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A propensity score-matched analysis of robotic versus open pancreatoduodenectomy for pancreatic cancer based on margin status

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Abstract

Background

No study has shown the oncologic non-inferiority of robotic pancreatoduodenectomy (RPD) versus open pancreatoduodenectomy (OPD) for pancreatic cancer (PC).

Methods

This is a single institution propensity score matched study comparing RPD and ODP for resectable PC, based on factors predictive of R1 resection (≤ 1 mm). Only patients operated on after completion of the learning curve in both procedures and for whom circumferential margins were assessed according to the Leeds pathology protocol were included. The primary study endpoint was the rate of R1 resection. Secondary study endpoints were as follows: number of examined lymph nodes (N), rate of perioperative transfusions, percentage of patients receiving adjuvant therapies, occurrence of local recurrence, overall survival, disease-free survival, and sample size calculation for randomized controlled trials (RCT).

Results

Factors associated with R1 resection were tumor diameter, number of positive N, N ratio, logarithm odds of positive N, and duodenal infiltration. The matching process identified 20 RPDs and 24 OPDs. All RPDs were completed robotically. R1 resection was identified in 11 RPDs (55.0%) and in 10 OPDs (41.7%) (p = 0.38). There was no difference in the rate of R1 at each margin as well as in the proportion of patients with multiple R1 margins. RPD and OPD were also equivalent with respect to all secondary study endpoints, with a trend towards lower rate of blood transfusions in RPD. Based on the figures presented herein, a non-inferiority RCT comparing RPD and OPD having the rate of R1 resection as the primary study endpoint requires 3355 pairs.

Conclusions

RPD and OPD achieved the same rate of R1 resections in resectable PC. RPD was also non-inferior to OPD with respect to all secondary study endpoints. Because of the high number of patients required to run a RCT, further assessment of RPD for PC would require the implementation of an international registry.

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References

  1. Montagnini AL, Røsok BI, Asbun HJ, Barkun J, Besselink MG, Boggi U, Conlon KC, Fingerhut A, Han HS, Hansen PD, Hogg ME, Kendrick ML, Palanivelu C, Shrikhande SV, Wakabayashi G, Zeh H, Vollmer CM, Kooby DA (2017) Standardizing terminology for minimally invasive pancreatic resection. HPB 9:182–189

    Article  Google Scholar 

  2. 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 100:917–925

    Article  CAS  Google Scholar 

  3. Zureikat AH, Moser AJ, Boone BA, Bartlett DL, Zenati M, Zeh HJ (2013) 250 robotic pancreatic resections: safety and feasibility. Ann Surg 258:554–559

    Article  Google Scholar 

  4. Napoli N, Kauffmann EF, Palmeri M, Miccoli M, Costa F, Vistoli F, Amorese G, Boggi U (2016) The learning curve in robotic pancreaticoduodenectomy. Dig Surg 33:299–307

    Article  CAS  Google Scholar 

  5. Napoli N, Kauffmann EF, Menonna F, Perrone VG, Brozzetti S, Boggi U (2016) Indications, technique, and results of robotic pancreatoduodenectomy. Updates Surg 68:295–305

    Article  Google Scholar 

  6. Boggi U, Napoli N, Costa F, Kauffmann EF, Menonna F, Iacopi S, Vistoli F, Amorese G (2016) Robotic-assisted pancreatic resections. World J Surg 40:2497–2506

    Article  Google Scholar 

  7. Napoli N, Kauffmann EF, Menonna F, Costa F, Iacopi S, Amorese G, Giorgi S, Baggiani A, Boggi U (2018) Robotic versus open pancreatoduodenectomy: a propensity score matched analysis based on factors predictive of postoperative pancreatic fistula. Surg Endosc 32:1234–1247

    Article  Google Scholar 

  8. Sabater L, García-Granero A, Escrig-Sos J, Gómez-Mateo Mdel C, Sastre J, Ferrández A, Ortega J (2014) Outcome quality standards in pancreatic oncologic surgery. Ann Surg Oncol 21:1138–1146

    Article  Google Scholar 

  9. Merkow RP, Bilimoria KY, Bentrem DJ, Pitt HA, Winchester DP, Posner MC, Ko CY, Pawlik TM (2014) National assessment of margin status as a quality indicator after pancreatic cancer surgery. Ann Surg Oncol 21:1067–1074

    Article  Google Scholar 

  10. Tomlinson JS, Jain S, Bentrem DJ, Sekeris EG, Maggard MA, Hines OJ, Reber HA, Ko CY (2007) Accuracy of staging node-negative pancreas cancer: a potential quality measure. Arch Surg 142:767–774

    Article  Google Scholar 

  11. Ball CG, Pitt HA, Kilbane ME, Dixon E, Sutherland FR, Lillemoe KD (2010) Peri-operative blood transfusion and operative time are quality indicators for pancreatoduodenectomy. HPB 12:465–471

    Article  Google Scholar 

  12. Wu W, He J, Cameron JL, Makary M, Soares K, Ahuja N, Rezaee N, Herman J, Zheng L, Laheru D, Choti MA, Hruban RH, Pawlik TM, Wolfgang CL, Weiss MJ (2014) The impact of postoperative complications on the administration of adjuvant therapy following pancreaticoduodenectomy for adenocarcinoma. Ann Surg Oncol 21:2873–2881

    Article  Google Scholar 

  13. Nussbaum DP, Adam MA, Youngwirth LM, Ganapathi AM, Roman SA, Tyler DS, Sosa JA, Blazer DG (2016) Minimally invasive pancreaticoduodenectomy does not improve use or time to initiation of adjuvant chemotherapy for patients with pancreatic adenocarcinoma. Ann Surg Oncol 23:1026–1033

    Article  Google Scholar 

  14. Esposito I, Kleeff J, Bergmann F, Reiser C, Herpel E, Friess H, Schirmacher P, Büchler MW (2008) Most pancreatic cancer resections are R1 resections. Ann Surg Oncol 15:1651–1660

    Article  Google Scholar 

  15. Sugiura T, Uesaka K, Mihara K, Sasaki K, Kanemoto H, Mizuno T, Okamura Y (2013) Margin status, recurrence pattern, and prognosis after resection of pancreatic cancer. Surgery 154:1078–1086

    Article  Google Scholar 

  16. Verbeke CS, Leitch D, Menon KV, McMahon MJ, Guillou PJ, Anthoney A (2006) Redefining the R1 resection in pancreatic cancer. Br J Surg 93:1232–1237

    Article  CAS  Google Scholar 

  17. Von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, STROBE Initiative (2007) The Strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370(9596):1453–1457

    Article  Google Scholar 

  18. Fisher WE, Hodges SE, Wu MF, Hilsenbeck SG, Brunicardi FC (2012) Assessment of the learning curve for pancreaticoduodenectomy. Am J Surg 203:684–690

    Article  Google Scholar 

  19. Tempero MA, Malafa MP, Al-Hawary M, Asbun H, Bain A, Behrman SW, Benson AB 3rd, Binder E, Cardin DB, Cha C, Chiorean EG, Chung V, Czito B, Dillhoff M, Dotan E, Ferrone CR, Hardacre J, Hawkins WG, Herman J, Ko AH, Komanduri S, Koong A, LoConte N, Lowy AM, Moravek C, Nakakura EK, O’Reilly EM, Obando J, Reddy S, Scaife C, Thayer S, Weekes CD, Wolff RA, Wolpin BM, Burns J, Darlow S (2017) Pancreatic adenocarcinoma, version 2.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 15:1028–1061

    Article  Google Scholar 

  20. Kauffmann EF, Napoli N, Menonna F, Vistoli F, Amorese G, Campani D, Pollina LE, Funel N, Cappelli C, Caramella D, Boggi U (2016) Robotic pancreatoduodenectomy with vascular resection. Langenbecks Arch Surg 401:1111–1122

    Article  Google Scholar 

  21. Boggi U, Del Chiaro M, Croce C, Vistoli F, Signori S, Moretto C, Amorese G, Mazzeo S, Cappelli C, Campani D, Mosca F (2009) Prognostic implications of tumor invasion or adhesion to peripancreatic vessels in resected pancreatic cancer. Surgery 146:869–881

    Article  Google Scholar 

  22. Strobel O, Hank T, Hinz U, Bergmann F, Schneider L, Springfeld C, Jäger D, Schirmacher P, Hackert T, Büchler MW (2017) Pancreatic cancer surgery: the new R-status counts. Ann Surg 265:565–573

    Article  Google Scholar 

  23. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, International Study Group on Pancreatic Fistula Definition (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13

    Article  Google Scholar 

  24. 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 142:761–768

    Article  Google Scholar 

  25. 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 142:20–25

    Article  Google Scholar 

  26. 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 240:205–213

    Article  Google Scholar 

  27. 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 37:1901–1908

    Article  Google Scholar 

  28. 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 258:1–7

    Article  Google Scholar 

  29. Lonjon G, Porcher R, Ergina P, Fouet M, Boutron I (2017) Potential pitfalls of reporting and bias in observational studies with propensity score analysis assessing a surgical procedure: a methodological systematic review. Ann Surg 265:901–909

    Article  Google Scholar 

  30. Cirocchi R, Partelli S, Trastulli S, Coratti A, Parisi A, Falconi M (2013) A systematic review on robotic pancreaticoduodenectomy. Surg Oncol 22:238–246

    Article  Google Scholar 

  31. 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 29:9–23

    Article  Google Scholar 

  32. 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 216:1–14

    Article  Google Scholar 

  33. Butler JR, Ahmad SA, Katz MH, Cioffi JL, Zyromski NJ (2016) A systematic review of the role of periadventitial dissection of the superior mesenteric artery in affecting margin status after pancreatoduodenectomy for pancreatic adenocarcinoma. HPB 18:305–311

    Article  Google Scholar 

  34. Ishizaki Y, Sugo H, Yoshimoto J, Imamura H, Kawasaki S (2010) Pancreatoduodenectomy with or without early ligation of the inferior pancreatoduodenal artery: comparison of intraoperative blood loss and short-term outcome. World J Surg 34:2939–2944

    Article  Google Scholar 

  35. Ricci C, Casadei R, Taffurelli G, Pacilio CA, Ricciardiello M, Minni F (2018) Minimally invasive pancreaticoduodenectomy: what is the best “choice”? A systematic review and network meta-analysis of non-randomized comparative studies. World J Surg 42:788–805

    Article  Google Scholar 

  36. Ferrone CR, Marchegiani G, Hong TS, Ryan DP, Deshpande V, McDonnell EI, Sabbatino F, Santos DD, Allen JN, Blaszkowsky LS, Clark JW, Faris JE, Goyal L, Kwak EL, Murphy JE, Ting DT, Wo JY, Zhu AX, Warshaw AL, Lillemoe KD, Fernández-del Castillo C (2015) Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann Surg 261:12–17

    Article  Google Scholar 

  37. Belli C, Cereda S, Anand S, Reni M (2013) Neoadjuvant therapy in resectable pancreatic cancer: a critical review. Cancer Treat Rev 39:518–524

    Article  Google Scholar 

  38. Casadei R, Di Marco M, Ricci C, Santini D, Serra C, Calculli L, D’Ambra M, Guido A, Morselli-Labate AM, Minni F (2015) Neoadjuvant chemoradiotherapy and surgery versus surgery alone in resectable pancreatic cancer: a single-center prospective, randomized, controlled trial which failed to achieve accrual targets. J Gastrointest Surg 19:1802–1812

    Article  Google Scholar 

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Correspondence to Ugo Boggi.

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Disclosures

Emanuele F Kauffmann, Niccolò Napoli, Francesca Menonna, Sara Iacopi, Carlo Lombardo, Juri Bernardini, Gabriella Amorese, Andrea Cacciato Insilla, Niccola Funel, Daniela Campani, Carla Cappelli, Davide Caramella, and Ugo Boggi have no conflicts of interest or financial ties to disclose.

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Kauffmann, E.F., Napoli, N., Menonna, F. et al. A propensity score-matched analysis of robotic versus open pancreatoduodenectomy for pancreatic cancer based on margin status. Surg Endosc 33, 234–242 (2019). https://doi.org/10.1007/s00464-018-6301-2

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  • DOI: https://doi.org/10.1007/s00464-018-6301-2

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