Surgical Endoscopy

, Volume 32, Issue 5, pp 2387–2396 | Cite as

Minimally invasive surgical approaches offer earlier time to adjuvant chemotherapy but not improved survival in resected pancreatic cancer

  • Katelin A. Mirkin
  • Erin K. Greenleaf
  • Christopher S. Hollenbeak
  • Joyce Wong



Pancreatic surgery encompasses complex operations with significant potential morbidity. Greater experience in minimally invasive surgery (MIS) has allowed resections to be performed laparoscopically and robotically. This study evaluates the impact of surgical approach in resected pancreatic cancer.


The National Cancer Data Base (2010–2012) was reviewed for patients with stages 1–3 resected pancreatic carcinoma. Open approaches were compared to MIS. A sub-analysis was then performed comparing robotic and laparoscopic approaches.


Of the 9047 patients evaluated, surgical approach was open in 7511 (83%), laparoscopic in 992 (11%), and robotic in 131 (1%). The laparoscopic and robotic conversion rate to open was 28% (n = 387) and 17% (n = 26), respectively. Compared to open, MIS was associated with more distal resections (13.5, 24.3%, respectively, p < 0.0001), shorter hospital length of stay (LOS) (11.3, 9.5 days, respectively, p < 0.0001), more margin-negative resections (75, 79%, p = 0.038), and quicker time to initiation of chemotherapy (TTC) (59.1, 56.3 days, respectively, p = 0.0316). There was no difference in number of lymph nodes obtained based on surgical approach (p = 0.5385). When stratified by type of resection (head, distal, or total), MIS offered significantly shorter LOS in all types. Multivariate analysis demonstrated no survival benefit for any MIS approach relative to open (all, p > 0.05). When adjusted for patient, disease, and treatment characteristics, TTC was not an independent prognostic factor (HR 1.09, p = 0.084).


MIS appears to offer comparable surgical oncologic benefit with improved LOS and shorter TTC. This effect, however, was not associated with improved survival.


Pancreatic cancer Minimally invasive surgery MIS Time to adjuvant therapy NCDB 



There are no funding sources to disclose in relation to this project.

Compliance with ethical standards


The National Cancer Data Base (NCDB) is a joint project of the Commission on Cancer (CoC) of the American College of Surgeons and the American Cancer Society. The CoC’s NCDB and the hospitals participating in the CoC NCDB are the source of the de-identified data used herein; they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the authors.


Dr. Mirkin, Dr. Greenleaf, Dr. Hollenbeak, and Dr. Wong have no conflicts of interest or financial ties to disclose.


  1. 1.
    Are C, Dhir M, Ravipati L (2011) History of pancreaticoduodenectomy: early misconceptions, initial milestones and the pioneers. HPB 13:377–384CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Trendelenburg WO (1886) Beitrage zur Chirurgie der Bauchorgane. Deutsche Zeitschrift Fur CHirurgie 24:326–354CrossRefGoogle Scholar
  3. 3.
    Griffin JF, Poruk KE, Wolfgang CL (2015) Pancreatic cancer surgery: past, present, and future. Chin J Cancer Res 27:332–348PubMedPubMedCentralGoogle Scholar
  4. 4.
    Schnelldorfer T, Sarr MG (2009) Alessandro Codivilla and the first pancreatoduodenectomy. Arch Surg 144:1179–1184CrossRefPubMedGoogle Scholar
  5. 5.
    Halsted W (1889) Contributions to the surgery of the bile passages, especially of the common bile-duct. Boston Med Surg J 141:645–654CrossRefGoogle Scholar
  6. 6.
    Kausch W (1912) Das Carcinom der Papilla duodeni und seine radikale Entfernung. Beitr Klin Chir 78:438–486Google Scholar
  7. 7.
    Whipple AO, Parsons WB, Mullins CR (1935) Treatment of carcinoma of the ampulla of vater. Ann Surg 102:763–779CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Crile G Jr (1970) The advantages of bypass operations over radical pancreatoduodenectomy in the treatment of pancreatic carcinoma. Surg Gynecol Obstet 130:1049–1053PubMedGoogle Scholar
  9. 9.
    Hansen P, Bax T, Swanstrom L (1997) Laparoscopic adrenalectomy: history, indications, and current techniques for a minimally invasive approach to adrenal pathology. Endoscopy 29:309–314CrossRefPubMedGoogle Scholar
  10. 10.
    Bonjer HJ, Hop WC, Nelson H, Sargent DJ, Lacy AM, Castells A, Guillou PJ, Thorpe H, Brown J, Delgado S, Kuhrij E, Haglind E, Påhlman L, Transatlantic Laparoscopically Assisted vs Open Colectomy Trials Study Group (2007) Laparoscopically assisted vs open colectomy for colon cancer: a meta-analysis. Arch Surg 142:298–303CrossRefPubMedGoogle Scholar
  11. 11.
    Lee MS, Lee JH, Park DJ, Lee HJ, Kim HH, Yang HK (2013) Comparison of short- and long-term outcomes of laparoscopic-assisted total gastrectomy and open total gastrectomy in gastric cancer patients. Surg Endosc 27:2598–2605CrossRefPubMedGoogle Scholar
  12. 12.
    Khan O, Nizar S, Vasilikostas G, Wan A (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. J Thorac Dis 4:465–466PubMedPubMedCentralGoogle Scholar
  13. 13.
    Nix J, Smith A, Kurpad R, Nielsen ME, Wallen EM, Pruthi RS (2010) Prospective randomized controlled trial of robotic versus open radical cystectomy for bladder cancer: perioperative and pathologic results. Eur Urol 57:196–201CrossRefPubMedGoogle Scholar
  14. 14.
    Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, Barakat R, Pearl ML, Sharma SK (2012) Recurrence and survival after random assignment to laparoscopy versus laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group LAP2 Study. J Clin Oncol 30:695–700CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Soper NJ, Brunt LM, Dunnegan DL, Meininger TA (1994) Laparoscopic distal pancreatectomy in the porcine model. Surg Endosc 8:57–60 (discussion 60–51).CrossRefPubMedGoogle Scholar
  16. 16.
    Gagner M, Pomp A, Herrera MF (1996) Early experience with laparoscopic resections of islet cell tumors. Surgery 120:1051–1054CrossRefPubMedGoogle Scholar
  17. 17.
    Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410CrossRefPubMedGoogle Scholar
  18. 18.
    Melvin WS, Needleman BJ, Krause KR, Ellison EC (2003) Robotic resection of pancreatic neuroendocrine tumor. J Laparoendosc Adv Surg Tech A 13:33–36CrossRefPubMedGoogle Scholar
  19. 19.
    Palanivelu C, Rajan PS, Rangarajan M, Vaithiswaran V, Senthilnathan P, Parthasarathi R, Praveen Raj P (2009) Evolution in techniques of laparoscopic pancreaticoduodenectomy: a decade long experience from a tertiary center. J Hepatobiliary Pancreat Surg 16:731–740CrossRefPubMedGoogle Scholar
  20. 20.
    Kendrick ML, Cusati D (2010) Total laparoscopic pancreaticoduodenectomy: feasibility and outcome in an early experience. Arch Surg 145:19–23CrossRefPubMedGoogle Scholar
  21. 21.
    MacKenzie S, Kosari K, Sielaff T, Johnson E (2011) The robotic Whipple: operative strategy and technical considerations. J Robot Surg 5:3–9CrossRefPubMedGoogle Scholar
  22. 22.
    Baker EH, Ross SW, Seshadri R, Swan RZ, Iannitti DA, Vrochides D, Martinie JB (2016) Robotic pancreaticoduodenectomy: comparison of complications and cost to the open approach. Int J Med Robot 12:554–560CrossRefPubMedGoogle Scholar
  23. 23.
    Murakami Y, Uemura K, Sudo T, Hashimoto Y, Kondo N, Nakagawa N, Sasaki H, Sueda T (2013) Early initiation of adjuvant chemotherapy improves survival of patients with pancreatic carcinoma after surgical resection. Cancer Chemother Pharmacol 71:419–429CrossRefPubMedGoogle Scholar
  24. 24.
    Neoptolemos JP, Stocken DD, Friess H, Bassi C, Dunn JA, Hickey H, Beger H, Fernandez-Cruz L, Dervenis C, Lacaine F, Falconi M, Pederzoli P, Pap A, Spooner D, Kerr DJ, Büchler MW; European Study Group for Pancreatic Cancer (2004) A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med 350:1200–1210Google Scholar
  25. 25.
    Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams RA, Sauter PK, Coleman J, Hruban RH, Lillemoe KD (2000) Resected adenocarcinoma of the pancreas-616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 4:567–579CrossRefPubMedGoogle Scholar
  26. 26.
    Jiang L, Yang KH, Guan QL, Cao N, Chen Y, Zhao P, Chen YL, Yao L (2013) Laparoscopy-assisted gastrectomy versus open gastrectomy for resectable gastric cancer: an update meta-analysis based on randomized controlled trials. Surg Endosc 27:2466–2480CrossRefPubMedGoogle Scholar
  27. 27.
    Merchant NB, Parikh AA, Kooby DA (2009) Should all distal pancreatectomies be performed laparoscopically? Adv Surg 43:283–300CrossRefPubMedGoogle Scholar
  28. 28.
    Stewart CL, Meguid C, Chapman B, Schulick R, Edil BH (2016) Evolving trends towards minimally invasive surgery for solid-pseudopapillary neoplasms. Ann Surg Oncol 23:4165–4168CrossRefPubMedGoogle Scholar
  29. 29.
    Hardacre JM (2010) Is there a learning curve for pancreaticoduodenectomy after fellowship training?. HPB Surg. doi: 10.1155/2010/230287 PubMedGoogle Scholar
  30. 30.
    Speicher PJ, Nussbaum DP, White RR, Zani S, Mosca PJ, Blazer DG 3rd, Clary BM, Pappas TN, Tyler DS, Perez A (2014) Defining the learning curve for team-based laparoscopic pancreaticoduodenectomy. Ann Surg Oncol 21(12):4014–4019CrossRefPubMedGoogle Scholar
  31. 31.
    Tran TB, Dua MM, Worhunsky DJ, Poultsides GA, Norton JA, Visser BC (2016) The first decade of laparoscopic pancreaticoduodenectomy in the United States: costs and outcomes using the nationwide inpatient sample. Surg Endosc 30:1778–1783CrossRefPubMedGoogle Scholar
  32. 32.
    Zhang YH, Zhang CW, Hu ZM, Hong DF (2016) Pancreatic cancer: open or minimally invasive surgery? World J Gastroenterol 22:7301–7310CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Sharpe SM, Talamonti MS, Wang CE, Prinz RA, Roggin KK, Bentrem DJ, Winchester DJ, Marsh RD, Stocker SJ, Baker MS (2015) 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 221:175–184CrossRefPubMedGoogle Scholar
  34. 34.
    Riviere D, Gurusamy KS, Kooby DA, Vollmer CM, Besselink MG, Davidson BR, van Laarhoven CJ (2016) Laparoscopic versus open distal pancreatectomy for pancreatic cancer. Cochrane Database Syst Rev 4:Cd011391PubMedGoogle Scholar
  35. 35.
    Gavriilidis P, Lim C, Menahem B, Lahat E, Salloum C, Azoulay D (2016) Robotic versus laparoscopic distal pancreatectomy: the first meta-analysis. HPB 18:567–574CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Baker EH, Ross SW, Seshadri R et al (2016) Robotic pancreaticoduodenectomy: comparison of complications and cost to the open approach. Int J Med Robot Comput Assist Surg 12(3):554–560CrossRefGoogle Scholar
  37. 37.
    Waters JA, Canal DF, Wiebke EA et al (2010) Robotic distal pancreatectomy: cost effective? Surgery 148(4):814–823CrossRefPubMedGoogle Scholar
  38. 38.
    Boone BA, Zenati M, Hogg ME et al (2015) Assessment of quality outcomes for robotic pancreaticoduodenectomy: identification of the learning curve. JAMA Surg 150(5):416–422CrossRefPubMedGoogle Scholar
  39. 39.
    Mirkin KA, Greenleaf EK, Hollenbeak CS, Wong J (2016) Time to the initiation of adjuvant chemotherapy does not impact survival in patients with resected pancreatic cancer. Cancer 122:2979–2987CrossRefPubMedGoogle Scholar
  40. 40.
    Daouadi M, Zureikat AH, Zenati MS, Choudry H, Tsung A, Bartlett DL, Hughes SJ, Lee KK, Moser AJ, Zeh HJ (2013) Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg 257:128–132CrossRefPubMedGoogle Scholar
  41. 41.
    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 262:146–155CrossRefPubMedGoogle Scholar
  42. 42.
    Croome KP, Farnell MB, Que FG, Reid-Lombardo KM, Truty MJ, Nagorney DM, Kendrick ML (2014) Total laparoscopic pancreaticoduodenectomy for pancreatic ductal adenocarcinoma: oncologic advantages over open approaches? Ann Surg 260:633–638 (discussion 638–640)CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Katelin A. Mirkin
    • 1
  • Erin K. Greenleaf
    • 1
  • Christopher S. Hollenbeak
    • 1
    • 2
  • Joyce Wong
    • 1
  1. 1.Division of Surgical Oncology, Department of Surgery, College of MedicineThe Pennsylvania State UniversityHersheyUSA
  2. 2.Department of Public Health Sciences, College of MedicineThe Pennsylvania State UniversityHersheyUSA

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