Abstract
Background
Pancreatic enucleation (PE) is a viable option for the removal of non-malignant pancreatic masses leading to complete preservation of organ function. Nevertheless, PE is associated with substantial rates of post-operative pancreatic fistula (POPF), particularly when the mass is close to the main pancreatic duct (MPD). Preoperative stenting of the MPD may prevent its injury when performing PE. This paper describes a novel technique of “deep” PE preceded by endoscopic stenting of the MPD.
Methods
From January 2017 to May 2019, patients with small pancreatic neuroendocrine tumors proximal to the MPD were candidates for PE with previous stenting of the MPD at the University of Verona, Italy, and at the UCLA Medical Center, Los Angeles, California. The endoscopic stenting was scheduled either the day before or 3 weeks before surgery, depending on the participating institute.
Results
Ten patients were included in this pilot study. The endoscopic procedure was successful and well tolerated in all cases. Open, laparoscopic and robotic PE were performed. Seven patients had surgical complications. Among these, six developed a post-operative pancreatic fistula (POPF), but neither grade C fistulas nor disruptions of the MPD were detected. At pathology, a low grade pancreatic neuroendocrine tumor was confirmed in all cases.
Conclusion
In the setting of high-volume centers, this procedure is safe, and it is associated with acceptable short-term surgical morbidity. The preoperative stenting of the MPD might extend the surgical indications for PE.
Similar content being viewed by others
References
Crippa S, Bassi C, Salvia R, Falconi M, Butturini G, Pederzoli P (2007) Enucleation of pancreatic neoplasms. Br J Surg. https://doi.org/10.1002/bjs.5833
Cauley CE, Pitt HA, Ziegler KM, Nakeeb A, Schmidt CM, Zyromski NJ, House MG, Lillemoe KD (2012) Pancreatic enucleation: improved outcomes compared to resection. J Gastrointest Surg. https://doi.org/10.1007/s11605-012-1893-7
Hackert T, Hinz U, Fritz S, Strobel O, Schneider L, Hartwig W, Büchler MW, Werner J (2011) Enucleation in pancreatic surgery: indications, technique, and outcome compared to standard pancreatic resections. Langenbeck’s Arch Surg. https://doi.org/10.1007/s00423-011-0801-z
Talamini MA, Moesinger R, Yeo CJ, Poulose B, Hruban RH, Cameron JL, Pitt HA (1998) Cystadenomas of the pancreas: is enucleation an adequate operation? Ann Surg. https://doi.org/10.1097/00000658-199806000-00013
Shi Y, Peng C, Shen B, Deng X, Jin J, Wu Z, Zhan Q, Li H (2016) Pancreatic enucleation using the da Vinci robotic surgical system: a report of 26 cases. Int J Med Robot Comput Assist Surg. https://doi.org/10.1002/rcs.1719
Tanaka K, Misawa T, Haruki K, Saito R, Gocho T, Akiba T (2017) Enucleation of solid pseudopapillary tumor with a preoperative nasopancreatic drainage stent in a child. Asian J Endosc Surg. https://doi.org/10.1111/ases.12397
De Bruijn KMJ, Van Eijck CHJ (2015) New-onset diabetes after distal pancreatectomy: a systematic review. Ann Surg. https://doi.org/10.1097/SLA.0000000000000819
Beger HG, Poch B, Mayer B, Siech M (2018) New onset of diabetes and pancreatic exocrine insufficiency after pancreaticoduodenectomy for benign and malignant tumors: a systematic review and meta-analysis of long-term results. Ann Surg. https://doi.org/10.1097/SLA.0000000000002422
Falconi M, Mantovani W, Crippa S, Mascetta G, Salvia R, Pederzoli P (2008) Pancreatic insufficiency after different resections for benign tumours. Br J Surg. https://doi.org/10.1002/bjs.5652
Jilesen APJ, Van Eijck CHJ, Busch ORC, Van Gulik TM, Gouma DJ, Van Dijkum EJMN (2016) Postoperative outcomes of enucleation and standard resections in patients with a pancreatic neuroendocrine tumor. World J Surg. https://doi.org/10.1007/s00268-015-3341-9
Crippa S, Zerbi A, Boninsegna L, Capitanio V, Partelli S, Balzano G, Pederzoli P, Di Carlo V, Falconi M (2012) Surgical management of insulinomas: short- and long-term outcomes after enucleations and pancreatic resections. Arch Surg. https://doi.org/10.1001/archsurg.2011.1843
Brient C, Regenet N, Sulpice L, Brunaud L, Mucci-Hennekine S, Carrère N, Milin J, Ayav A, Pradere B, Hamy A, Bresler L, Meunier B, Mirallié E (2012) Risk factors for postoperative pancreatic fistulization subsequent to enucleation. J Gastrointest Surg. https://doi.org/10.1007/s11605-012-1971-x
Cherif R, Gaujoux S, Couvelard A, Dokmak S, Vuillerme MP, Ruszniewski P, Belghiti J, Sauvanet A (2012) Parenchyma-sparing resections for pancreatic neuroendocrine tumors. J Gastrointest Surg. https://doi.org/10.1007/s11605-012-2002-7
Heeger K, Falconi M, Partelli S, Waldmann J, Crippa S, Fendrich V, Bartsch DK (2014) Increased rate of clinically relevant pancreatic fistula after deep enucleation of small pancreatic tumors. Langenbeck’s Arch Surg. https://doi.org/10.1007/s00423-014-1171-0
Strobel O, Cherrez A, Hinz U, Mayer P, Kaiser J, Fritz S, Schneider L, Klauss M, Büchler MW, Hackert T (2015) Risk of pancreatic fistula after enucleation of pancreatic tumours. Br J Surg. https://doi.org/10.1002/bjs.9843
Wang X, Tan CL, Zhang H, Chen YH, Yang M, Ke NW, Liu XB (2018) Short-term outcomes and risk factors for pancreatic fistula after pancreatic enucleation: a single-center experience of 142 patients. J Surg Oncol. https://doi.org/10.1002/jso.24804
Dalla Valle R, Cremaschi E, Lamecchi L, Guerini F, Rosso E, Iaria M (2019) Open and minimally invasive pancreatic neoplasms enucleation: a systematic review. Surg Endosc. https://doi.org/10.1007/s00464-019-06967-9
Afghani E, Akshintala VS, Khashab MA, Law JK, Hutfless SM, Kim KJ, Lennon AM, Kalloo AN, Singh VK (2014) 5-Fr vs 3-Fr pancreatic stents for the prevention of post-ERCP pancreatitis in high-risk patients: a systematic review and network meta-analysis. Endoscopy. https://doi.org/10.1055/s-0034-1365701
Salvia R, Malleo G, Butturini G, Dal Molin M, Esposito A, Marchegiani G, Paiella S, Malpaga A, Fontana M, Personi B, Bassi C (2013) Perioperative management of patients undergoing pancreatic resection: implementation of a care plan in a tertiary-care center. J Surg Oncol. https://doi.org/10.1002/jso.23285
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. https://doi.org/10.1016/j.surg.2007.05.005
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 (US). https://doi.org/10.1016/j.surg.2016.11.014
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. https://doi.org/10.1016/j.surg.2007.02.001
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. https://doi.org/10.1097/01.sla.0000133083.54934.ae
Lu WJ, Xu B, Gao SL, Dong X, Zhang B, Wu YL (2012) Enucleation of benign or borderline pancreatic head tumors adjacent to the common pancreatic duct. Pancreas. https://doi.org/10.1097/MPA.0b013e318229b891
Jin JB, Qin K, Li H, Wu ZC, Zhan Q, Deng XX, Chen H, Shen BY, Peng CH, Li HW (2016) Robotic enucleation for benign or borderline tumours of the pancreas: a retrospective analysis and comparison from a high-volume centre in Asia. World J Surg. https://doi.org/10.1007/s00268-016-3655-2
Shimura T, Suehiro T, Suzuki H, Mochida Y, Okada K, Araki K, Kuwano H (2007) Preoperative endoscopic pancreatic stenting for prophylaxis of pancreatic duct disruption during extirpation of a pancreatic head tumor. Am J Surg. https://doi.org/10.1016/j.amjsurg.2006.11.043
Song KB, Kim SC, Hwang DW, Lee JH, Lee DJ, Lee JW, Jun ES, Sin SH, Kim HE, Park KM, Lee YJ (2015) Enucleation for benign or low-grade malignant lesions of the pancreas: Single-center experience with 65 consecutive patients. Surgery (US). https://doi.org/10.1016/j.surg.2014.10.008
Ide S, Uchida K, Inoue M, Koike Y, Otake K, Matsushita K, Hashimoto K, Nagano Y, Inoue H, Isaji S, Kusunoki M (2012) Tumor enucleation with preoperative endoscopic transpapillary stenting for pediatric insulinoma. Pediatr Surg Int. https://doi.org/10.1007/s00383-012-3104-8
Misawa T, Imazu H, Fujiwara Y, Kitamura H, Tsutsui N, Ito R, Shiba H, Futagawa Y, Wakiyama S, Ishida Y, Yanaga K (2013) Efficacy of nasopancreatic stenting prior to laparoscopic enucleation of pancreatic neuroendocrine tumor. Asian J Endosc Surg. https://doi.org/10.1111/ases.12006
Kim S, Kim JW, Jung PY, Kwon HY, Shim H, Jang JY, Bae KS (2017) Diagnostic and therapeutic role of endoscopic retrograde pancreatography in the management of traumatic pancreatic duct injury patients: single center experience for 34 years. Int J Surg. https://doi.org/10.1016/j.ijsu.2017.03.054
Krige JEJ, Kotze UK, Navsaria PH, Nicol AJ (2015) Endoscopic and operative treatment of delayed complications after pancreatic trauma: an analysis of 27 civilians treated in an academic Level 1 Trauma Centre. Pancreatology. https://doi.org/10.1016/j.pan.2015.06.008
Buccimazza I, Thomson SR, Anderson F, Naidoo NM, Clarke DL (2006) Isolated main pancreatic duct injuries spectrum and management. Am J Surg. https://doi.org/10.1016/j.amjsurg.2005.11.015
Maire F, Ponsot P, Debove C, Dokmak S, Ruszniewski P, Sauvanet A (2015) Endoscopic management of pancreatic fistula after enucleation of pancreatic tumors. Surg Endosc. https://doi.org/10.1007/s00464-014-4034-4
Tryliskyy Y, Bryce GJ (2018) Post-ERCP pancreatitis: pathophysiology, early identification and risk stratification. Adv Clin Exp Med. https://doi.org/10.17219/acem/66773
Neuhaus H (2004) Therapeutic pancreatic endoscopy. Endoscopy. https://doi.org/10.1055/s-2004-814119
Dumonceau JM, Andriulli A, Elmunzer BJ, Mariani A, Meister T, Deviere J, Marek T, Baron TH, Hassan C, Testoni PA, Kapral C (2014) Prophylaxis of post-ERCP pancreatitis: European Society of Gastrointestinal Endoscopy (ESGE) guideline—updated June 2014. Endoscopy. https://doi.org/10.1055/s-0034-1377875
Zolotarevsky E, Fehmi SM, Anderson MA, Schoenfeld PS, Elmunzer BJ, Kwon RS, Piraka CR, Wamsteker EJ, Scheiman JM, Korsnes SJ, Normolle DP, Kim HM, Elta GH (2011) Prophylactic 5-Fr pancreatic duct stents are superior to 3-Fr stents: a randomized controlled trial. Endoscopy. https://doi.org/10.1055/s-0030-1256305
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
MG and GT designed the study; all authors performed the data collection; MG, CSF, GM and GT wrote the paper; LL, SR, DT and BC revised the paper.
Corresponding author
Ethics declarations
Disclosures
Tommaso Giuliani, Giovanni Marchegiani, Mark D. Girgis, Stefano Francesco Crinò, Venkataraman R. Muthusamy, Laura Bernardoni, Antonio Pea, Marco Ramera, Salvatore Paiella, Luca Landoni, Armando Gabbrielli, Roberto Salvia, Timothy R. Donahue and Claudio Bassi have no conflict of interest or financial ties to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary file1 (MP4 36943 kb)
Rights and permissions
About this article
Cite this article
Giuliani, T., Marchegiani, G., Girgis, M.D. et al. Endoscopic placement of pancreatic stent for “Deep” pancreatic enucleations operative technique and preliminary experience at two high-volume centers. Surg Endosc 34, 2796–2802 (2020). https://doi.org/10.1007/s00464-020-07501-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-020-07501-y