Semin Liver Dis 2013; 33(03): 226-235
DOI: 10.1055/s-0033-1351780
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Laparoscopic Liver Resection: Lessons at the End of the Second Decade

Cheguevara Afaneh
1   Section of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, New York Presbyterian Hospital Weill Cornell Medical College, New York
,
Michael D. Kluger
1   Section of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, New York Presbyterian Hospital Weill Cornell Medical College, New York
› Author Affiliations
Further Information

Publication History

Publication Date:
13 August 2013 (online)

Abstract

Laparoscopic liver surgery has evolved over the last two decades. Advancements in surgical technology, surgical technique, and postoperative care have aided in lifting barriers to laparoscopic liver resection (LLR). In this review, the authors highlight the modern indications, benefits, safety, and feasibility of laparoscopic liver resections. Moreover, they analyze various studies comparing laparoscopic major hepatectomies to open surgery. Morbidity and mortality rates are at an all-time low in this era of laparoscopic liver surgery. The role of laparoscopy for oncologic resections is compared with open liver resections. Attention is given to oncologic margins and survival rates. In addition, the authors examine the safety and efficacy of LLR for nontraditional laparoscopic segments and tumors abutting major hepatic vasculature. Various resection techniques are reviewed including the use of the hanging-maneuver and modern stapling devices. Finally, they examine several novel techniques for laparoscopic liver resections including the hybrid technique, as is used in laparoscopic living donor hepatectomies, the use of hand-assistance to avoid conversion to open surgery, and the use of the robotic platform to aid in complex biliary or vascular reconstructions. Current barriers to laparoscopic liver surgery will continue to fall over the next decade.

 
  • References

  • 1 Gagner M, Rheault M, Dubuc J. Laparoscopic partial hepatectomy for liver tumor. Surg Endosc 1992; 6: 97-98
  • 2 Azagra JS, Goergen M, Gilbart E, Jacobs D. Laparoscopic anatomical (hepatic) left lateral segmentectomy-technical aspects. Surg Endosc 1996; 10 (7) 758-761
  • 3 Cherqui D, Husson E, Hammoud R , et al. Laparoscopic liver resections: a feasibility study in 30 patients. Ann Surg 2000; 232 (6) 753-762
  • 4 Cherqui D, Soubrane O, Husson E , et al. Laparoscopic living donor hepatectomy for liver transplantation in children. Lancet 2002; 359 (9304) 392-396
  • 5 Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg 2009; 250 (5) 831-841
  • 6 Bryant R, Laurent A, Tayar C, Cherqui D. Laparoscopic liver resection-understanding its role in current practice: the Henri Mondor Hospital experience. Ann Surg 2009; 250 (1) 103-111
  • 7 Buell JF, Thomas MT, Rudich S , et al. Experience with more than 500 minimally invasive hepatic procedures. Ann Surg 2008; 248 (3) 475-486
  • 8 Chen HY, Juan CC, Ker CG. Laparoscopic liver surgery for patients with hepatocellular carcinoma. Ann Surg Oncol 2008; 15 (3) 800-806
  • 9 Cho JY, Han HS, Yoon YS, Shin SH. Experiences of laparoscopic liver resection including lesions in the posterosuperior segments of the liver. Surg Endosc 2008; 22 (11) 2344-2349
  • 10 Koffron AJ, Auffenberg G, Kung R, Abecassis M. Evaluation of 300 minimally invasive liver resections at a single institution: less is more. Ann Surg 2007; 246 (3) 385-392 , discussion 392–394
  • 11 Buell JF, Cherqui D, Geller DA , et al; World Consensus Conference on Laparoscopic Surgery. The international position on laparoscopic liver surgery: The Louisville Statement, 2008. Ann Surg 2009; 250 (5) 825-830
  • 12 Chang S, Laurent A, Tayar C, Karoui M, Cherqui D. Laparoscopy as a routine approach for left lateral sectionectomy. Br J Surg 2007; 94 (1) 58-63
  • 13 Gumbs AA, Jarufe N, Gayet B. Minimally invasive approaches to extrapancreatic cholangiocarcinoma. Surg Endosc 2013; 27 (2) 406-414
  • 14 Machado MA, Makdissi FF, Surjan RC, Mochizuki M. Laparoscopic resection of hilar cholangiocarcinoma. J Laparoendosc Adv Surg Tech A 2012; 22 (10) 954-956
  • 15 Yu H, Wu SD, Chen DX, Zhu G. Laparoscopic resection of Bismuth type I and II hilar cholangiocarcinoma: an audit of 14 cases from two institutions. Dig Surg 2011; 28 (1) 44-49
  • 16 Belli G, Cioffi L, Fantini C , et al. Laparoscopic redo surgery for recurrent hepatocellular carcinoma in cirrhotic patients: feasibility, safety, and results. Surg Endosc 2009; 23 (8) 1807-1811
  • 17 Cai XJ, Yang J, Yu H , et al. Clinical study of laparoscopic versus open hepatectomy for malignant liver tumors. Surg Endosc 2008; 22 (11) 2350-2356
  • 18 Laurent A, Tayar C, Andréoletti M, Lauzet JY, Merle JC, Cherqui D. Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 2009; 16 (3) 310-314
  • 19 Topal B, Fieuws S, Aerts R, Vandeweyer H, Penninckx F. Laparoscopic versus open liver resection of hepatic neoplasms: comparative analysis of short-term results. Surg Endosc 2008; 22 (10) 2208-2213
  • 20 Dagher I, Proske JM, Carloni A, Richa H, Tranchart H, Franco D. Laparoscopic liver resection: results for 70 patients. Surg Endosc 2007; 21 (4) 619-624
  • 21 Tranchart H, Di Giuro G, Lainas P , et al. Laparoscopic resection for hepatocellular carcinoma: a matched-pair comparative study. Surg Endosc 2010; 24 (5) 1170-1176
  • 22 Viganò L, Tayar C, Laurent A, Cherqui D. Laparoscopic liver resection: a systematic review. J Hepatobiliary Pancreat Surg 2009; 16 (4) 410-421
  • 23 Belli G, Fantini C, D'Agostino A , et al. Laparoscopic versus open liver resection for hepatocellular carcinoma in patients with histologically proven cirrhosis: short- and middle-term results. Surg Endosc 2007; 21 (11) 2004-2011
  • 24 Dagher I, Lainas P, Carloni A , et al. Laparoscopic liver resection for hepatocellular carcinoma. Surg Endosc 2008; 22 (2) 372-378
  • 25 Lai EC, Tang CN, Yang GP, Li MK. Minimally invasive surgical treatment of hepatocellular carcinoma: long-term outcome. World J Surg 2009; 33 (10) 2150-2154
  • 26 Sasaki A, Nitta H, Otsuka K, Takahara T, Nishizuka S, Wakabayashi G. Ten-year experience of totally laparoscopic liver resection in a single institution. Br J Surg 2009; 96 (3) 274-279
  • 27 Fong Y, Brennan MF, Turnbull A, Colt DG, Blumgart LH. Gallbladder cancer discovered during laparoscopic surgery. Potential for iatrogenic tumor dissemination. Arch Surg 1993; 128 (9) 1054-1056
  • 28 Johnstone PA, Rohde DC, Swartz SE, Fetter JE, Wexner SD. Port site recurrences after laparoscopic and thoracoscopic procedures in malignancy. J Clin Oncol 1996; 14 (6) 1950-1956
  • 29 Cherqui D, Laurent A, Mocellin N , et al. Liver resection for transplantable hepatocellular carcinoma: long-term survival and role of secondary liver transplantation. Ann Surg 2009; 250 (5) 738-746
  • 30 Sarpel U, Hefti MM, Wisnievsky JP, Roayaie S, Schwartz ME, Labow DM. Outcome for patients treated with laparoscopic versus open resection of hepatocellular carcinoma: case-matched analysis. Ann Surg Oncol 2009; 16 (6) 1572-1577
  • 31 Shimada M, Hashizume M, Maehara S , et al. Laparoscopic hepatectomy for hepatocellular carcinoma. Surg Endosc 2001; 15 (6) 541-544
  • 32 Cherqui D, Laurent A, Tayar C , et al. Laparoscopic liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: midterm results and perspectives. Ann Surg 2006; 243 (4) 499-506
  • 33 Lee KF, Chong CN, Wong J, Cheung YS, Wong J, Lai P. Long-term results of laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma: a case-matched analysis. World J Surg 2011; 35 (10) 2268-2274
  • 34 Slim A, Garancini M, Di Sandro S , et al. Laparoscopic versus open liver surgery: a single center analysis of post-operative in-hospital and post-discharge results. Langenbecks Arch Surg 2012; 397 (8) 1305-1311
  • 35 Yoon YS, Han HS, Cho JY, Ahn KS. Total laparoscopic liver resection for hepatocellular carcinoma located in all segments of the liver. Surg Endosc 2010; 24 (7) 1630-1637
  • 36 Poon RT, Fan ST, Lo CM , et al. Improving survival results after resection of hepatocellular carcinoma: a prospective study of 377 patients over 10 years. Ann Surg 2001; 234 (1) 63-70
  • 37 Yin Z, Fan X, Ye H, Yin D, Wang J. Short- and long-term outcomes after laparoscopic and open hepatectomy for hepatocellular carcinoma: a global systematic review and meta-analysis. Ann Surg Oncol 2013; 20 (4) 1203-1215
  • 38 Castaing D, Vibert E, Ricca L, Azoulay D, Adam R, Gayet B. Oncologic results of laparoscopic versus open hepatectomy for colorectal liver metastases in two specialized centers. Ann Surg 2009; 250 (5) 849-855
  • 39 Nguyen KT, Laurent A, Dagher I , et al. Minimally invasive liver resection for metastatic colorectal cancer: a multi-institutional, international report of safety, feasibility, and early outcomes. Ann Surg 2009; 250 (5) 842-848
  • 40 Belghiti J, Hiramatsu K, Benoist S, Massault P, Sauvanet A, Farges O. Seven hundred forty-seven hepatectomies in the 1990s: an update to evaluate the actual risk of liver resection. J Am Coll Surg 2000; 191 (1) 38-46
  • 41 Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez PL. Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg 2003; 138 (7) 763-769 , discussion 769
  • 42 Truant S, Bouras AF, Hebbar M , et al. Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc 2011; 25 (11) 3668-3677
  • 43 Gigot JF, Glineur D, Santiago Azagra J , et al; Hepatobiliary and Pancreatic Section of the Royal Belgian Society of Surgery and the Belgian Group for Endoscopic Surgery. Laparoscopic liver resection for malignant liver tumors: preliminary results of a multicenter European study. Ann Surg 2002; 236 (1) 90-97
  • 44 Morino M, Morra I, Rosso E, Miglietta C, Garrone C. Laparoscopic vs open hepatic resection: a comparative study. Surg Endosc 2003; 17 (12) 1914-1918
  • 45 Costi R, Scatton O, Haddad L , et al. Lessons learned from the first 100 laparoscopic liver resections: not delaying conversion may allow reduced blood loss and operative time. J Laparoendosc Adv Surg Tech A 2012; 22 (5) 425-431
  • 46 Kaneko H, Tsuchiya M, Otsuka Y , et al. Laparoscopic hepatectomy for hepatocellular carcinoma in cirrhotic patients. J Hepatobiliary Pancreat Surg 2009; 16 (4) 433-438
  • 47 Dagher I, O'Rourke N, Geller DA , et al. Laparoscopic major hepatectomy: an evolution in standard of care. Ann Surg 2009; 250 (5) 856-860
  • 48 Tzanis D, Shivathirthan N, Laurent A , et al. European experience of laparoscopic major hepatectomy. J Hepatobiliary Pancreat Sci 2013; 20 (2) 120-124
  • 49 Tsai TJ, Chouillard EK, Gumbs AA. Laparoscopic right hepatectomy with intrahepatic transection of the right bile duct. Ann Surg Oncol 2012; 19 (2) 467-468
  • 50 Abu Hilal M, Di Fabio F, Teng MJ, Lykoudis P, Primrose JN, Pearce NW. Single-centre comparative study of laparoscopic versus open right hepatectomy. J Gastrointest Surg 2011; 15 (5) 818-823
  • 51 Dagher I, Di Giuro G, Dubrez J, Lainas P, Smadja C, Franco D. Laparoscopic versus open right hepatectomy: a comparative study. Am J Surg 2009; 198 (2) 173-177
  • 52 Cho JY, Han HS, Yoon YS, Shin SH. Feasibility of laparoscopic liver resection for tumors located in the posterosuperior segments of the liver, with a special reference to overcoming current limitations on tumor location. Surgery 2008; 144 (1) 32-38
  • 53 Huang MT, Lee WJ, Wang W, Wei PL, Chen RJ. Hand-assisted laparoscopic hepatectomy for solid tumor in the posterior portion of the right lobe: initial experience. Ann Surg 2003; 238 (5) 674-679
  • 54 Ishizawa T, Gumbs AA, Kokudo N, Gayet B. Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 2012; 256 (6) 959-964
  • 55 Robles R, Marín C, Abellán B, López A, Pastor P, Parrilla P. A new approach to hand-assisted laparoscopic liver surgery. Surg Endosc 2008; 22 (11) 2357-2364
  • 56 Cho JY, Han HS, Yoon YS, Shin SH. Outcomes of laparoscopic liver resection for lesions located in the right side of the liver. Arch Surg 2009; 144 (1) 25-29
  • 57 Chen KH, Jeng KS, Huang SH, Chu SH. Laparoscopic caudate hepatectomy for cancer—an innovative approach to the no-man's land. J Gastrointest Surg 2013; 17 (3) 522-526
  • 58 Yoon YS, Han HS, Cho JY, Kim JH, Kwon Y. Laparoscopic liver resection for centrally located tumors close to the hilum, major hepatic veins, or inferior vena cava. Surgery 2013; 153 (4) 502-509
  • 59 Wakabayashi G, Nitta H, Takahara T, Shimazu M, Kitajima M, Sasaki A. Standardization of basic skills for laparoscopic liver surgery towards laparoscopic donor hepatectomy. J Hepatobiliary Pancreat Surg 2009; 16 (4) 439-444
  • 60 Buell JF, Gayet B, Han HS , et al. Evaluation of stapler hepatectomy during a laparoscopic liver resection. HPB (Oxford) 2013; ; [Epub ahead of print]
  • 61 Schmandra TC, Mierdl S, Bauer H, Gutt C, Hanisch E. Transoesophageal echocardiography shows high risk of gas embolism during laparoscopic hepatic resection under carbon dioxide pneumoperitoneum. Br J Surg 2002; 89 (7) 870-876
  • 62 Farges O, Jagot P, Kirstetter P, Marty J, Belghiti J. Prospective assessment of the safety and benefit of laparoscopic liver resections. J Hepatobiliary Pancreat Surg 2002; 9 (2) 242-248
  • 63 Vibert E, Perniceni T, Levard H, Denet C, Shahri NK, Gayet B. Laparoscopic liver resection. Br J Surg 2006; 93 (1) 67-72
  • 64 Kluger MD, Vigano L, Barroso R, Cherqui D. The learning curve in laparoscopic major liver resection. J Hepatobiliary Pancreat Sci 2013; 20 (2) 131-136
  • 65 Fong Y, Jarnagin W, Conlon KC, DeMatteo R, Dougherty E, Blumgart LH. Hand-assisted laparoscopic liver resection: lessons from an initial experience. Arch Surg 2000; 135 (7) 854-859
  • 66 Baker TB, Jay CL, Ladner DP , et al. Laparoscopy-assisted and open living donor right hepatectomy: a comparative study of outcomes. Surgery 2009; 146 (4) 817-823 , discussion 823–825
  • 67 Koffron AJ, Kung RD, Baker T, Fryer J, Clark L, Abecassis MM. Laparoscopic-assisted right lobe donor hepatectomy. Am J Transplant 2006; 6 (10) 2522-2525
  • 68 Lin NC, Nitta H, Wakabayashi G. Laparoscopic major hepatectomy: a systematic literature review and comparison of 3 techniques. Ann Surg 2013; 257 (2) 205-213
  • 69 Nagai S, Brown L, Yoshida A, Kim D, Kazimi M, Abouljoud MS. Mini-incision right hepatic lobectomy with or without laparoscopic assistance for living donor hepatectomy. Liver Transpl 2012; 18 (10) 1188-1197
  • 70 Nitta H, Sasaki A, Fujita T , et al. Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 2010; 251 (3) 450-453
  • 71 Soyama A, Takatsuki M, Hidaka M , et al. Standardized less invasive living donor hemihepatectomy using the hybrid method through a short upper midline incision. Transplant Proc 2012; 44 (2) 353-355
  • 72 Idrees K, Bartlett DL. Robotic liver surgery. Surg Clin North Am 2010; 90 (4) 761-774
  • 73 Hanly EJ, Talamini MA. Robotic abdominal surgery. Am J Surg 2004; 188 (4A, Suppl): 19S-26S
  • 74 Ji WB, Wang HG, Zhao ZM, Duan WD, Lu F, Dong JH. Robotic-assisted laparoscopic anatomic hepatectomy in China: initial experience. Ann Surg 2011; 253 (2) 342-348
  • 75 Packiam V, Bartlett DL, Tohme S , et al. Minimally invasive liver resection: robotic versus laparoscopic left lateral sectionectomy. J Gastrointest Surg 2012; 16 (12) 2233-2238
  • 76 Giulianotti PC, Sbrana F, Bianco FM, Addeo P. Robot-assisted laparoscopic extended right hepatectomy with biliary reconstruction. J Laparoendosc Adv Surg Tech A 2010; 20 (2) 159-163
  • 77 Giulianotti PC, Coratti A, Sbrana F , et al. Robotic liver surgery: results for 70 resections. Surgery 2011; 149 (1) 29-39
  • 78 Lai EC, Tang CN, Yang GP, Li MK. Approach to manage the complications of choledochoduodenostomy: robot-assisted laparoscopic Roux-en-Y hepaticojejunostomy. Surg Laparosc Endosc Percutan Tech 2011; 21 (5) e228-e231
  • 79 Lai EC, Tang CN, Li MK. Robot-assisted laparoscopic hemi-hepatectomy: technique and surgical outcomes. Int J Surg 2012; 10 (1) 11-15
  • 80 Pearce NW, Di Fabio F, Teng MJ, Syed S, Primrose JN, Abu Hilal M. Laparoscopic right hepatectomy: a challenging, but feasible, safe and efficient procedure. Am J Surg 2011; 202 (5) e52-e58
  • 81 Cardinal JS, Reddy SK, Tsung A, Marsh JW, Geller DA. Laparoscopic major hepatectomy: pure laparoscopic approach versus hand-assisted technique. J Hepatobiliary Pancreat Sci 2013; 20 (2) 114-119
  • 82 Nitta H, Sasaki A, Otsuka Y, Tsuchiya M, Kaneko H, Wakabayashi G. Impact of hybrid techniques on laparoscopic major hepatectomies. J Hepatobiliary Pancreat Sci 2013; 20 (2) 111-113
  • 83 Belli G, Limongelli P, Fantini C , et al. Laparoscopic and open treatment of hepatocellular carcinoma in patients with cirrhosis. Br J Surg 2009; 96 (9) 1041-1048
  • 84 Ito K, Ito H, Are C , et al. Laparoscopic versus open liver resection: a matched-pair case control study. J Gastrointest Surg 2009; 13 (12) 2276-2283
  • 85 Tsinberg M, Tellioglu G, Simpfendorfer CH , et al. Comparison of laparoscopic versus open liver tumor resection: a case-controlled study. Surg Endosc 2009; 23 (4) 847-853
  • 86 Ker CG, Chen JS, Kuo KK , et al. Liver surgery for hepatocellular carcinoma: laparoscopic versus open approach. Int J Hepatol 2011; 2011: 596792
  • 87 Cannon RM, Scoggins CR, Callender GG, McMasters KM, Martin II RC. Laparoscopic versus open resection of hepatic colorectal metastases. Surgery 2012; 152 (4) 567-573 , discussion 573–574