Laparoscopic versus open pancreaticoduodenectomy for pancreatic neuroendocrine tumors: a single-center experience

  • Hanbaro Kim
  • Ki Byung Song
  • Dae Wook Hwang
  • Jae Hoon Lee
  • Shadi Alshammary
  • Song Cheol KimEmail author



The efficacy and outcomes of laparoscopic resection for pancreatic neuroendocrine tumors (PNETs) are well established; however, specific data regarding the outcomes of laparoscopic pancreaticoduodenectomy (L-PD) are limited. The purpose of the present study was to compare the clinical and oncological outcomes following L-PD versus open PD (O-PD) in patients with PNETs.


This retrospective study included 149 patients with PNETs who underwent PD at the Asan Medical Center between January 2006 and December 2017. In 58 patients, a laparoscopic approach was used (L-PD group), and in 91, an open technique was used (O-PD group).


The mean operative time was longer in the L-PD group than in the O-PD group (417.4 min vs. 362.2 min; p = 0.002), and the mean duration of postoperative stay was shorter in the L-PD group (12.6 days vs. 17.8 days; p < 0.001). The estimated blood loss (433.2 ml vs. 415.0 ml; p = 0.824) and the overall complication rate (34.5% vs. 38.5%; p = 0.624) did not significantly differ between the two groups. Regarding the oncological outcomes, there were no significant differences in the resection margins, tumor size, tumor grading, or T/N stage. The number of harvested lymph nodes in the L-PD group was lower than that in the O-PD group (7.1 vs. 10.8; p = 0.002). The 3-year overall survival rate was 91.9% in the L-PD group and 93.6% in the O-PD group (p = 0.974). The 3-year disease-free survival rate was 94.8% in the L-PD group and 86.7% in the O-PD group (p = 0.225).


L-PD is feasible for the treatment of PNETs in selected patients and has the advantages of short recovery time and reduced hospital stay. The survival rate was similar in both groups; however, due to the difference in the harvested lymph nodes, a randomized trial should confirm the oncological safety of L-PD for PNETs.


Pancreatic NET Laparoscopy Pancreaticoduodenectomy 



This study was supported by a Grant of the Korean Health Technology R&D Project, Ministry of Health & Welfare, South Korea (Grant Number: HI14C2640).

Compliance with ethical standards


Hanbaro Kim, Ki Byung Song, Dae Wook Hwang, Jae Hoon Lee, Shadi Alshammary, and Song Cheol Kim have no conflicts of interest or financial ties to disclose.


  1. 1.
    Halfdanarson TR, Rubin J, Farnell MB, Grant CS, Petersen GM (2008) Pancreatic endocrine neoplasms: epidemiology and prognosis of pancreatic endocrine tumors. Endocr Relat Cancer 15:409–427CrossRefGoogle Scholar
  2. 2.
    Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey JN, Rashid A, Evans DB (2008) One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol 26:3063–3072CrossRefGoogle Scholar
  3. 3.
    Ekeblad S, Skogseid B, Dunder K, Oberg K, Eriksson B (2008) Prognostic factors and survival in 324 patients with pancreatic endocrine tumor treated at a single institution. Clin Cancer Res 14:7798–7803CrossRefGoogle Scholar
  4. 4.
    Sadot E, Reidy-Lagunes DL, Tang LH, Do RK, Gonen M, D’Angelica MI, DeMatteo RP, Kingham TP, Groot Koerkamp B, Untch BR, Brennan MF, Jarnagin WR, Allen PJ (2016) Observation versus resection for small asymptomatic pancreatic neuroendocrine tumors: a matched case-control study. Ann Surg Oncol 23:1361–1370CrossRefGoogle Scholar
  5. 5.
    Spolverato G, Bagante F, Aldrighetti L, Poultsides G, Bauer TW, Field RC, Marques HP, Weiss M, Maithel SK, Pawlik TM (2017) Neuroendocrine liver metastasis: prognostic implications of primary tumor site on patients undergoing curative intent liver surgery. J Gastrointest Surg 21:2039–2047CrossRefGoogle Scholar
  6. 6.
    Cheema A, Weber J, Strosberg JR (2012) Incidental detection of pancreatic neuroendocrine tumors: an analysis of incidence and outcomes. Ann Surg Oncol 19:2932–2936CrossRefGoogle Scholar
  7. 7.
    Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410CrossRefGoogle Scholar
  8. 8.
    Cho CS, Kooby DA, Schmidt CM, Nakeeb A, Bentrem DJ, Merchant NB, Parikh AA, Martin RC 2nd, Scoggins CR, Ahmad SA, Kim HJ, Hamilton N, Hawkins WG, Weber SM (2011) Laparoscopic versus open left pancreatectomy: can preoperative factors indicate the safer technique? Ann Surg 253:975–980CrossRefGoogle Scholar
  9. 9.
    Jusoh AC, Ammori BJ (2012) Laparoscopic versus open distal pancreatectomy: a systematic review of comparative studies. Surg Endosc 26:904–913CrossRefGoogle Scholar
  10. 10.
    Al-Taan OS, Stephenson JA, Briggs C, Pollard C, Metcalfe MS, Dennison AR (2010) Laparoscopic pancreatic surgery: a review of present results and future prospects. HPB 12:239–243CrossRefGoogle Scholar
  11. 11.
    Song KB, Kim SC, Park JB, Kim YH, Jung YS, Kim MH, Lee SK, Seo DW, Lee SS, Park DH, Han DJ (2011) Single-center experience of laparoscopic left pancreatic resection in 359 consecutive patients: changing the surgical paradigm of left pancreatic resection. Surg Endosc 25:3364–3372CrossRefGoogle Scholar
  12. 12.
    Xie K, Zhu YP, Xu XW, Chen K, Yan JF, Mou YP (2012) Laparoscopic distal pancreatectomy is as safe and feasible as open procedure: a meta-analysis. World J Gastroenterol 18:1959–1967CrossRefGoogle Scholar
  13. 13.
    Drymousis P, Raptis DA, Spalding D, Fernandez-Cruz L, Menon D, Breitenstein S, Davidson B, Frilling A (2014) Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB 16:397–406CrossRefGoogle Scholar
  14. 14.
    Tamburrino D, Partelli S, Renzi C, Crippa S, Muffatti F, Perali C, Parisi A, Randolph J, Fusai GK, Cirocchi R, Falconi M (2017) Systematic review and meta-analysis on laparoscopic pancreatic resections for neuroendocrine neoplasms (PNENs). Expert Rev Gastroenterol Hepatol 11:65–73CrossRefGoogle Scholar
  15. 15.
    Han SH, Han IW, Heo JS, Choi SH, Choi DW, Han S, You YH (2018) Laparoscopic versus open distal pancreatectomy for nonfunctioning pancreatic neuroendocrine tumors: a large single-center study. Surg Endosc 32:443–449CrossRefGoogle Scholar
  16. 16.
    Song KB, Kim SC, Hwang DW, Lee JH, Lee DJ, Lee JW, Park KM, Lee YJ (2015) Matched case-control analysis comparing laparoscopic and open pylorus-preserving pancreaticoduodenectomy in patients with periampullary tumors. Ann Surg 262:146–155CrossRefGoogle Scholar
  17. 17.
    Lee CS, Kim EY, You YK, Hong TH (2018) Perioperative outcomes of laparoscopic pancreaticoduodenectomy for benign and borderline malignant periampullary disease compared to open pancreaticoduodenectomy. Langenbeck’s Arch Surg 403:591–597CrossRefGoogle Scholar
  18. 18.
    Daniel Dindo M, Nicolas Demartines MD, Pierre-Alain Clavien MD (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefGoogle Scholar
  19. 19.
    Bassi C, Marchegiani G, Dervenis C, Sarr M, Abu Hilal M, Adham M, Allen P, Andersson R, Asbun HJ, Besselink MG, Conlon K, Del Chiaro M, Falconi M, Fernandez-Cruz L, Fernandez-Del Castillo C, Fingerhut A, Friess H, Gouma DJ, Hackert T, Izbicki J, Lillemoe KD, Neoptolemos JP, Olah A, Schulick R, Shrikhande SV, Takada T, Takaori K, Traverso W, Vollmer CR, Wolfgang CL, Yeo CJ, Salvia R, Buchler M (2017) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 years after. Surgery 161:584–591CrossRefGoogle Scholar
  20. 20.
    Mehrabi A, Fischer L, Hafezi M, Dirlewanger A, Grenacher L, Diener MK, Fonouni H, Golriz M, Garoussi C, Fard N, Rahbari NN, Werner J, Buchler MW (2014) A systematic review of localization, surgical treatment options, and outcome of insulinoma. Pancreas 43:675–686CrossRefGoogle Scholar
  21. 21.
    Pang L, Kong J, Wang Y, Zhang Y (2018) Laparoscopic versus open pylorus-preserving pancreatoduodenectomy. The first meta-analyse of retrospective matched cases. Acta Cir Bras 33:40–48CrossRefGoogle Scholar
  22. 22.
    Asbun HJ, Stauffer JA (2012) Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System. J Am Coll Surg 215:810–819CrossRefGoogle Scholar
  23. 23.
    Tol JA, Gouma DJ, Bassi C, Dervenis C, Montorsi M, Adham M, Andren-Sandberg A, Asbun HJ, Bockhorn M, Buchler MW, Conlon KC, Fernandez-Cruz L, Fingerhut A, Friess H, Hartwig W, Izbicki JR, Lillemoe KD, Milicevic MN, Neoptolemos JP, Shrikhande SV, Vollmer CM, Yeo CJ, Charnley RM (2014) Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS). Surgery 156:591–600CrossRefGoogle Scholar
  24. 24.
    Tomassetti P, Campana D, Piscitelli L, Casadei R, Santini D, Nori F, Morselli-Labate AM, Pezzilli R, Corinaldesi R (2005) Endocrine pancreatic tumors: factors correlated with survival. Ann Oncol 16:1806–1810CrossRefGoogle Scholar
  25. 25.
    Bettini R, Boninsegna L, Mantovani W, Capelli P, Bassi C, Pederzoli P, Delle Fave GF, Panzuto F, Scarpa A, Falconi M (2008) Prognostic factors at diagnosis and value of WHO classification in a mono-institutional series of 180 non-functioning pancreatic endocrine tumours. Ann Oncol 19:903–908CrossRefGoogle Scholar
  26. 26.
    Bilimoria KY, Talamonti MS, Tomlinson JS, Stewart AK, Winchester DP, Ko CY, Bentrem DJ (2008) Prognostic score predicting survival after resection of pancreatic neuroendocrine tumors: analysis of 3851 patients. Ann Surg 247:490–500CrossRefGoogle Scholar
  27. 27.
    Justin R, Parekh SCW, Bergsland Emily K, Nakakura Eric K (2012) Lymph node sampling rates and predictors of nodal metastasis in pancreatic neuroendocrine tumor resections: the UCSF experience with 149 patients. Pancreas 41:840–844CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Surgery, College of MedicineHallym UniversityChuncheonSouth Korea
  2. 2.Division of Hepatobiliary and Pancreatic Surgery, Department of SurgeryUniversity of Ulsan College of Medicine and Asan Medical CenterSongpa-guSouth Korea
  3. 3.Department of Surgery, College of MedicineImam Abdulrahman Bin Faisal UniversityDammamSaudi Arabia

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