Skip to main content
Log in

Mils for HCC: the state of art

  • Review Article
  • Published:
Updates in Surgery Aims and scope Submit manuscript

Abstract

After an initial skepticism, minimally invasive liver surgery (MILS) gained popularity and is nowadays a consolidated option in specialized centers for the surgical treatment of selected patients affected by both benign and malignant liver diseases. Nevertheless, the role of MILS in the surgical treatment of hepato-cellular carcinoma (HCC) developed on the background of chronic liver disease is still a matter of debate. The indications and the current evidences on MILS for HCC are discussed in this paper. MILS being less invasive and harmful for the patients proved to offer a reduction in post-operative morbidity and specific benefits have been highlighted in case of patients affected by HCC and chronic liver disease. In fact, by minimizing liver manipulation and mobilization and by preserving the collateral blood and lymphatic flow, MILS seems to reduce the incidence of post-operative ascites and post-operative liver failure without compromising the oncologic outcomes. This has been confirmed by an analysis of 21 comparative studies and 5 metanalyses comparing MILS and open surgery for HCC. With an adequate surgical training, MILS for HCC can be undertaken safely even in case of major hepatectomies and technically demanding operations such as resections of posteriorly located tumors proved to be feasible in specialized centers. Therefore, with an appropriate patients’ selection, MILS for HCC is becoming the preferred option for the surgical treatment of HCC in cirrhotic patients.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Nguyen KT, Gamblin TC, Geller DA (2009) World review of laparoscopic liver resection-2804 patients. Ann Surg 250(5):831–841

    Article  PubMed  Google Scholar 

  2. Koffron AJ, Auffenberg G, Kung R, Abecassis M (2007) Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg 246(3):385–392

    Article  PubMed Central  PubMed  Google Scholar 

  3. Buell JF, Thomas MT, Rudich S, Marvin M, Nagubandi R, Ravindra KV et al (2008) Experience with more than 500 minimally invasive hepatic procedures. Ann Surg 248(3):475–486

    PubMed  Google Scholar 

  4. Sasaki A, Nitta H, Otsuka K, Takahara T, Nishizuka S, Wakabayashi G (2009) Ten-year experience of totally laparoscopic liver resection in a single institution. Br J Surg 96(3):274–279

    Article  CAS  PubMed  Google Scholar 

  5. Bryant R, Laurent A, Tayar C, Cherqui D (2009) Laparoscopic liver resection-understanding its role in current practice: the Henri Mondor Hospital experience. Ann Surg 250(1):103–111

    Article  PubMed  Google Scholar 

  6. El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557–2576

    Article  CAS  PubMed  Google Scholar 

  7. Schütte K, Bornschein J, Malfertheiner P (2009) Hepatocellular carcinoma: epidemiological trends and risk factors. Dig Dis 27:80–92

    PubMed  Google Scholar 

  8. Yao FY, Bass NM, Nikolai B, Davern TJ, Kerlan R, Wu V et al (2002) Liver transplantation for hepatocellular carcinoma: analysis of survival according to the intention-to-treat principle and dropout from the waiting list. Liver Transpl 8:873–883

    Article  PubMed  Google Scholar 

  9. Ziser A, Plevak DJ, Wiesner RH, Rakela J, Offord KP, Brown DL (1999) Morbidity and mortality in cirrhotic patients undergoing anesthesia and surgery. Anesthesiology 90:42–53

    Article  CAS  PubMed  Google Scholar 

  10. Mansour A, Watson W, Shayani V, Pickleman J (1997) Abdominal operations in patients with cirrhosis: still a major surgical challenge. Surgery 122:730–735

    Article  CAS  PubMed  Google Scholar 

  11. Belli G, Fantini C, D’Agostino A, Belli A, Russolillo N (2004) Laparoscopic liver resections for hepatocellular carcinoma (HCC) in cirrhotic patients. HPB (Oxford) 6(4):236–246

    Article  Google Scholar 

  12. Belli G, Fantini C, D’Agostino A, Belli A, Cioffi L, Russolillo N (2006) Laparoscopic left lateral hepatic lobectomy: a safer and faster technique. J Hepatobiliary Pancreat Surg 13(2):149–154

    Article  PubMed  Google Scholar 

  13. Belli G, Fantini C, D’Agostino A, Belli A, Russolillo N, Cioffi L (2005) Laparoscopic liver resection without a Pringle maneuver for HCC in cirrhotic patients. Chir Ital 57(1):15–25

    PubMed  Google Scholar 

  14. Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez PL (2003) Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg 138:763–769

    Article  PubMed  Google Scholar 

  15. Ker CG, Chen HY, Juan CC, Chang WS, Tsai CY, Lo HW et al (2000) Laparoscopic subsegmentectomy for hepatocellular carcinoma with cirrhosis. Hepatogastroenterology 47:1260–1263

    CAS  PubMed  Google Scholar 

  16. Kaneko H, Takagi S, Otsuka Y, Tsuchiya M, Tamura A, Katagiri T et al (2005) Laparoscopic liver resection of hepatocellular carcinoma. Am J Surg 189:190–194

    Article  PubMed  Google Scholar 

  17. Shimada M, Hashizume M, Maehara S, Tsujita E, Rikimaru T, Yamashita Y et al (2001) Laparoscopic hepatectomy for hepatocellular carcinoma. Surg Endosc 15:541–544

    Article  CAS  PubMed  Google Scholar 

  18. Belli G, Fantini C, D’Agostino A, Cioffi L, Langella S, Russolillo N et al (2007) Laparoscopic versus open liver resection for hepatocellular carcinoma in patients with histologically proven cirrhosis: short- and middle-term results. Surg Endosc 21(11):2004–2011

    Article  CAS  PubMed  Google Scholar 

  19. Cherqui D, Laurent A, Tayar C, Chang S, Van Nhieu JT, Loriau J et al (2006) Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: midterm results and perspectives. Ann Surg 243:499–506

    Article  PubMed Central  PubMed  Google Scholar 

  20. Dokmak S, Raut V, Aussilhou B, Ftériche FS, Farges O, Sauvanet A et al (2014) Laparoscopic left lateral resection is the gold standard for benign liver lesions: a case-control study. HPB (Oxford) 16(2):183-187. doi:10.1111/hpb.12108

  21. Chang S, Laurent A, Tayar C, Karoui M, Cherqui D (2007) Laparoscopy as a routine approach for left lateral sectionectomy. Br J Surg 94(1):58–63

    Article  CAS  PubMed  Google Scholar 

  22. Aldrighetti L, Pulitanò C, Catena M, Arru M, Guzzetti E, Casati M et al (2008) A prospective evaluation of laparoscopic versus open left lateral hepatic sectionectomy. J Gastrointest Surg 12(3):457–462

    Article  PubMed  Google Scholar 

  23. Dagher I, Gayet B, Tzanis D, Tranchart H, Fuks D, Soubrane O et al (2014) International experience for laparoscopic major liver resection. J Hepatobiliary Pancreat Sci 21(10):732–736

    Article  PubMed  Google Scholar 

  24. Lee KF, Chong CN, Wong J, Cheung YS, Wong J et al (2011) Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg 35:2268–2274

    Article  PubMed  Google Scholar 

  25. Ker CG, Chen JS, Kuo KK, Chuang SC, Wang SJ, Chang WC et al (2011) Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol 2011:596792

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Tranchart H, Di Giuro G, Lainas P, Roudie J, Agostini H, Franco D et al (2010) Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc 24:1170–1176

    Article  PubMed  Google Scholar 

  27. Belli G, Limongelli P, Fantini C, D’Agostino A, Cioffi L, Belli A et al (2009) Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg 96:1041–1048

    Article  CAS  PubMed  Google Scholar 

  28. Limongelli P, Vitiello C, Belli A, Pai M, Tolone S, Del Genio G et al (2014) Costs of laparoscopic and open liver and pancreatic resection: a systematic review. World J Gastroenterol 20(46):17595–17602

    Article  PubMed Central  PubMed  Google Scholar 

  29. Belli G, Fantini C, Belli A, Limongelli P (2011) Laparoscopic liver resection for hepatocellular carcinoma in cirrhosis: long-term outcomes. Dig Surg 28(2):134–140

    Article  PubMed  Google Scholar 

  30. Dagher I, Belli G, Fantini C, Laurent A, Tayar C, Lainas P et al (2010) Laparoscopic hepatectomy for hepatocellular carcinoma: a European experience. J Am Coll Surg 211(1):16–23

    Article  PubMed  Google Scholar 

  31. Kim H, Suh KS, Lee KW, Yi NJ, Hong G, Suh SW et al (2014) Long-term outcome of laparoscopic versus open liver resection for hepatocellular carcinoma: a case-controlled study with propensity score matching. Surg Endosc 28(3):950–960

    Article  PubMed  Google Scholar 

  32. Cheung TT, Poon RT, Yuen WK, Chok KS, Jenkins CR, Chan SC et al (2013) Long-term survival analysis of pure laparoscopic versus open hepatectomy for hepatocellular carcinoma in patients with cirrhosis: a single-center experience. Ann Surg 257(3):506–511

    Article  PubMed  Google Scholar 

  33. Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamazoe S, Yamamoto S et al (2013) Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc 27:2592–2597

    Article  PubMed  Google Scholar 

  34. Aldrighetti L, Guzzetti E, Pulitanò C, Cipriani F, Catena M, Paganelli M et al (2010) Case-matched analysis of totally laparoscopic versus open liver resection for HCC: short and middle term results. J Surg Oncol 102:82–86

    Article  PubMed  Google Scholar 

  35. Kluger MD, Vigano L, Barroso R, Cherqui D (2013) The learning curve in laparoscopic major liver resection. J Hepatobiliary Pancreat Sci 20(2):131–136

    Article  PubMed  Google Scholar 

  36. Vigano L, Laurent A, Tayar C, Tomatis M, Ponti A, Cherqui D (2009) The learning curve in laparoscopic liver resection: improved feasibility and reproducibility. Ann Surg 250(5):772–782

    Article  PubMed  Google Scholar 

  37. Memeo R, de’Angelis N, Compagnon P, Salloum C, Cherqui D, Laurent A et al (2014) Laparoscopic vs. open liver resection for hepatocellular carcinoma of cirrhotic liver: a case-control study. World J Surg 38:2919–2926

    Article  PubMed  Google Scholar 

  38. Ai JH, Li JW, Chen J, Bie P, Wang SG, Zheng SG (2013) Feasibility and safety of laparoscopic liver resection for hepatocellular carcinoma with a tumor size of 5–10 cm. PLoS One 8(8):e72328

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S et al (2011) Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a casematched study. Surg Endosc 25:3668–3677

    Article  CAS  PubMed  Google Scholar 

  40. Nguyen KT, Marsh JW, Tsung A, Steel JJ, Gamblin TC, Geller DA (2011) Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg 146:348–356

    Article  PubMed  Google Scholar 

  41. Hu BS, Chen K, Tan HM, Ding XM, Tan JW (2011) Comparison of laparoscopic vs open liver lobectomy (segmentectomy) for hepatocellular carcinoma. World J Gastroenterol 17:4725–4728

    Article  PubMed Central  PubMed  Google Scholar 

  42. Kim HH, Park EK, Seoung JS, Hur YH, Koh YS, Kim JC et al (2011) Liver resection for hepatocellular carcinoma: case-matched analysis of laparoscopic versus open resection. J Korean Surg Soc 80:412–419

    Article  PubMed Central  PubMed  Google Scholar 

  43. Alemi F, Kwon E, Freise C, Kang SM, Hirose R, Stewart L et al (2010) Hepatic surgery at a VA tertiary medical center: lessons learned. Am J Surg 200:591–595

    Article  PubMed  Google Scholar 

  44. Sarpel U, Hefti MM, Wisnievsky JP, Roayaie S, Schwartz ME, Labow DM (2009) Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: case matched analysis. Ann Surg Oncol 16:1572–1577

    Article  CAS  PubMed  Google Scholar 

  45. Lai EC, Tang CN, Ha JP, Li MK (2009) Laparoscopic liver resection for hepatocellular carcinoma: ten-year experience in a single center. Arch Surg 144:143–147 (Discussion 148)

    Article  PubMed  Google Scholar 

  46. Endo Y, Ohta M, Sasaki A, Kai S, Eguchi H, Iwaki K et al (2009) A comparative study of the long-term outcomes after laparoscopy-assisted and open left lateral hepatectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech 19:e171–e174

    Article  PubMed  Google Scholar 

  47. Zhou YM, Shao WY, Zhao YF, Xu DH, Li B (2011) Meta-analysis of laparoscopic versus open resection for hepatocellular carcinoma. Dig Dis Sci 56:1937–1943

    Article  PubMed  Google Scholar 

  48. Li N, Wu YR, Wu B, Lu MQ (2012) Surgical and oncologic outcomes following laparoscopic versus open liver resection for hepatocellular carcinoma: a meta-analysis. Hepatol Res. 42:51–59

    Article  PubMed  Google Scholar 

  49. Xiong JJ, Altaf K, Javed MA, Huang W, Mukherjee R, Mai G et al (2012) Meta-analysis of laparoscopic vs open liver resection for hepatocellular carcinoma. World J Gastroenterol 18:6657–6668

    Article  PubMed Central  PubMed  Google Scholar 

  50. Yin Z, Fan X, Ye H, Yin D, Wang J (2013) Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol 20:1203–1215

    Article  PubMed  Google Scholar 

  51. Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I et al (2009) World consensus conference on laparoscopic surgery. The international position on laparoscopic liver surgery: the Louisville statement, 2008. Ann Surg 250(5):825–830

    Article  PubMed  Google Scholar 

  52. Morise Z, Ciria R, Cherqui D, Chen KH, Belli G, Wakabayashi G (2015) Can we expand the indications for laparoscopic liver resection? A systematic review and meta-analysis of laparoscopic liver resection for patients with hepatocellular carcinoma and chronic liver disease. J Hepatobiliary Pancreat Sci 22(5):342–352

    Article  PubMed  Google Scholar 

  53. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS et al (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261(4):619–629

    PubMed  Google Scholar 

  54. Santambrogio R, Opocher E, Zuin M, Selmi C, Bertolini E, Costa M et al (2009) Surgical resection versus laparoscopic radiofrequency ablation in patients with hepatocellular carcinoma and Child-Pugh class a liver cirrhosis. Ann Surg Oncol 16(12):3289–3298

    Article  PubMed  Google Scholar 

  55. Cillo U, Noaro G, Vitale A, Neri D, D’Amico F, Gringeri E et al (2014) HePaTIC Study Group. Laparoscopic microwave ablation in patients with hepatocellular carcinoma: a prospective cohort study. HPB (Oxford) 16(11):979–986

    Google Scholar 

  56. Belli G, D’Agostino A, Fantini C, Cioffi L, Belli A, Russolillo N et al (2007) Laparoscopic radiofrequency ablation combined with laparoscopic liver resection for more than one HCC on cirrhosis. Surg Laparosc Endosc Percutan Tech 17(4):331–334

    Article  PubMed  Google Scholar 

  57. Laurent A, Tayar C, Andréoletti M, Lauzet JY, Merle JC, Cherqui D (2009) Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 16(3):310–314

    Article  PubMed  Google Scholar 

  58. Belli G, Cioffi L, Fantini C, D’Agostino A, Russo G, Limongelli P et al (2009) Laparoscopic redo surgery for recurrent hepatocellular carcinoma in cirrhotic patients: feasibility, safety, and results. Surg Endosc 23(8):1807–1811

    Article  PubMed  Google Scholar 

  59. Isetani M, Morise Z, Kawabe N, Tomishige H, Nagata H, Kawase J et al (2015) Pure laparoscopic hepatectomy as repeat surgery and repeat hepatectomy. World J Gastroenterol 21(3):961–968

    PubMed Central  PubMed  Google Scholar 

  60. Cioffi L, Belli A, Fantini C, D’Agostino A, Belli G, Russo G (2015) Repeat liver surgery by laparoscopy for a malignant recurrence after previous open or laparoscopic resection. Hepatoma Res 1(1):30–35

    Article  Google Scholar 

  61. Ogiso S, Conrad C, Araki K, Nomi T, Anil Z, Gayet B (2015) Laparoscopic transabdominal with transdiaphragmatic access improves resection of difficult posterosuperior liver lesions. Ann Surg [Epub ahead of print]

  62. Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256(6):959–964

    Article  PubMed  Google Scholar 

  63. Cho JY, Han HS, Yoon YS, Choi Y, Lee W (2015) Outcomes of laparoscopic right posterior sectionectomy in patients with hepatocellular carcinoma in the era of laparoscopic surgery. Surgery [Epub ahead of print]

  64. Yoon YS, Han HS, Cho JY, Kim JH, Kwon Y (2013) Laparoscopic liver resection for centrally located tumors close to the hilum, major hepatic veins, or inferior vena cava. Surgery 153(4):502–509

    Article  PubMed  Google Scholar 

  65. Belli G, Fantini C, D’Agostino A, Cioffi L, Limongelli P, Russo G et al (2008) Laparoscopic segment VI liver resection using a left lateral decubitus position: a personal modified technique. J Gastrointest Surg 12(12):2221–2226

    Article  PubMed  Google Scholar 

  66. Belli G, Gayet B, Han HS, Wakabayashi G, Kim KH, Cannon R et al (2013) International Consensus Group for Laparoscopic Liver Surgery. Laparoscopic left hemihepatectomy a consideration for acceptance as standard of care. Surg Endosc 27(8):2721–2726

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrea Belli.

Ethics declarations

Conflict of interest

The authors have no potential conflict of interest to declare.

Ethical standard

The study was approved by the Ethics Committee of the Department and conformed to the ethical guidelines of the Helsinki Declaration (as revised in Tokyo 2004). No study advertising was made and no remuneration was offered.

Research involving human participants or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

No informed consent is required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Belli, A., Fantini, C., Cioffi, L. et al. Mils for HCC: the state of art. Updates Surg 67, 105–109 (2015). https://doi.org/10.1007/s13304-015-0316-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13304-015-0316-1

Keywords

Navigation