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Laparoscopic pancreatic enucleation: cystic lesions and proximity to the Wirsung duct increase postoperative pancreatic fistula

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Abstract

Background

Risk factors for postoperative pancreatic fistula (POPF) following pancreatic enucleation by the open approach (OpenEN) are well known. However, ENs are more frequently performed laparoscopically (LapEN). The aim of this study was to analyze the risk factors of POPF following LapEN.

Methods and patients

All patients in our prospective database who underwent LapEN were evaluated. We report the demographics, surgical, early and long-term outcomes. Numerous variables were analyzed to identify the risk factors of POPF.

Results

From 2008 to 2020, 650 laparoscopic pancreatic resections were performed including 64 EN (10%). The median age was 51 years old (17–79), median BMI was 24 (19–48), and 44 patients were women (69%). The main presentation was an incidental diagnosis (n = 40; 62%), pain (n= 10;16%), and hypoglycemia (n = 8;12%). The main indications were neuroendocrine tumors (40; 63%), mucinous cystadenomas (15; 23%), intraductal papillary mucinous neoplasie (3; 5%), and other benign cysts (6; 9%). Lesions were located on the distal pancreas (43; 67%), head (n = 17; 27%), and neck (4; 6%). The median size was 20 mm (9–110); 30 mm (20–110) for mucinous cystadenoma and 18 mm (8–33) for NET. The median operative time was 90 mn (30–330), median blood loss was 20 ml (0–800) ml, and there were no transfusions and one conversion. There were no mortalities and overall morbidity (n = 22; 34%) included grades B and C POPF (10;16%) and post-pancreatectomy hemorrhage (4; 6%). The median hospital stay was 7 days (3–42). There were no invaded lymph nodes and all cystic lesions were nonmalignant. After a mean follow-up of 24 months, there was no recurrence. The risk factors for grades B/C POPF were mucinous cystadenoma and proximity to the Wirsung duct < 3 mm.

Conclusion

In this series, the outcome of LapEN was excellent with no mortality and a low rate of morbidity. However, the risk of POPF is increased with cystic lesions and those close to the Wirsung duct.

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References

  1. Asbun HJ, Moekotte AL, Vissers FL et al (2020) The Miami international evidence-based guidelines on minimally invasive pancreas resection. Ann Surg 271(1):1–14

    Article  Google Scholar 

  2. Dokmak S, Ftériche FS, Aussilhou B et al (2017) The Largest European Single-Center Experience: 300 laparoscopic pancreatic resections. J Am Coll Surg 225(2):226-234.e2

    Article  Google Scholar 

  3. Kooby DA, Gillespie T, Bentrem D et al (2008) Left-sided pancreatectomy: a multicenter comparison of laparoscopic and open approaches. Ann Surg 248(3):438–446

    Article  Google Scholar 

  4. Song KB, Kim SC, Park JB et al (2011) Single-center experience of laparoscopic left pancreatic resection in 359 consecutive patients: changing the surgical paradigm of left pancreatic resection. Surg Endosc 25(10):3364–3372

    Article  Google Scholar 

  5. de Rooij T, van Hilst J, van Santvoort H et al (2019) Minimally Invasive Versus Open Distal Pancreatectomy (LEOPARD): a multicenter patient-blinded randomized controlled trial. Ann Surg 269(1):2–9

    Article  Google Scholar 

  6. Bjornsson B, Larsson AL, Hjalmarsson C, Gasslander T, Sandstrom P (2020) Comparison of the duration of hospital stay after laparoscopic or open distal pancreatectomy: randomized controlled trial. Br J Surg 1:1

    Google Scholar 

  7. Dedieu A, Rault A, Collet D et al (2011) Laparoscopic enucleation of pancreatic neoplasm. Surg Endosc 25(2):572–576

    Article  CAS  Google Scholar 

  8. Fernández-Cruz L, Molina V, Vallejos R et al (2012) Outcome after laparoscopic enucleation for non-functional neuroendocrine pancreatic tumours. HPB (Oxford) 14(3):171–176

    Article  Google Scholar 

  9. Sauvanet A, Gaujoux S, Blanc B, Couvelard A, Dokmak S, Vullierme MP, Ruszniewski P, Belghiti J, Lévy P (2014) Parenchyma-sparing pancreatectomy for presumed noninvasive intraductal papillary mucinous neoplasms of the pancreas. Ann Surg 260(2):364–371. https://doi.org/10.1097/SLA.0000000000000601

    Article  Google Scholar 

  10. Crippa S, Bassi C, Salvia R, Falconi M, Butturini G, Pederzoli P (2007) Enucleation of pancreatic neoplasms. Br J Surg 94(10):1254–1259. https://doi.org/10.1002/bjs.5833

    Article  CAS  Google Scholar 

  11. Sahakyan MA, Røsok BI, Kazaryan AM, Barkhatov L, Haugvik SP, Fretland ÅA, Ignjatovic D, Labori KJ, Edwin B (2017) Role of laparoscopic enucleation in the treatment of pancreatic lesions: case series and case-matched analysis. Surg Endosc 31(5):2310–2316. https://doi.org/10.1007/s00464-016-5233-y

    Article  Google Scholar 

  12. 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(2):205–213

    Article  Google Scholar 

  13. Bassi C, Marchegiani G, Dervenis C et al (2017) The 2016 update of the International Study Group (ISGPS) definition and grading of postoperative pancreatic fistula: 11 Years After. Surgery 161(3):584–591

    Article  Google Scholar 

  14. Wente MN, Bassi C, Dervenis C et al (2007) Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery 142(5):761–768

    Article  Google Scholar 

  15. Wente MN, Veit JA, Bassi C et al (2007) Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery 142(1):20–25

    Article  Google Scholar 

  16. Pitt SC, Pitt HA, Baker MS, Christians K, Touzios JG, Kiely JM, Weber SM, Wilson SD, Howard TJ, Talamonti MS, Rikkers LF (2009) Small pancreatic and periampullary neuroendocrine tumors: resect or enucleate? J Gastrointest Surg 13(9):1692–1698. https://doi.org/10.1007/s11605-009-0946-z

    Article  Google Scholar 

  17. Kuroki T, Eguchi S (2014) Laparoscopic parenchyma-sparing pancreatectomy. J Hepatobiliary Pancreat Sci 21(5):323–327. https://doi.org/10.1002/jhbp.29

    Article  Google Scholar 

  18. 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. Langenbecks Arch Surg 399(3):315–321. https://doi.org/10.1007/s00423-014-1171-0

    Article  Google Scholar 

  19. Heidsma CM, Tsilimigras DI, van Dieren S, Rocha F, Abbott DE, Fields R, Smith PM, Poultsides GA et al (2021) Indications and outcomes of enucleation versus formal pancreatectomy for pancreatic neuroendocrine tumors. HPB (Oxford) 23(3):413–421. https://doi.org/10.1016/j.hpb.2020.06.015

    Article  Google Scholar 

  20. Hüttner FJ, Koessler-Ebs J, Hackert T, Ulrich A, Büchler MW, Diener MK (2015) Meta-analysis of surgical outcome after enucleation versus standard resection for pancreatic neoplasms. Br J Surg 102(9):1026–1036. https://doi.org/10.1002/bjs.9819

    Article  Google Scholar 

  21. 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 16(7):1347–1353. https://doi.org/10.1007/s11605-012-1893-7

    Article  CAS  Google Scholar 

  22. Weilin M, Xu H, Yang L, Wenqi C, Huanyu W, Wentao Z, Dayong J, Wenchuan W, Dansong W, Tiantao K, Lei Z, Wenhui L, Xuefeng X (2020) Propensity score-matched analysis of clinical outcome after enucleation versus regular pancreatectomy in patients with small non-functional pancreatic neuroendocrine tumors. Pancreatology 20(2):169–176. https://doi.org/10.1016/j.pan.2019.12.007

    Article  Google Scholar 

  23. Giuliani T, De Pastena M, Paiella S, Marchegiani G, Landoni L, Festini M, Ramera M, Marinelli V, Casetti L, Esposito A, Bassi C, Salvia R (2021) Pancreatic enucleation patients share the same quality of life as the general population at long-term follow-up: a propensity-score matched analysis. Ann Surg. https://doi.org/10.1097/SLA.0000000000004911

    Article  Google Scholar 

  24. Costi R, Randone B, Mal F, Basato S, Lévard H, Gayet B (2013) A critical appraisal of laparoscopic pancreatic enucleations: right-sided procedures (Pancreatic Head, Uncus) are not mini-invasive surgery. Surg Laparosc Endosc Percutan Tech 23(6):524–531. https://doi.org/10.1097/SLE.0b013e31828e3d86

    Article  Google Scholar 

  25. Faitot F, Gaujoux S, Barbier L, Novaes M, Dokmak S, Aussilhou B, Couvelard A, Rebours V, Ruszniewski P, Belghiti J, Sauvanet A (2015) Reappraisal of pancreatic enucleations: a single-center experience of 126 procedures. Surgery 158(1):201–210. https://doi.org/10.1016/j.surg.2015.03.023

    Article  Google Scholar 

  26. Tanaka M, Fernández-Del Castillo C, Kamisawa T et al (2017) Revisions of international consensus Fukuoka guidelines for the management of IPMN of the pancreas. Pancreatology 17(5):738–753

    Article  Google Scholar 

  27. Bernardoni L, Crinò SF, De Conti G, Conti Bellocchi MC, De Pretis N, Amodio A, Frulloni L, Gabbrielli A (2017) Preliminary experience with pancreatic sphincterotomy as treatment for intraductal papillary mucinous neoplasm-associated recurrent pancreatitis. Endosc Int Open 5(11):E1144–E1150. https://doi.org/10.1055/s-0043-119753

    Article  Google Scholar 

  28. Dokmak S, Ftériche FS, Meniconi RL, Aussilhou B, Duquesne I, Perrone G, Romdhani C, Belghiti J, Lévy P, Soubrane O, Sauvanet A (2019) Pancreatic fistula following laparoscopic distal pancreatectomy is probably unrelated to the stapler size but to the drainage modality and significantly decreased with a small suction drain. Langenbecks Arch Surg 404(2):203–212. https://doi.org/10.1007/s00423-019-01756-3

    Article  Google Scholar 

  29. 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 33(10):3192–3199. https://doi.org/10.1007/s00464-019-06967-9

    Article  Google Scholar 

  30. Zhang RC, Zhou YC, Mou YP, Huang CJ, Jin WW, Yan JF, Wang YX, Liao Y (2016) Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis. Surg Endosc 30(7):2657–2665. https://doi.org/10.1007/s00464-015-4538-6

    Article  Google Scholar 

  31. 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 158(5):1203–1210. https://doi.org/10.1016/j.surg.2014.10.008

    Article  Google Scholar 

  32. Ei S, Mihaljevic AL, Kulu Y, Kaiser J, Hinz U, Büchler MW, Hackert T (2020) Enucleation for benign or borderline tumors of the pancreas: comparing open and minimally invasive surgery. HPB (Oxford) 18:S1365. https://doi.org/10.1016/j.hpb.2020.10.001

    Article  Google Scholar 

  33. Duconseil P, Marchese U, Ewald J, Giovannini M, Mokart D, Delpero JR, Turrini O (2018) A pancreatic zone at higher risk of fistula after enucleation. World J Surg Oncol 16(1):177. https://doi.org/10.1186/s12957-018-1476-5

    Article  Google Scholar 

  34. 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 16(10):1883–1887. https://doi.org/10.1007/s11605-012-1971-x

    Article  Google Scholar 

  35. Zhang T, Xu J, Wang T, Liao Q, Dai M, Zhao Y (2013) Enucleation of pancreatic lesions: indications, outcomes, and risk factors for clinical pancreatic fistula. J Gastrointest Surg 17:2099–2104

    Article  Google Scholar 

  36. 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 117(2):182–190. https://doi.org/10.1002/jso.24804

    Article  CAS  Google Scholar 

  37. 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 102(10):1258–1266. https://doi.org/10.1002/bjs.9843

    Article  CAS  Google Scholar 

  38. Xu J, Li F, Zhan H, Liu H, Wu D, Hu S, Wang L (2021) Laparoscopic enucleation of pancreatic tumours: a single-institution experience of 66 cases. ANZ J Surg 91(1–2):106–110. https://doi.org/10.1111/ans.16450

    Article  Google Scholar 

  39. Crippa S, Salvia R, Warshaw AL, Domínguez I, Bassi C, Falconi M, Thayer SP, Zamboni G, Lauwers GY, Mino-Kenudson M, Capelli P, Pederzoli P, Castillo CF (2008) Mucinous cystic neoplasm of the pancreas is not an aggressive entity: lessons from 163 resected patients. Ann Surg 247(4):571–579. https://doi.org/10.1097/SLA.0b013e31811f4449

    Article  Google Scholar 

  40. Griffin JF, Page AJ, Samaha GJ, Christopher A, Bhaijee F, Pezhouh MK, Peters NA, Hruban RH, He J, Makary MA, Lennon AM, Cameron JL, Wolfgang CL, Weiss MJ (2017) Patients with a resected pancreatic mucinous cystic neoplasm have a better prognosis than patients with an intraductal papillary mucinous neoplasm: a large single institution series. Pancreatology 17(3):490–496. https://doi.org/10.1016/j.pan.2017.04.003

    Article  Google Scholar 

  41. Park JW, Jang JY, Kang MJ, Kwon W, Chang YR, Kim SW (2014) Mucinous cystic neoplasm of the pancreas: is surgical resection recommended for all surgically fit patients? Pancreatology 14(2):131–136. https://doi.org/10.1016/j.pan.2013.12.006

    Article  Google Scholar 

  42. Dokmak S, Aussilhou B, Ftériche FS, Dembinski J, Romdhani C, Sauvanet A (2021) The outcome of laparoscopic pancreatoduodenectomy is improved with patient selection and the learning curve. Surg Endosc. https://doi.org/10.1007/s00464-021-08493-z

    Article  Google Scholar 

  43. Dembinski J, Hammoud D, Lemaire A, Ftériche FS, Aussilhou B, Sauvanet A, Dokmak S (2021) Laparoscopic enucleation of a deep neuroendocrine tumor of the pancreatic head avoiding pancreatoduodenectomy. Ann Surg Oncol. https://doi.org/10.1245/s10434-021-09723-3

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank D.Roche for her editorial assistance and correction of the article.

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Correspondence to Safi Dokmak.

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Béatrice Aussilhou, Morgane Bouquot, Fadhel Samir Ftériche, Mickael Lesurtel, Alain Sauvanet, and Safi Dokmak have no conflict of interest or financial ties to disclose in relation to the results of the present study.

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Aussilhou, B., Ftériche, F.S., Bouquot, M. et al. Laparoscopic pancreatic enucleation: cystic lesions and proximity to the Wirsung duct increase postoperative pancreatic fistula. Surg Endosc 37, 544–555 (2023). https://doi.org/10.1007/s00464-022-09527-w

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