Skip to main content
SpringerLink
Log in

Short-term and long-term outcomes after robot-assisted versus laparoscopic distal pancreatectomy for pancreatic neuroendocrine tumors (pNETs): a multicenter comparative study

  • Original Article
  • Published:
Langenbeck's Archives of Surgery Aims and scope Submit manuscript

Abstract

Purpose

Minimally invasive surgery has increasingly gained popularity as a treatment of choice for pancreatectomy with encouraging initial results in robotic distal pancreatectomy (RDP). However, few data are available on the comparison between RDP and laparoscopic distal pancreatectomy (LDP) for pancreatic neuroendocrine tumors (pNETs). Our aim, thus, is to compare perioperative and long-term outcomes as well as total costs of RDP and LDP for pNETs.

Methods

All RDPs and LDPs for pNETs performed in four referral centers from 2008 to 2016 were included. Perioperative outcomes, histopathological results, overall (OS) and disease-free survival (DFS), and total costs were evaluated.

Results

Ninety-six RDPs and 85 LDPs were included. Demographic and clinical characteristics were comparable between the two cohorts. Operative time was 36.5 min longer in the RDP group (p = 0.009) but comparable to LDP after removing the docking time (247.9 vs 233.7 min; p = 0.6). LDP related to a lower spleen preservation rate (44.7% vs 65.3%; p < 0.0001) and higher blood loss (239.7 ± 112 vs 162.5 ± 98 cc; p < 0.0001). Advantages in operative time for RDP were documented in case of the spleen preservation procedures (265 ± 41.52 vs 291 ± 23 min; p = 0.04). Conversion rate, postoperative morbidity, and pancreatic fistula rate were similar between the two groups, as well as histopathological data, OS, and DFS. Significant advantages were evidenced for LDP regarding mean total costs (9235 (± 1935) € vs 11,226 (± 2365) €; p < 0.0001).

Conclusions

Both RDP and LDP are safe and efficacious for pNETs treatment. However, RDP offers advantages with a higher spleen preservation rate and lower blood loss. Costs still remain the main limitation of the robotic approach.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Hill JS, McPhee JT, McDade TP, Zhou Z, Sullivan ME, Whalen GF, Tseng JF (2009) Pancreatic neuroendocrine tumors: the impact of surgical resection on survival. Cancer 115(4):741–751. https://doi.org/10.1002/cncr.24065

    Article  PubMed  Google Scholar 

  2. Gagner M, Pomp A, Herrera MF (1996) Early experience with laparoscopic resections of islet cell tumors. Surgery 120(6):1051–1054

    Article  CAS  PubMed  Google Scholar 

  3. Antonakis PT, Ashrafian H, Martinez-Isla A (2015) Pancreatic insulinomas: laparoscopic management. World J Gastrointest Endosc 7(16):1197–1207. https://doi.org/10.4253/wjge.v7.i16.1197

    Article  PubMed  PubMed Central  Google Scholar 

  4. Fernandez-Cruz L, Martinez I, Gilabert R, Cesar-Borges G, Astudillo E, Navarro S (2004) Laparoscopic distal pancreatectomy combined with preservation of the spleen for cystic neoplasms of the pancreas. J Gastrointest Surg 8(4):493–501. https://doi.org/10.1016/j.gassur.2003.11.014

    Article  PubMed  Google Scholar 

  5. Liu H, Peng C, Zhang S, Wu Y, Fang H, Sheng H, Peng S (2007) Strategy for the surgical management of insulinomas: analysis of 52 cases. Dig Surg 24(6):463–470. https://doi.org/10.1159/000111822

    Article  CAS  PubMed  Google Scholar 

  6. Sa Cunha A, Beau C, Rault A, Catargi B, Collet D, Masson B (2007) Laparoscopic versus open approach for solitary insulinoma. Surg Endosc 21(1):103–108. https://doi.org/10.1007/s00464-006-0021-8

    Article  PubMed  Google Scholar 

  7. Fernandez Ranvier GG, Shouhed D, Inabnet WB 3rd (2016) Minimally invasive techniques for resection of pancreatic Neuroendocrine tumors. Surg Oncol Clin N Am 25(1):195–215. https://doi.org/10.1016/j.soc.2015.08.009

    Article  PubMed  Google Scholar 

  8. Melvin WS, Needleman BJ, Krause KR, Schneider C, Wolf RK, Michler RE, Ellison EC (2002) Computer-enhanced robotic telesurgery. Initial experience in foregut surgery. Surg Endosc 16(12):1790–1792. https://doi.org/10.1007/s00464-001-8192-9

    Article  CAS  PubMed  Google Scholar 

  9. 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(1):128–132. https://doi.org/10.1097/SLA.0b013e31825fff08

    Article  PubMed  Google Scholar 

  10. Chen S, Zhan Q, Chen JZ, Jin JB, Deng XX, Chen H, Shen BY, Peng CH, Li HW (2015) Robotic approach improves spleen-preserving rate and shortens postoperative hospital stay of laparoscopic distal pancreatectomy: a matched cohort study. Surg Endosc 29(12):3507–3518. https://doi.org/10.1007/s00464-015-4101-5

    Article  PubMed  Google Scholar 

  11. Giulianotti PC, Sbrana F, Bianco FM, Elli EF, Shah G, Addeo P, Caravaglios G, Coratti A (2010) Robot-assisted laparoscopic pancreatic surgery: single-surgeon experience. Surg Endosc 24(7):1646–1657. https://doi.org/10.1007/s00464-009-0825-4

    Article  PubMed  Google Scholar 

  12. Kang CM, Kim DH, Lee WJ, Chi HS (2011) Conventional laparoscopic and robot-assisted spleen-preserving pancreatectomy: does da Vinci have clinical advantages? Surg Endosc 25(6):2004–2009. https://doi.org/10.1007/s00464-010-1504-1

    Article  PubMed  Google Scholar 

  13. Lai EC, Tang CN (2013) Current status of robot-assisted laparoscopic pancreaticoduodenectomy and distal pancreatectomy: a comprehensive review. Asian J Endosc Surg 6(3):158–164. https://doi.org/10.1111/ases.12040

    Article  PubMed  Google Scholar 

  14. Lee SY, Allen PJ, Sadot E, D'Angelica MI, DeMatteo RP, Fong Y, Jarnagin WR, Kingham TP (2015) Distal pancreatectomy: a single institution's experience in open, laparoscopic, and robotic approaches. J Am Coll Surg 220(1):18–27. https://doi.org/10.1016/j.jamcollsurg.2014.10.004

    Article  PubMed  Google Scholar 

  15. Waters JA, Canal DF, Wiebke EA, Dumas RP, Beane JD, Aguilar-Saavedra JR, Ball CG, House MG, Zyromski NJ, Nakeeb A, Pitt HA, Lillemoe KD, Schmidt CM (2010) Robotic distal pancreatectomy: cost effective? Surgery 148(4):814–823. https://doi.org/10.1016/j.surg.2010.07.027

    Article  PubMed  Google Scholar 

  16. Zureikat AH, Moser AJ, Boone BA, Bartlett DL, Zenati M, Zeh HJ 3rd (2013) 250 robotic pancreatic resections: safety and feasibility. Ann Surg 258(4):554–559; discussion 559-562. https://doi.org/10.1097/SLA.0b013e3182a4e87c

    Article  PubMed  PubMed Central  Google Scholar 

  17. Melvin WS, Needleman BJ, Krause KR, Ellison EC (2003) Robotic resection of pancreatic neuroendocrine tumor. J Laparoendosc Adv Surg Tech A 13(1):33–36. https://doi.org/10.1089/109264203321235449

    Article  CAS  PubMed  Google Scholar 

  18. Falconi M, Plockinger U, Kwekkeboom DJ, Manfredi R, Korner M, Kvols L, Pape UF, Ricke J, Goretzki PE, Wildi S, Steinmuller T, Oberg K, Scoazec JY, Frascati Consensus C, European Neuroendocrine Tumor S (2006) Well-differentiated pancreatic nonfunctioning tumors/carcinoma. Neuroendocrinology 84(3):196–211. https://doi.org/10.1159/000098012

    Article  CAS  PubMed  Google Scholar 

  19. Falconi M, Bartsch DK, Eriksson B, Kloppel G, Lopes JM, O'Connor JM, Salazar R, Taal BG, Vullierme MP, O'Toole D, Conference p BC (2012) ENETS Consensus guidelines for the management of patients with digestive neuroendocrine neoplasms of the digestive system: well-differentiated pancreatic non-functioning tumors. Neuroendocrinology 95(2):120–134. https://doi.org/10.1159/000335587

    Article  CAS  PubMed  Google Scholar 

  20. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196. https://doi.org/10.1097/SLA.0b013e3181b13ca2

    Article  PubMed  Google Scholar 

  21. 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 D (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138(1):8–13. https://doi.org/10.1016/j.surg.2005.05.001

    Article  Google Scholar 

  22. Wente MN, Veit JA, Bassi C, Dervenis C, Fingerhut A, Gouma DJ, Izbicki JR, Neoptolemos JP, Padbury RT, Sarr MG, Yeo CJ, Buchler MW (2007) Postpancreatectomy hemorrhage (PPH): an international study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142(1):20–25. https://doi.org/10.1016/j.surg.2007.02.001

    Article  PubMed  Google Scholar 

  23. Bosman FTCF, Hruban RH (2010) WHO classification of tumours of the digestive system. International Agency for Research on Cancer (IARC), Lyon

    Google Scholar 

  24. Kloppel G, Rindi G, Perren A, Komminoth P, Klimstra DS (2010) The ENETS and AJCC/UICC TNM classifications of the neuroendocrine tumors of the gastrointestinal tract and the pancreas: a statement. Virchows Arch 456(6):595–597. https://doi.org/10.1007/s00428-010-0924-6

    Article  PubMed  Google Scholar 

  25. Ayav A, Bresler L, Brunaud L, Boissel P, Sfcl, Afce (2005) Laparoscopic approach for solitary insulinoma: a multicentre study. Langenbeck's Arch Surg 390(2):134–140. https://doi.org/10.1007/s00423-004-0526-3

    Article  CAS  Google Scholar 

  26. Kim SC, Park KT, Hwang JW, Shin HC, Lee SS, Seo DW, Lee SK, Kim MH, Han DJ (2008) Comparative analysis of clinical outcomes for laparoscopic distal pancreatic resection and open distal pancreatic resection at a single institution. Surg Endosc 22(10):2261–2268. https://doi.org/10.1007/s00464-008-9973-1

    Article  PubMed  Google Scholar 

  27. Warshaw AL (1988) Conservation of the spleen with distal pancreatectomy. Arch Surg 123(5):550–553

    Article  CAS  PubMed  Google Scholar 

  28. Shoup M, Brennan MF, McWhite K, Leung DH, Klimstra D, Conlon KC (2002) The value of splenic preservation with distal pancreatectomy. Arch Surg 137(2):164–168

    Article  PubMed  Google Scholar 

  29. Baldwin KM, Katz SC, Espat NJ, Somasundar P (2011) Laparoscopic spleen-preserving distal pancreatectomy in elderly subjects: splenic vessel sacrifice may be associated with a higher rate of splenic infarction. HPB (Oxford) 13(9):621–625. https://doi.org/10.1111/j.1477-2574.2011.00341.x

    Article  Google Scholar 

  30. Melotti G, Butturini G, Piccoli M, Casetti L, Bassi C, Mullineris B, Lazzaretti MG, Pederzoli P (2007) Laparoscopic distal pancreatectomy: results on a consecutive series of 58 patients. Ann Surg 246(1):77–82. https://doi.org/10.1097/01.sla.0000258607.17194.2b

    Article  PubMed  PubMed Central  Google Scholar 

  31. Zhou W, Lv R, Wang X, Mou Y, Cai X, Herr I (2010) Stapler vs suture closure of pancreatic remnant after distal pancreatectomy: a meta-analysis. Am J Surg 200(4):529–536. https://doi.org/10.1016/j.amjsurg.2009.12.022

    Article  PubMed  Google Scholar 

  32. 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(1):65–73. https://doi.org/10.1080/17474124.2017.1253473

    Article  CAS  PubMed  Google Scholar 

  33. Strijker M, van Santvoort HC, Besselink MG, van Hillegersberg R, Borel Rinkes IH, Vriens MR, Molenaar IQ (2013) Robot-assisted pancreatic surgery: a systematic review of the literature. HPB (Oxford) 15(1):1–10. https://doi.org/10.1111/j.1477-2574.2012.00589.x

    Article  Google Scholar 

  34. Hwang HK, Kang CM, Chung YE, Kim KA, Choi SH, Lee WJ (2013) Robot-assisted spleen-preserving distal pancreatectomy: a single surgeon's experiences and proposal of clinical application. Surg Endosc 27(3):774–781. https://doi.org/10.1007/s00464-012-2551-6

    Article  PubMed  Google Scholar 

  35. Gumbs AA, Gres P, Madureira F, Gayet B (2008) Laparoscopic vs open resection of pancreatic endocrine neoplasms: single institution's experience over 14 years. Langenbeck's Arch Surg 393(3):391–395. https://doi.org/10.1007/s00423-007-0255-5

    Article  Google Scholar 

  36. Zhou ZQ, Kim SC, Song KB, Park KM, Lee JH, Lee YJ (2014) Laparoscopic spleen-preserving distal pancreatectomy: comparative study of spleen preservation with splenic vessel resection and splenic vessel preservation. World J Surg 38(11):2973–2979. https://doi.org/10.1007/s00268-014-2671-3

    Article  PubMed  Google Scholar 

  37. Hu M, Zhao G, Luo Y, Liu R (2011) Laparoscopic versus open treatment for benign pancreatic insulinomas: an analysis of 89 cases. Surg Endosc 25(12):3831–3837. https://doi.org/10.1007/s00464-011-1800-4

    Article  PubMed  Google Scholar 

  38. Haugvik SP, Marangos IP, Rosok BI, Pomianowska E, Gladhaug IP, Mathisen O, Edwin B (2013) Long-term outcome of laparoscopic surgery for pancreatic neuroendocrine tumors. World J Surg 37(3):582–590. https://doi.org/10.1007/s00268-012-1893-5

    Article  PubMed  Google Scholar 

  39. Qu L, Zhiming Z, Xianglong T, Yuanxing G, Yong X, Rong L, Yee LW (2018) Short-and mid-term outcomes of robotic versus laparoscopic distal pancreatosplenectomy for pancreatic ductal adenocarcinoma: a retrospective propensity score-matched study. Int J Surg 55:81–86

    Article  PubMed  Google Scholar 

  40. Guerrini GP, Lauretta A, Belluco C, Olivieri M, Forlin M, Basso S, Breda B, Bertola G, Di Benedetto F (2017) Robotic versus laparoscopic distal pancreatectomy: an up-to-date meta-analysis. BMC Surg 17(1):105

    Article  PubMed  PubMed Central  Google Scholar 

  41. Lo CY, Chan WF, Lo CM, Fan ST, Tam PK (2004) Surgical treatment of pancreatic insulinomas in the era of laparoscopy. Surg Endosc 18(2):297–302. https://doi.org/10.1007/s00464-003-8156-3

    Article  PubMed  Google Scholar 

  42. Butturini G, Damoli I, Crepaz L, Malleo G, Marchegiani G, Daskalaki D, Esposito A, Cingarlini S, Salvia R, Bassi C (2015) A prospective non-randomised single-center study comparing laparoscopic and robotic distal pancreatectomy. Surg Endosc 29(11):3163–3170. https://doi.org/10.1007/s00464-014-4043-3

    Article  PubMed  Google Scholar 

  43. Magge D, Gooding W, Choudry H, Steve J, Steel J, Zureikat A, Krasinskas A, Daouadi M, Lee KK, Hughes SJ, Zeh HJ 3rd, Moser AJ (2013) Comparative effectiveness of minimally invasive and open distal pancreatectomy for ductal adenocarcinoma. JAMA Surg 148(6):525–531. https://doi.org/10.1001/jamasurg.2013.1673

    Article  PubMed  Google Scholar 

  44. Han SH, Han IW, Heo JS, Choi SH, Choi DW, Han S, You YH (2017) Laparoscopic versus open distal pancreatectomy for nonfunctioning pancreatic neuroendocrine tumors: a large single-center study. Surg Endosc 32:443–449. https://doi.org/10.1007/s00464-017-5702-y

    Article  PubMed  Google Scholar 

  45. Xourafas D, Tavakkoli A, Clancy TE, Ashley SW (2015) Distal pancreatic resection for neuroendocrine tumors: is laparoscopic really better than open? J Gastrointest Surg 19(5):831–840. https://doi.org/10.1007/s11605-015-2788-1

    Article  PubMed  PubMed Central  Google Scholar 

  46. Phan GQ, Yeo CJ, Hruban RH, Lillemoe KD, Pitt HA, Cameron JL (1998) Surgical experience with pancreatic and peripancreatic neuroendocrine tumors: review of 125 patients. J Gastrointest Surg 2(5):472–482

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors would like to thank Iana Shutrova for the assistance in proofreading the manuscript.

Author information

Authors and Affiliations

  1. Fondazione Policlinico “A.Gemelli” IRCCS of Rome, CRMPG (Gemelli Pancreatic Advanced Research Center), Università Cattolica del Sacro Cuore of Rome, Largo Agostino Gemelli 8, 00166, Rome, Italy

    Sergio Alfieri, Claudio Fiorillo, Fausto Rosa, Roberta Menghi, Giovanni Battista Doglietto & Giuseppe Quero

  2. Casa di Cura Pederzoli, Via Monte Baldo 24, 37019, Peschiera del Garda, Verona, Italy

    Giovanni Butturini & Isacco Damoli

  3. Chirurgia Generale Universitaria dell’Ospedale di Cisanello, Via Paradisa, 2, 56124, Pisa, Italy

    Ugo Boggi, Luca Morelli, Fabio Vistoli, Nelide De Lio & Gregorio Di Franco

  4. Fondazione IRCCS Policlinico San Matteo, Viale Camillo Golgi, 19, 27100, Pavia, Italy

    Andrea Pietrabissa, Andrea Peri & Luigi Pugliese

  5. Dipartimento di Chirurgia Generale e Pancreatica, Policlinico G.B. Rossi, Piazzale Ludovico Antonio Scuro 10, 37134, Verona, Italy

    Marco Ramera, Alessandro Esposito & Luca Landoni

  6. Digestive Surgical Unit, Department of Surgery, Fondation “A.Gemelli” Hospital of Rome, Catholic University of Sacred Hearth, Largo Agostino Gemelli, 8, 00168, Rome, Italy

    Giuseppe Quero

Authors
  1. Sergio Alfieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giovanni Butturini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ugo Boggi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea Pietrabissa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luca Morelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fabio Vistoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Isacco Damoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrea Peri
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudio Fiorillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Luigi Pugliese
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Marco Ramera
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Nelide De Lio
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Gregorio Di Franco
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Alessandro Esposito
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Luca Landoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Fausto Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Roberta Menghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Giovanni Battista Doglietto
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Giuseppe Quero
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

The Italian Robotic pNET Group

Contributions

Study conception and design: SA, GB, UB, AP, and LM. Acquisition of data: FV, ID, GQ, AE, and LL. Analysis and interpretation of data: AP, CF, LP, MR, NDL, and GDF. Drafting of the manuscript: GQ, FR, and RM. Critical revision of the manuscript: SA, GB, GBD, UB, and AP.

Corresponding author

Correspondence to Giuseppe Quero.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. For this type of study, formal consent is not required.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alfieri, S., Butturini, G., Boggi, U. et al. Short-term and long-term outcomes after robot-assisted versus laparoscopic distal pancreatectomy for pancreatic neuroendocrine tumors (pNETs): a multicenter comparative study. Langenbecks Arch Surg 404, 459–468 (2019). https://doi.org/10.1007/s00423-019-01786-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00423-019-01786-x

Keywords

Search

Navigation