carcinoma after primary hepatectomy: comparative effectiveness of treatment modalities. Surgery 151:700–709

    Article  PubMed  Google Scholar 

  28. 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

    Article  PubMed  Google Scholar 

  29. Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L, Fan ST, Yokoyama Y, Crawford M, Makuuchi M, Christophi C, Banting S, Brooke-Smith M, Usatoff V, Nagino M, Maddern G, Hugh TJ, Vauthey JN, Greig P, Rees M, Nimura Y, Figueras J, DeMatteo RP, Buchler MW, Weitz J (2011) Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery 149:680–688

    Article  PubMed  Google Scholar 

  30. Lee MKT, Gao F, Strasberg SM (2016) Completion of a liver surgery complexity score and classification based on an International Survey of Experts. J Am Coll Surg 223:332–342

    Article  PubMed  PubMed Central  Google Scholar 

  31. Ban D, Tanabe M, Ito H, Otsuka Y, Nitta H, Abe Y, Hasegawa Y, Katagiri T, Takagi C, Itano O, Kaneko H, Wakabayashi G (2014) A novel difficulty scoring system for laparoscopic liver resection. J Hepatobiliary Pancreat Sci 21:745–753

    Article  PubMed  Google Scholar 

  32. Shelat VG, Serin K, Samim M, Besselink MG, Al Saati H, Gioia PD, Pearce NW, Abu Hilal M (2014) Outcomes of repeat laparoscopic liver resection compared to the primary resection. World J Surg 38:3175–3180

    Article  CAS  PubMed  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    Article  PubMed  Google Scholar 

  35. Hirokawa F, Hayashi M, Asakuma M, Shimizu T, Inoue Y, Uchiyama K (2017) Intercostal trocars enable easier laparoscopic resection of liver tumors in segments 7 and 8. World J Surg 41:1340–1346

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Drs. Shin Nakahira, Shingo Seo, Shintaro Akabane, Toshihiro Misumi, and Yoshino Hiraaki for their help.

Funding

This work was supported by a grant from the Research Program on Hepatitis from the Japan Agency for Medical Research and Development (AMED; JP15fk0210016 h003 and JP16fk0210107).

Author information

Authors and Affiliations

  1. Department of Surgery, Kure Medical Center/Chugoku Cancer Center, 3-1 Aoyama, Kure, Hiroshima, 737-0023, Japan

    Takashi Onoe, Megumi Yamaguchi, Toshimitsu Irei, Kohei Ishiyama, Takeshi Sudo, Naoto Hadano, Masato Kojima, Haruna Kubota, Ryuta Ide, Hirofumi Tazawa, Wataru Shimizu, Takahisa Suzuki, Yosuke Shimizu, Takao Hinoi & Hirotaka Tashiro

  2. Department of Gastroenterological and Transplant Surgery, Institute of Biomedical and Health Sciences, Hiroshima University, 1-2-3 Kasumi, Minami-ku, Hiroshima, 734-8551, Japan

    Takashi Onoe & Hirotaka Tashiro

Authors
  1. Takashi Onoe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Megumi Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Toshimitsu Irei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kohei Ishiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takeshi Sudo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Naoto Hadano
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Masato Kojima
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Haruna Kubota
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ryuta Ide
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hirofumi Tazawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Wataru Shimizu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Takahisa Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yosuke Shimizu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Takao Hinoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Hirotaka Tashiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Takashi Onoe or Hirotaka Tashiro.

Ethics declarations

Disclosures

Takashi Onoe, Megumi Yamaguchi, Toshimitsu Irei, Kohei Ishiyama, Takeshi Sudo, Naoto Hadano, Masato Kojima, Haruna Kubota, Ryuta Ide, Hirofumi Tazawa, Wataru Shimizu, Takahisa Suzuki, Yosuke Shimizu, Takao Hinoi and Hirotaka Tashiro have no conflicts of interest or financial ties to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onoe, T., Yamaguchi, M., Irei, T. et al. Feasibility and efficacy of repeat laparoscopic liver resection for recurrent hepatocellular carcinoma. Surg Endosc 34, 4574–4581 (2020). https://doi.org/10.1007/s00464-019-07246-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-019-07246-3

Keywords

Search

Navigation