Surgical Endoscopy

, Volume 32, Issue 3, pp 1234–1247 | Cite as

Robotic versus open pancreatoduodenectomy: a propensity score-matched analysis based on factors predictive of postoperative pancreatic fistula

  • Niccolò Napoli
  • Emanuele F. Kauffmann
  • Francesca Menonna
  • Francesca Costa
  • Sara Iacopi
  • Gabriella Amorese
  • Serena Giorgi
  • Angelo Baggiani
  • Ugo BoggiEmail author



Improvement in morbidity of pancreatoduodenectomy (PD) largely depends on the reduction in the incidence of clinically relevant (CR) postoperative pancreatic fistula (POPF).


After internal validation of the clinical risk score (CRS) of POPF, and identification of other predictive factors for POPF, robotic (RPD), and open (OPD) PDs were stratified into risk categories and matched by propensity scores. The primary endpoint of this study was incidence of CR-POPF. Secondary endpoints were 90-day morbidity and mortality, and sample size calculation for randomized controlled trials (RCT).


No patient undergoing RPD was classified at negligible risk for POPF, and no CR-POPF occurred in 7 RPD at low risk. The matching process identified 48 and 11 pairs at intermediate and high risk for POPF, respectively. In the intermediate-risk group, RPD was associated with higher rates of CR-POPF (31.3% vs 12.5%) (p = 0.0026), with equivalent incidence of grade C POPF. In the high-risk group, CR-POPF occurred frequently, but in similar percentages, after either procedures. Starting from an unadjusted point estimate of the effect size of 1.71 (0.91–3.21), the pair-matched odds ratio for CR-POPF after RPD was 2.80 (1.01–7.78) for the intermediate-risk group, and 0.20 (0.01–4.17) for the high-risk group. Overall morbidity and mortality were equivalent in matched study groups. Sample size calculation for a non-inferiority RCT demonstrated that a total of 31,669 PDs would be required to randomize 682 patients at intermediate risk and 1852 patients at high risk.


In patients at intermediate risk, RPD is associated with higher rates of CR-POPF. Incidence of grade C POPF is similar in RPD and OPD, making overall morbidity and mortality also equivalent. A RCT, with risk stratification for POPF, would require an enormous number of patients. Implementation of an international registry could be the next step in the assessment of RPD.


Pancreatoduodenectomy Open pancreatoduodenectomy Robotic pancreatoduodenectomy Postoperative pancreatic fistula Propensity score 


Compliance with ethical standards


Niccolò Napoli, Emanuele Federico Kauffmann, Francesca Menonna, Francesca Costa, Sara Iacopi, Gabriella Amorese, Serena Giorgi, Angelo Baggiani, and Ugo Boggi have no conflicts of interest or financial ties to disclose.


  1. 1.
    Kelley WE (2008) The evolution of laparoscopy and the revolution in surgery in the decade of the 1990s. JSLS 12:351–357PubMedPubMedCentralGoogle Scholar
  2. 2.
    Allori AC, Leitman IM, Heitman E (2010) Delayed assessment and eager adoption of laparoscopic cholecystectomy: implications for developing surgical technologies. World J Gastroenterol 16:4115–4122CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Bonjer HJ, Deijen CL, Abis GA, Cuesta MA, van der Pas MH, de Lange-de Klerk ES, Lacy AM, Bemelman WA, Andersson J, Angenete E, Rosenberg J, Fuerst A, Haglind E, COLOR II Study Group (2015) A randomized trial of laparoscopic versus open surgery for rectal cancer. N Engl J Med 372:1324–1332CrossRefPubMedGoogle Scholar
  4. 4.
    Ni M, Mackenzie H, Widdison A, Jenkins JT, Mansfield S, Dixon T, Slade D, Coleman MG, Hanna GB (2016) What errors make a laparoscopic cancer surgery unsafe? An ad hoc analysis of competency assessment in the National Training Programme for laparoscopic colorectal surgery in England. Surg Endosc 30:1020–1027CrossRefPubMedGoogle Scholar
  5. 5.
    Nanidis TG, Antcliffe D, Kokkinos C, Borysiewicz CA, Darzi AW, Tekkis PP, Papalois VE (2008) Laparoscopic versus open live donor nephrectomy in renal transplantation: a meta-analysis. Ann Surg 247:58–70CrossRefPubMedGoogle Scholar
  6. 6.
    Shrikhande SV, Sivasanker M, Vollmer CM, Friess H, Besselink MG, Fingerhut A, Yeo CJ, Fernandez-delCastillo C, Dervenis C, Halloran C, Gouma DJ, Radenkovic D, Asbun HJ, Neoptolemos JP, Izbicki JR, Lillemoe KD, Conlon KC, Fernandez-Cruz L, Montorsi M, Bockhorn M, Adham M, Charnley R, Carter R, Hackert T, Hartwig W, Miao Y, Sarr M, Bassi C, Büchler MW, International Study Group of Pancreatic Surgery (ISGPS) (2017) Pancreatic anastomosis after pancreatoduodenectomy: a position statement by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 161:584–591CrossRefPubMedGoogle Scholar
  7. 7.
    Vollmer CM Jr, Sanchez N, Gondek S, McAuliffe J, Kent TS, Christein JD et al (2012) A root-cause analysis of mortality following major pancreatectomy. J Gastrointest Surg 16:89–102CrossRefPubMedGoogle Scholar
  8. 8.
    Gawlas I, Sethi M, Winner M, Epelboym I, Lee JL, Schrope BA, Chabot JA, Allendorf JD (2013) Readmission after pancreatic resection is not an appropriate measure of quality. Ann Surg Oncol 20:1781–1787CrossRefPubMedGoogle Scholar
  9. 9.
    Gagner M, Pomp A (1994) Laparoscopic pylorus-preserving pancreatoduodenectomy. Surg Endosc 8:408–410CrossRefPubMedGoogle Scholar
  10. 10.
    Gagner M, Palermo M (2009) Laparoscopic Whipple procedure: review of the literature. J Hepatobiliary Pancreat Surg 16:726–730CrossRefPubMedGoogle Scholar
  11. 11.
    Boggi U, Amorese G, Vistoli F, Caniglia F, De Lio N, Perrone V, Barbarello L, Belluomini M, Signori S, Mosca F (2015) Laparoscopic pancreaticoduodenectomy: a systematic literature review. Surg Endosc 29:9–23CrossRefPubMedGoogle Scholar
  12. 12.
    McMillan MT, Zureikat AH, Hogg ME, Kowalsky SJ, Zeh HJ, Vollmer Sprys MH, Jr CM (2017) A propensity score-matched analysis of robotic vs open pancreatoduodenectomy on incidence of pancreatic fistula. JAMA Surg 152:327–335CrossRefPubMedGoogle Scholar
  13. 13.
    Adam MA, Choudhury K, Dinan MA, Reed SD, Scheri RP, Blazer DG 3rd, Roman SA, Sosa JA (2015) Minimally invasive versus open pancreaticoduodenectomy for cancer: practice patterns and short-term outcomes among 7061 patients. Ann Surg 262:372–377CrossRefPubMedGoogle Scholar
  14. 14.
    Chen S, Chen JZ, Zhan Q, Deng XX, Shen BY, Peng CH, Li HW (2015) Robot-assisted laparoscopic versus open pancreaticoduodenectomy: a prospective, matched, mid-term follow-up study. Surg Endosc 29:3698–3711CrossRefPubMedGoogle Scholar
  15. 15.
    Wellner UF, Küsters S, Sick O, Busch C, Bausch D, Bronsert P, Hopt UT, Karcz KW, Keck T (2014) Hybrid laparoscopic versus open pylorus-preserving pancreatoduodenectomy: retrospective matched case comparison in 80 patients. Langenbecks Arch Surg 399:849–856CrossRefPubMedGoogle Scholar
  16. 16.
    Bao PQ, Mazirka PO, Watkins KT (2014) Retrospective comparison of robot-assisted minimally invasive versus open pancreaticoduodenectomy for periampullary neoplasms. J Gastrointest Surg 18:682–689CrossRefPubMedGoogle Scholar
  17. 17.
    Chalikonda S, Aguilar-Saavedra JR, Walsh RM (2012) Laparoscopic robotic-assisted pancreaticoduodenectomy: a case-matched comparison with open resection. Surg Endosc 26:2397–2402CrossRefPubMedGoogle Scholar
  18. 18.
    Callery MP, Pratt WB, Kent TS, Chaikof EL, Vollmer CM Jr (2013) A prospectively validated clinical risk score accurately predicts pancreatic fistula after pancreatoduodenectomy. J Am Coll Surg 216:1–14CrossRefPubMedGoogle Scholar
  19. 19.
    Miller BC, Christein JD, Behrman SW, Drebin JA, Pratt WB, Callery MP, Vollmer CM Jr (2014) A multi-institutional external validation of the fistula risk score for pancreatoduodenectomy. J Gastrointest Surg 18:172–179CrossRefPubMedGoogle Scholar
  20. 20.
    Shubert CR, Wagie AE, Farnell MB, Nagorney DM, Que FG, Lombardo KMR, Truty MJ, Smoot RL, Kendrick ML (2015) Clinical risk score to predict pancreatic fistula after pancreatoduodenectomy: independent external validation for open and laparoscopic approaches. J Am Coll Surg 221:689–698CrossRefPubMedGoogle Scholar
  21. 21.
    Polanco PM, Zenati MS, Hogg ME, Shakir M, Boone BA, Barlett DL, Zeh HJ, Zureikat AH (2016) An analysis of risk factors for pancreatic fistula after robotic pancreaticoduodenectomy: outcomes from a consecutive series of standardized pancreatic reconstructions. Surg Endosc 30:1523–1529CrossRefPubMedGoogle Scholar
  22. 22.
    Boggi U, Signori S, De Lio N, Perrone VG, Vistoli F, Belluomini M, Cappelli C, Amorese G, Mosca F (2013) Feasibility of robotic pancreaticoduodenectomy. Br J Surg 100:917–925CrossRefPubMedGoogle Scholar
  23. 23.
    Mucksavage P, Kerbl DC, Lee JY (2011) The da Vinci® Surgical System overcomes innate hand dominance. J Endourol 25:1385–1388CrossRefPubMedGoogle Scholar
  24. 24.
    Mise Y, Vauthey JN, Zimmitti G, Parker NH, Conrad C, Aloia TA, Lee JE, Fleming JB, Katz MH (2015) Ninety-day postoperative mortality is a legitimate measure of hepatopancreatobiliary surgical quality. Ann Surg 262:1071–1078CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Swanson RS, Pezzi CM, Mallin K, Loomis AM, Winchester DP (2014) The 90-day mortality after pancreatectomy for cancer is double the 30-day mortality: more than 20,000 resections from the national cancer data base. Ann Surg Oncol 21:4059–4067CrossRefPubMedGoogle Scholar
  26. 26.
    Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, for the International Study Group on Pancreatic Fistula (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13CrossRefPubMedGoogle Scholar
  27. 27.
    Pancreas Club Calculator ISGPS leak definition. Available at:
  28. 28.
    Wente MN, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Traverso LW, Yeo CJ, Büchler MW (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142:761–768CrossRefPubMedGoogle Scholar
  29. 29.
    Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Yeo CJ, Büchler MW (2007) Postpancreatectomy hemorrhage (PPH)—an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142:20–25CrossRefPubMedGoogle Scholar
  30. 30.
    Gross JB (1983) Estimating allowable blood loss: corrected for dilution. Anesthesiology 58:277–280CrossRefPubMedGoogle Scholar
  31. 31.
    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
  32. 32.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Petermann D, Demartines N, Schäfer M (2013) Severe postoperative complications adversely affect long-term survival after R1 resection for pancreatic head adenocarcinoma. World J Surg 37:1901–1908CrossRefPubMedGoogle Scholar
  34. 34.
    Slankamenac K, Graf R, Barkun J, Puhan MA, Clavien PA (2013) The comprehensive complication index: a novel continuous scale to measure surgical morbidity. Ann Surg 258:1–7CrossRefPubMedGoogle Scholar
  35. 35.
    Napoli N, Kauffmann EF, Menonna F, Perrone VG, Brozzetti S, Boggi U (2016) Indications technique and results of robotic pancreatoduodenectomy. Updates Surg 68:295–305CrossRefPubMedGoogle Scholar
  36. 36.
    Kauffmann EF, Napoli N, Menonna F, Vistoli F, Amorese G, LE Campani Pollina, Funel N, Cappelli C, Caramella D, Boggi U (2016) Robotic pancreatoduodenectomy with vascular resection. Langenbecks Arch Surg 401:1111–1122CrossRefPubMedGoogle Scholar
  37. 37.
    Boggi U, Napoli N, Costa F, Kauffmann EF, Menonna F, Iacopi S, Vistoli F, Amorese G (2016) Robotic pancreatic resections. World J Surg 40:2497–2506CrossRefPubMedGoogle Scholar
  38. 38.
    Napoli N, Kauffmann EF, Palmeri M, Miccoli M, Costa F, Vistoli F, Amorese G, Boggi U (2016) The learning curve in robotic pancreatoduodenectomy. Dig Surg 33:299–307CrossRefPubMedGoogle Scholar
  39. 39.
    Kang CM, Kim DH, Lee WJ (2010) Ten years of experience with resection of left-sided pancreatic ductal adenocarcinoma: evolution and initial experience to a laparoscopic approach. Surg Endosc 24:1533–1541CrossRefPubMedGoogle Scholar
  40. 40.
    Pratt WB, Maithel SK, Vanounou T, Huang ZS, Callery MP, Vollmer CM Jr (2007) Clinical and economic validation of the International Study Group of Pancreatic Fistula (ISGPF) classification scheme. Ann Surg 245:443–451CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    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 638–40) CrossRefPubMedGoogle Scholar
  42. 42.
    Zureikat AH, Moser AJ, Boone BA, Bartlett DL, Zenati M, Zeh HJ 3rd (2013) 250 robotic pancreatic resections: safety and feasibility. Ann Surg 258:554–559 (discussion 559–62) PubMedPubMedCentralGoogle Scholar
  43. 43.
    Strobel O, Büchler MW (2015) Increased mortality due to lack of experience with minimally invasive pancreatoduodenectomy. Chirurg 86:496CrossRefPubMedGoogle Scholar
  44. 44.
    de la Fuente SG (2013) Laparoscopic pancreaticoduodenectomies: a word of caution. J Am Coll Surg 216:1218CrossRefPubMedGoogle Scholar
  45. 45.
    Zureikat AH, Nguyen KT, Bartlett DL, Zeh HJ, Moser AJ (2011) Robotic-assisted major pancreatic resection and reconstruction. Arch Surg 146:256–261CrossRefPubMedGoogle Scholar
  46. 46.
    McMillan MT, Soi S, Asbun HJ, Ball CG, Bassi C, Beane JD, Behrman SW, Berger AC, Bloomston M, Callery MP, Christein JD, Dixon E, Drebin JA, Fernandez-del Castillo C, Fisher WE, Ven Fong Z, House MG, Hughes SJ, Kent TS, Kunstman JW, Malleo G, Miller BC, Salem RR, Soares K, Valero V, Wolfgang CL, Vollmer CM (2016) Risk-adjusted outcomes of clinically relevant pancreatic fistula following pancreatoduodenectomy: a model for performance evaluation. Ann Surg 264:344–352CrossRefPubMedGoogle Scholar
  47. 47.
    Dokmak S, Ftériche FS, Aussilhou B, Bensafta Y, Lévy P, Ruszniewski P (2015) Laparoscopic pancreaticoduodenectomy should not be routine for resection of periampullary tumors. J Am Coll Surg 220:831–838CrossRefPubMedGoogle Scholar
  48. 48.
    Fujii T, Sugimoto H, Yamada S, Kanda M, Suenaga M, Takami H, Hattori M, Inokawa Y, Nomoto S, Fujiwara M, Kodera Y (2014) Modified Blumgart anastomosis for pancreaticojejunostomy: technical improvement in matched historical control study. J Gastrointest Surg 18:1108–1115CrossRefPubMedGoogle Scholar
  49. 49.
    Poves I, Morató O, Burdío F, Grande L (2017) Laparoscopic-adapted Blumgart pancreaticojejunostomy in laparoscopic pancreaticoduodenectomy. Surg Endosc 31:2837–2845CrossRefPubMedGoogle Scholar
  50. 50.
    Halloran CM, Platt K, Gerard A, Polydoros F, O’Reilly DA, Gomez D, Smith A, Neoptolemos JP, Soonwalla Z, Taylor M, Blazeby JM, Ghaneh P (2016) PANasta Trial; Cattell Warren versus Blumgart techniques of panreatico-jejunostomy following pancreato-duodenectomy: study protocol for a randomized controlled trial. Trials 17:30CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Division of General and Transplant SurgeryUniversity of PisaPisaItaly
  2. 2.Division of Anesthesia and Intensive CareUniversity of PisaPisaItaly
  3. 3.Division of Hygiene and EpidemiologyUniversity of PisaPisaItaly
  4. 4.Azienda Ospedaliera Universitaria PisanaUniversità di PisaPisaItaly

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