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  • Review Article
  • Published:

Laparoscopic pancreatic surgery for benign and malignant disease

This article has been updated

Key Points

  • Indications for pancreatic resection do not differ for laparoscopic or open surgery; whether a pancreatic resection can be performed laparoscopically depends on the surgeon's training and experience

  • Most studies on laparoscopic distal pancreatectomy have reported outcomes superior to the open approach, mainly regarding intraoperative blood loss, spleen preservation, length of stay and overall costs

  • Laparoscopic Whipple has similar outcomes to the open approach, although inferior outcomes have been associated with the initial learning curve phase and when this procedure is performed in low-volume hospitals

  • Laparoscopic pancreatic surgery is associated with a considerable learning curve effect, necessitating structured introduction by trained surgeons and substantial case volumes per centre

  • Randomized data are needed before drawing conclusions on definite benefits of a laparoscopic approach; the first randomized controlled trials on laparoscopic pancreatic surgery are ongoing

Abstract

Laparoscopic surgery for benign and malignant pancreatic lesions has slowly been gaining acceptance over the past decade and is being introduced in many centres. Some studies suggest that this approach is equivalent to or better than open surgery, but randomized data are needed to assess outcomes. In this Review, we aim to provide a comprehensive overview of the state of the art in laparoscopic pancreatic surgery by aggregating high-quality published evidence. Various aspects, including the benefits, limitations, oncological efficacy, learning curve and latest innovations, are discussed. The focus is on laparoscopic Whipple procedure and laparoscopic distal pancreatectomy for both benign and malignant disease, but robot-assisted surgery is also addressed. Surgical and oncological outcomes are discussed as well as quality of life parameters and the cost efficiency of laparoscopic pancreatic surgery. We have also included decision-aid algorithms based on the literature and our own expertise; these algorithms can assist in the decision to perform a laparoscopic or open procedure.

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Figure 1: Anatomical structures involved in pancreatic surgery.
Figure 2: Decision-aid algorithm for laparoscopic Whipple.
Figure 3: Decision-aid algorithm for laparoscopic distal pancreatectomy.
Figure 4: Techniques for spleen-preserving distal pancreatectomy.

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Change history

  • 18 February 2016

    In the version of this article initially published online, the first sentence of the abstract misspelled "Laparoscopic". This error has now been corrected in the HTML and PDF versions of this article.

References

  1. Tol, J. A. et al. Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS). Surgery 156, 591–600 (2014).

    Article  PubMed  Google Scholar 

  2. Torre, L. A. et al. Global cancer statistics, 2012. CA Cancer J. Clin. 65, 87–108 (2015).

    Article  PubMed  Google Scholar 

  3. Howlader, N. et al. SEER Cancer Statistics Review, 1975–2011. National Cancer Institute [online], (2014).

    Google Scholar 

  4. Rahib, L. et al. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 74, 2913–2921 (2014).

    Article  CAS  PubMed  Google Scholar 

  5. Bilimoria, K. Y. et al. National failure to operate on early stage pancreatic cancer. Ann. Surg. 246, 173–180 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ryan, D. P., Hong, T. S. & Bardeesy, N. Pancreatic adenocarcinoma. N. Engl. J. Med. 371, 1039–1049 (2014).

    Article  CAS  PubMed  Google Scholar 

  7. Hartwig, W., Werner, J., Jäger, D., Debus, J. & Büchler, M. W. Improvement of surgical results for pancreatic cancer. Lancet Oncol. 14, e476–e485 (2013).

    Article  PubMed  Google Scholar 

  8. Marangos, I. P. et al. Laparoscopic resection of exocrine carcinoma in central and distal pancreas results in a high rate of radical resections and long postoperative survival. Surgery 151, 717–723 (2012).

    Article  PubMed  Google Scholar 

  9. Kooby, D. A. et al. A multicenter analysis of distal pancreatectomy for adenocarcinoma: is laparoscopic resection appropriate? J. Am. Coll. Surg. 210, 779–785 (2010).

    Article  PubMed  Google Scholar 

  10. de Rooij, T. et al. Outcomes of distal pancreatectomy for pancreatic ductal adenocarcinoma in the Netherlands: a nationwide retrospective analysis. Ann. Surg. Oncol. 23, 585–591 (2012).

    Article  Google Scholar 

  11. Luo, J., Xiao, L., Wu, C., Zheng, Y. & Zhao, N. The incidence and survival rate of population-based pancreatic cancer patients: Shanghai Cancer Registry 2004–2009. PLoS ONE 8, e76052 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Distler, M. et al. Evaluation of survival in patients after pancreatic head resection for ductal adenocarcinoma. BMC Surg. 13, 12 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Bliss, L. A., Witkowski, E. R., Yang, C. J. & Tseng, J. F. Outcomes in operative management of pancreatic cancer. J. Surg. Oncol. 110, 592–598 (2014).

    Article  PubMed  Google Scholar 

  14. Haeno, H. et al. Computational modeling of pancreatic cancer reveals kinetics of metastasis suggesting optimum treatment strategies. Cell 148, 362–375 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nigri, G. R. et al. Metaanalysis of trials comparing minimally invasive and open distal pancreatectomies. Surg. Endosc. 25, 1642–1651 (2011).

    Article  PubMed  Google Scholar 

  16. Jin, T. et al. A systematic review and meta-analysis of studies comparing laparoscopic and open distal pancreatectomy. HPB (Oxford) 14, 711–724 (2012).

    Article  Google Scholar 

  17. Jusoh, A. C. & Ammori, B. J. Laparoscopic versus open distal pancreatectomy: a systematic review of comparative studies. Surg. Endosc. 26, 904–913 (2012).

    Article  PubMed  Google Scholar 

  18. Pericleous, S., Middleton, N., McKay, S. C., Bowers, K. A. & Hutchins, R. R. Systematic review and meta-analysis of case-matched studies comparing open and laparoscopic distal pancreatectomy: is it a safe procedure? Pancreas 41, 993–1000 (2012).

    Article  PubMed  Google Scholar 

  19. Sui, C. J., Li, B., Yang, J. M., Wang, S. J. & Zhou, Y. M. Laparoscopic versus open distal pancreatectomy: a meta-analysis. Asian J. Surg. 35, 1–8 (2012).

    Article  PubMed  Google Scholar 

  20. Venkat, R. et al. Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann. Surg. 255, 1048–1059 (2012).

    Article  PubMed  Google Scholar 

  21. Nakamura, M. & Nakashima, H. Laparoscopic distal pancreatectomy and pancreatoduodenectomy: is it worthwhile? A meta-analysis of laparoscopic pancreatectomy. J. Hepatobiliary Pancreat. Sci. 20, 421–428 (2013).

    Article  PubMed  Google Scholar 

  22. Drymousis, P. et al. Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford) 16, 397–406 (2014).

    Article  Google Scholar 

  23. Mehrabi, A. et al. A systematic review and meta-analysis of laparoscopic versus open distal pancreatectomy for benign and malignant lesions of the pancreas: it's time to randomize. Surgery 157, 45–55 (2015).

    Article  PubMed  Google Scholar 

  24. Boggi, U. et al. Laparoscopic pancreaticoduodenectomy: a systematic literature review. Surg. Endosc. 29, 9–23 (2015).

    Article  PubMed  Google Scholar 

  25. Strijker, M. et al. Robot-assisted pancreatic surgery: a systematic review of the literature. HPB (Oxford) 15, 1–10 (2013).

    Article  Google Scholar 

  26. Correa-Gallego, C. et al. Minimally-invasive versus open pancreaticoduodenectomy: systematic review and meta-analysis. J. Am. Coll. Surg. 218, 129–139 (2014).

    Article  PubMed  Google Scholar 

  27. Ammori, B. J. & Ayiomamitis, G. D. Laparoscopic pancreaticoduodenectomy and distal pancreatectomy: a UK experience and a systematic review of the literature. Surg. Endosc. 25, 2084–2099 (2011).

    Article  PubMed  Google Scholar 

  28. Cuschieri, A. Laparoscopic surgery of the pancreas. J. R. Coll. Surg. Edinb. 39, 178–184 (1994).

    CAS  PubMed  Google Scholar 

  29. Gagner, M. & Pomp, A. Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg. Endosc. 8, 408–410 (1994).

    Article  CAS  PubMed  Google Scholar 

  30. Gagner, M. & Pomp, A. Laparoscopic pancreatic resection: is it worthwhile? J. Gastrointest. Surg. 1, 20–25 (1997).

    Article  CAS  PubMed  Google Scholar 

  31. Croome, K. P. et al. Pancreaticoduodenectomy with major vascular resection: a comparison of laparoscopic versus open approaches. J. Gastrointest. Surg. 19, 189–194 (2015).

    Article  PubMed  Google Scholar 

  32. Kendrick, M. L. & Sclabas, G. M. Major venous resection during total laparoscopic pancreaticoduodenectomy. HPB (Oxford) 13, 454–458 (2011).

    Article  Google Scholar 

  33. Lee, J. S. et al. Laparoscopic pancreaticoduodenectomy assisted by mini-laparotomy. Surg. Laparosc. Endosc. Percutan. Tech. 23, e98–e102 (2013).

    Article  PubMed  Google Scholar 

  34. Palanivelu, C. et al. Laparoscopic pancreaticoduodenectomy: technique and outcomes. J. Am. Coll. Surg. 205, 222–230 (2007).

    Article  PubMed  Google Scholar 

  35. Corcione, F. et al. Laparoscopic pancreaticoduodenectomy: experience of 22 cases. Surg. Endosc. 27, 2131–2136 (2013).

    Article  PubMed  Google Scholar 

  36. Langan, R. C. et al. Laparoscopic-assisted versus open pancreaticoduodenectomy: early favorable physical quality-of-life measures. Surgery 156, 379–384 (2014).

    Article  PubMed  Google Scholar 

  37. Buchs, N. C. et al. Outcomes of robot-assisted pancreaticoduodenectomy in patients older than 70 years: a comparative study. World J. Surg. 34, 2109–2114 (2010).

    Article  PubMed  Google Scholar 

  38. Lai, E. C., Yang, G. P. & Tang, C. N. Robot-assisted laparoscopic pancreaticoduodenectomy versus open pancreaticoduodenectomy — a comparative study. Int. J. Surg. 10, 475–479 (2012).

    Article  PubMed  Google Scholar 

  39. Boggi, U. et al. Feasibility of robotic pancreaticoduodenectomy. Br. J. Surg. 100, 917–925 (2013).

    Article  CAS  PubMed  Google Scholar 

  40. Wellner, U. F. et al. Hybrid laparoscopic versus open pylorus-preserving pancreatoduodenectomy: retrospective matched case comparison in 80 patients. Langenbecks Arch. Surg. 399, 849–856 (2014).

    Article  PubMed  Google Scholar 

  41. Palanivelu, C. et al. Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J. Hepatobiliary Pancreat. Surg. 16, 731–740 (2009).

    Article  CAS  PubMed  Google Scholar 

  42. Magge, D. et al. Comparative effectiveness of minimally invasive and open distal pancreatectomy for ductal adenocarcinoma. JAMA Surg. 148, 525–531 (2013).

    Article  PubMed  Google Scholar 

  43. Cho, C. S. et al. Laparoscopic versus open left pancreatectomy: can preoperative factors indicate the safer technique? Ann. Surg. 253, 975–980 (2011).

    Article  PubMed  Google Scholar 

  44. Croome, K. P. et al. Total laparoscopic pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: oncologic advantages over open approaches? Ann. Surg. 260, 633–638 (2014).

    Article  PubMed  Google Scholar 

  45. Kendrick, M. L. & Cusati, D. Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch. Surg. 145, 19–23 (2010).

    Article  PubMed  Google Scholar 

  46. Jensen, R. T. et al. ENETS Consensus Guidelines for the management of patients with digestive neuroendocrine neoplasms: functional pancreatic endocrine tumor syndromes. Neuroendocrinology 95, 98–119 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kulke, M. H. et al. NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas 39, 735–752 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Tanaka, M. et al. International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology 12, 183–197 (2012).

    Article  PubMed  Google Scholar 

  49. Del Chiaro, M. et al. European experts consensus statement on cystic tumours of the pancreas. Dig. Liver Dis. 45, 703–711 (2013).

    Article  PubMed  Google Scholar 

  50. Vege, S. S., Ziring, B., Jain, R., Moayyedi, P. & Clinical Guidelines Committee. American Gastroenterological Association institute guideline on the diagnosis and management of asymptomatic neopastic pancreatic cysts. Gastroenterology 148, 819–822 (2015).

    Article  PubMed  Google Scholar 

  51. Lee, S. H. et al. Minimally invasive RAMPS in well-selected left-sided pancreatic cancer within Yonsei criteria: long-term (>median 3 years) oncologic outcomes. Surg. Endosc. 28, 2848–2855 (2014).

    Article  PubMed  Google Scholar 

  52. Strasberg, S. M., Drebin, J. A. & Linehan, D. Radical antegrade modular pancreatosplenectomy. Surgery 133, 521–527 (2003).

    Article  PubMed  Google Scholar 

  53. Strasberg, S. M., Linehan, D. C. & Hawkins, W. G. Radical antegrade modular pancreatosplenectomy procedure for adenocarcinoma of the body and tail of the pancreas: ability to obtain negative tangential margins. J. Am. Coll. Surg. 204, 244–249 (2007).

    Article  PubMed  Google Scholar 

  54. Strasberg, S. M. & Fields, R. Left-sided pancreatic cancer: distal pancreatectomy and its variants: radical antegrade modular pancreatosplenectomy and distal pancreatectomy with celiac axis resection. Cancer J. 18, 562–570 (2012).

    Article  PubMed  Google Scholar 

  55. Mitchem, J. B. et al. Long-term results of resection of adenocarcinoma of the body and tail of the pancreas using radical antegrade modular pancreatosplenectomy procedure. J. Am. Coll. Surg. 214, 46–52 (2012).

    Article  PubMed  Google Scholar 

  56. Kang, C. M., Lee, S. H. & Lee, W. J. Minimally invasive radical pancreatectomy for left-sided pancreatic cancer: current status and future perspectives. World J. Gastroenterol. 20, 2343–2351 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Choi, S. H., Seo, M. A., Hwang, H. K., Kang, C. M. & Lee, W. J. Is it worthwhile to preserve adult spleen in laparoscopic distal pancreatectomy? Perioperative and patient-reported outcome analysis. Surg. Endosc. 26, 3149–3156 (2012).

    Article  PubMed  Google Scholar 

  58. Nau, P. et al. Laparoscopic distal pancreatectomy with splenic conservation: an operation without increased morbidity. Gastroenterol. Res. Pract. 2009, 846340 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Kimura, W. et al. Spleen-preserving distal pancreatectomy with conservation of the splenic artery and vein. Surgery 120, 885–890 (1996).

    Article  CAS  PubMed  Google Scholar 

  60. Jain, G., Chakravartty, S. & Patel, A. G. Spleen-preserving distal pancreatectomy with and without splenic vessel ligation: a systematic review. HPB (Oxford) 15, 403–410 (2013).

    Article  Google Scholar 

  61. Yoon, Y. S., Lee, K. H., Han, H. S., Cho, J. Y. & Ahn, K. S. Patency of splenic vessels after laparoscopic spleen and splenic vessel-preserving distal pancreatectomy. Br. J. Surg. 96, 633–640 (2009).

    Article  PubMed  Google Scholar 

  62. Yoon, Y. S. et al. Effects of laparoscopic versus open surgery on splenic vessel patency after spleen and splenic vessel-preserving distal pancreatectomy: a retrospective multicenter study. Surg. Endosc. 29, 583–588 (2015).

    Article  PubMed  Google Scholar 

  63. Nakamura, M. et al. Lateral approach for laparoscopic splenic vessel-preserving distal pancreatectomy. Surgery 150, 326–331 (2011).

    Article  PubMed  Google Scholar 

  64. Warshaw, A. L. Conservation of the spleen with distal pancreatectomy. Arch. Surg. 123, 550–553 (1988).

    Article  CAS  PubMed  Google Scholar 

  65. Adam, J. P. et al. Laparoscopic spleen-preserving distal pancreatectomy: splenic vessel preservation compared with the Warshaw technique. JAMA Surg. 148, 246–252 (2013).

    Article  Google Scholar 

  66. Matsushima, H. et al. Laparoscopic spleen-preserving distal pancreatectomy with and without splenic vessel preservation: the role of the Warshaw procedure. Pancreatology 14, 530–535 (2014).

    Article  PubMed  Google Scholar 

  67. Chalikonda, S., Aguilar-Saavedra, J. R. & Walsh, R. M. Laparoscopic robotic-assisted pancreaticoduodenectomy: a case-matched comparison with open resection. Surg. Endosc. 26, 2397–2402 (2012).

    Article  CAS  PubMed  Google Scholar 

  68. Song, K. B. et al. Matched case-control analysis comparing laparoscopic and open pylorus-preserving pancreaticoduodenectomy in patients with periampullary tumors. Ann. Surg. 262, 146–155 (2015).

    Article  PubMed  Google Scholar 

  69. Dokmak, S. et al. Laparoscopic pancreaticoduodenectomy should not be routine for resection of periampullary tumors. J. Am. Coll. Surg. 220, 831–838 (2015).

    Article  PubMed  Google Scholar 

  70. Boone, B. A. et al. Assessment of quality outcomes for robotic pancreaticoduodenectomy: identification of the learning curve. JAMA Surg. 150, 416–422 (2015).

    Article  PubMed  Google Scholar 

  71. Asbun, H. J. & Stauffer, J. A. Laparoscopic versus open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System. J. Am. Coll. Surg. 215, 810–819 (2012).

    Article  PubMed  Google Scholar 

  72. Kuroki, T., Adachi, T., Okamoto, T. & Kanematsu, T. A non-randomized comparative study of laparoscopy-assisted pancreaticoduodenectomy and open pancreaticoduodenectomy. Hepatogastroenterology 59, 570–573 (2012).

    Article  PubMed  Google Scholar 

  73. Mesleh, M. G., Stauffer, J. A., Bowers, S. P. & Asbun, H. J. Cost analysis of open and laparoscopic pancreaticoduodenectomy: a single institution comparison. Surg. Endosc. 27, 4518–4523 (2013).

    Article  PubMed  Google Scholar 

  74. Speicher, P. J. et al. Defining the learning curve for team-based laparoscopic pancreaticoduodenectomy. Ann. Surg. Oncol. 21, 4014–4019 (2014).

    Article  PubMed  Google Scholar 

  75. Abdelgadir Adam, M. et al. Minimally invasive versus open pancreaticoduodenectomy for cancer: practice patterns and short-term outcomes among 7061 patients. Ann. Surg. 262, 372–377 (2015).

    Article  Google Scholar 

  76. Sharpe, S. M. et al. Early national experience with laparoscopic pancreaticoduodenectomy for ductal adenocarcinoma: a comparison of laparoscopic pancreaticoduodenectomy and open pancreaticoduodenectomy from the National Cancer Data Base. J. Am. Coll. Surg. 221, 175–184 (2015).

    Article  PubMed  Google Scholar 

  77. World Health Organization. International Clinical Trials Registry Platform [online], (2015).

  78. de Rooij, T. et al. A nationwide comparison of laparoscopic and open distal pancreatectomy for benign and malignant disease. J. Am. Coll. Surg. 220, 263–270 (2015).

    Article  PubMed  Google Scholar 

  79. Nakamura, M. et al. Multicenter comparative study of laparoscopic and open distal pancreatectomy using propensity score-matching. J. Hepatobiliary Pancreat. Sci. 22, 731–736 (2015).

    Article  PubMed  Google Scholar 

  80. Abu Hilal, M., Hamdan, M., Di Fabio, F., Pearce, N. W. & Johnson, C. D. Laparoscopic versus open distal pancreatectomy: a clinical and cost-effectiveness study. Surg. Endosc. 26, 1670–1674 (2012).

    Article  PubMed  Google Scholar 

  81. Fox, A. M. et al. Comparison of outcomes and costs between laparoscopic distal pancreatectomy and open resection at a single center. Surg. Endosc. 26, 1220–1230 (2012).

    Article  PubMed  Google Scholar 

  82. Braga, M. et al. Results of 100 consecutive laparoscopic distal pancreatectomies: postoperative outcome, cost-benefit analysis, and quality of life assessment. Surg. Endosc. 29, 1871–1878 (2015).

    Article  PubMed  Google Scholar 

  83. Eom, B. W. et al. Clinical outcomes compared between laparoscopic and open distal pancreatectomy. Surg. Endosc. 22, 1334–1338 (2008).

    Article  CAS  PubMed  Google Scholar 

  84. Abu Hilal, M., Jain, G., Kasasbeh, F., Zuccaro, M. & Elberm, H. Laparoscopic distal pancreatectomy: critical analysis of preliminary experience from a tertiary referral centre. Surg. Endosc. 23, 2743–2747 (2009).

    Article  PubMed  Google Scholar 

  85. Adam, M. A. et al. Minimally invasive distal pancreatectomy for cancer: short-term oncologic outcomes in 1,733 patients. World J. Surg. 39, 2564–2572 (2015).

    Article  PubMed  Google Scholar 

  86. Sharpe, S. M. et al. The laparoscopic approach to distal pancreatectomy for ductal adenocarcinoma results in shorter lengths of stay without compromising oncologic outcomes. Am. J. Surg. 209, 557–563 (2015).

    Article  PubMed  Google Scholar 

  87. Shin, S. H. et al. A comparative study of laparoscopic versus open distal pancreatectomy for left-sided ductal adenocarcinoma: a propensity score-matched analysis. J. Am. Coll. Surg. 220, 177–185 (2015).

    Article  PubMed  Google Scholar 

  88. Sulpice, L. et al. Laparoscopic distal pancreatectomy for pancreatic ductal adenocarcinoma: time for a randomized controlled trial? Results of an all-inclusive national observational study. Ann. Surg. 262, 868–874 (2015).

    Article  PubMed  Google Scholar 

  89. World Health Organization. International Clinical Trials Registry Platform [online], (2015).

  90. World Health Organization. International Clinical Trials Registry Platform [online], (2015).

  91. Jayaraman, S. et al. Laparoscopic distal pancreatectomy: evolution of a technique at a single institution. J. Am. Coll. Surg. 211, 503–509 (2010).

    Article  PubMed  Google Scholar 

  92. Vijan, S. S. et al. Laparoscopic versus open distal pancreatectomy: a single-insitution comparative study. Arch. Surg. 145, 616–621 (2010).

    Article  PubMed  Google Scholar 

  93. Richardson, J. et al. Implementation of enhanced recovery programme for laparoscopic distal pancreatectomy: feasibility, safety and cost analysis. Pancreatology 15, 185–190 (2015).

    Article  PubMed  Google Scholar 

  94. Waters, J. A. et al. Robotic distal pancreatectomy: cost effective? Surgery 148, 814–823 (2010).

    Article  PubMed  Google Scholar 

  95. Rutz, D. R. et al. Cost comparison analysis of open versus laparoscopic distal pancreatectomy. HPB (Oxford) 16, 907–914 (2014).

    Article  Google Scholar 

  96. Ricci, C. et al. Laparoscopic distal pancreatectomy in benign or premalignant pancreatic lesions: is it really more cost-effective than open approach? J. Gastrointest. Surg. 19, 1415–1424 (2015).

    Article  PubMed  Google Scholar 

  97. Tran Cao, H. S. et al. Improved perioperative outcomes with minimally invasive distal pancreatectomy: results from a population-based analysis. JAMA Surg. 149, 237–243 (2014).

    Article  PubMed  Google Scholar 

  98. Braga, M. et al. Learning curve for laparoscopic distal pancreatectomy in a high-volume hospital. Updates Surg. 64, 179–183 (2012).

    Article  PubMed  Google Scholar 

  99. Napoli, N. et al. The learning curve in robotic distal pancreatectomy. Updates Surg. 67, 257–264 (2015).

    Article  PubMed  Google Scholar 

  100. Ricci, C. et al. Laparoscopic distal pancreatectomy: what factors are related to the learning curve? Surg. Today 45, 50–56 (2015).

    Article  PubMed  Google Scholar 

  101. Kim, S. C. et al. Short-term clinical outcomes for 100 consecutive cases of laparoscopic pylorus-preserving pancreatoduodenectomy: improvement with surgical experience. Surg. Endosc. 27, 95–103 (2013).

    Article  PubMed  Google Scholar 

  102. Bao, P. Q., Mazirka, P. O. & Watkins, K. T. Retrospective comparison of robot-assisted minimally invasive versus open pancreaticoduodenectomy for periampullary neoplasms. J. Gastrointest. Surg. 18, 682–689 (2014).

    Article  PubMed  Google Scholar 

  103. Zureikat, A. H., Breaux, J. A., Steel, J. L. & Hughes, S. J. Can laparoscopic pancreaticoduodenectomy be safely implemented? J. Gastrointest. Surg. 15, 1151–1157 (2011).

    Article  PubMed  Google Scholar 

  104. Topal, B., Van de Sande, S., Fieuws, S. & Penninckx, F. Effect of centralization of pancreaticoduodenectomy on nationwide hospital mortality and length of stay. Br. J. Surg. 94, 1377–1381 (2007).

    Article  CAS  PubMed  Google Scholar 

  105. Balzano, G. et al. Effect of hospital volume on outcome of pancreaticoduodenectomy in Italy. Br. J. Surg. 95, 357–362 (2008).

    Article  CAS  PubMed  Google Scholar 

  106. Elberm, H. et al. Outcome after pancreaticoduodenectomy for T3 adenocarcinoma: a multivariable analysis from the UK Vascular Resection for Pancreatic Cancer Study Group. Eur. J. Surg. Oncol. 41, 1500–1507 (2015).

    Article  CAS  PubMed  Google Scholar 

  107. de Wilde, R. F. et al. Impact of nationwide centralization of pancreaticoduodenectomy on hospital mortality. Br. J. Surg. 993, 404–410 (2012).

    Article  Google Scholar 

  108. Broeders, I. A. Robotics: the next step? Best Pract. Res. Clin. Gastroenterol. 28, 225–232 (2014).

    Article  PubMed  Google Scholar 

  109. Butturini, G. et al. A prospective non-randomised single-center study comparing laparoscopic and robotic distal pancreatectomy. Surg. Endosc. 29, 3163–3170 (2015).

    Article  PubMed  Google Scholar 

  110. Kang, C. M., Kim, D. H., Lee, W. J. & Chi, H. S. Conventional laparoscopic and robot-assisted spleen-preserving pancreatectomy: does da Vinci have clinical advantages? Surg. Endosc. 25, 2004–2009 (2011).

    Article  PubMed  Google Scholar 

  111. Daouadi, M. et al. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann. Surg. 257, 128–132 (2013).

    Article  PubMed  Google Scholar 

  112. Cirocchi, R. et al. Current status of robotic distal pancreatectomy: a systematic review. Surg. Oncol. 22, 201–207 (2013).

    Article  PubMed  Google Scholar 

  113. Zureikat, A. H. et al. 250 robotic pancreatic resections: safety and feasibility. Ann. Surg. 258, 554–559 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  114. Chen, S. et al. Robotic approach improves spleen-preserving rate and shortens postoperative hospital stay of laparoscopic distal pancreatectomy: a matched cohort study. Surg. Endosc. 29, 3507–3518 (2015).

    Article  PubMed  Google Scholar 

  115. Lee, S. Y. et al. Distal pancreatectomy: a single institution's experience in open, laparoscopic, and robotic approaches. J. Am. Coll. Surg. 220, 18–27 (2015).

    Article  PubMed  Google Scholar 

  116. Dokmak, S., Aussilhou, B., Ftériche, F. S., Sauvanet, A. & Belghiti, J. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann. Surg. http://dx.doi.org/10.1097/SLA.0000000000001020 (2016).

  117. Kang, C. M. Is robot-assisted minimally invasive distal pancreatectomy superior to the laparoscopic technique? Ann. Surg. 261, e153–e154 (2015).

    Article  PubMed  Google Scholar 

  118. Giulianotti, P. C. et al. Robot-assisted laparoscopic pancreatic surgery: single-surgeon experience. Surg. Endosc. 24, 1646–1657 (2010).

    Article  PubMed  Google Scholar 

  119. Shakir, M. et al. The learning curve for robotic distal pancreatectomy: an analysis of outcomes of the first 100 consecutive cases at a high-volume pancreatic centre. HPB (Oxford) 17, 580–586 (2015).

    Article  Google Scholar 

  120. Suman, P., Rutledge, J. & Yiengpruksawan, A. Robotic distal pancreatectomy. JSLS 17, 627–635 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  121. Heemskerk, J., Bouvy, N. D. & Baeten, C. G. The end of robot-assisted laparoscopy? A critical appraisal of scientific evidence on the use of robot-assisted laparoscopic surgery. Surg. Endosc. 28, 1388–1398 (2014).

    Article  PubMed  Google Scholar 

  122. Khaled, Y. S. et al. A case-matched comparative study of laparoscopic versus open distal pancreatectomy. Surg. Laparosc. Endosc. Percutan. Tech. 25, 363–367 (2015).

    Article  PubMed  Google Scholar 

  123. Kooby, D. A. et al. Left-sided pancreatectomy: a multicenter comparison of laparoscopic and open approaches. Ann. Surg. 248, 438–446 (2008).

    PubMed  Google Scholar 

  124. Xourafas, D., Tavakkoli, A., Clancy, T. E. & Ashley, S. W. Distal pancreatic resection for neuroendocrine tumors: is laparoscopic really better than open? J. Gastrointest. Surg. 19, 831–840 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

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All authors researched data for the article and provided a substantial contribution to discussion of the content. T.d.R. and S.K. wrote the article. M.A.H., M.L.K., O.R.B. and M.G.B. contributed to reviewing and editing the manuscript before submission.

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Correspondence to Marc G. Besselink.

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Competing interests

T.d.R., O.R.B. and M.G.B. received educational grants from Ethicon (Johnson & Johnson Medical) to perform a nationwide training programme in laparoscopic pancreatic surgery (NLEG00569, BNLEA00021, BNLEA00065) and a research grant from Ethicon (Johnson & Johnson Medical) to perform a randomized controlled multicentre trial on laparoscopic versus open distal pancreatectomy (IIS 14–702). S.K., M.A.H. and M.L.K. declare no competing interests.

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de Rooij, T., Klompmaker, S., Hilal, M. et al. Laparoscopic pancreatic surgery for benign and malignant disease. Nat Rev Gastroenterol Hepatol 13, 227–238 (2016). https://doi.org/10.1038/nrgastro.2016.17

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