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Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis



The studies comparing laparoscopic enucleation (LE) with open enucleation (OE) are limited. This study aimed to compare perioperative outcomes of patients undergoing LE and OE and to assess the pancreatic function after LE.


Between February 2001 and July 2014, patients who underwent enucleation were reviewed. Patients were divided into two groups as LE and OE. Data considered for comparison analysis were patient demographics, intraoperative variables, morbidity, postoperative hospital stay, mortality, pathologic findings, and long-term follow-up (including pancreatic function).


Thirty-seven patients (15 LE and 22 OE) were included in the final analysis. Baseline characteristics were similar in the two groups. LE group showed significantly shorter operating time (118.2 ± 33.1 vs. 155.2 ± 44.3 min, p = 0.009), lower estimated blood loss (80.0 ± 71.2 vs. 195.5 ± 103.4 ml, p = 0.001), shorter first flatus time (1.8 ± 1.0 vs. 3.4 ± 1.8 days, p = 0.004), shorter diet start time (2.4 ± 1.0 vs. 4.4 ± 2.0 days, p = 0.001), shorter postoperative hospital stay (7.9 ± 3.4 vs. 11.2 ± 5.7 days, p = 0.046). Postoperative outcomes, including morbidity (40.0 vs. 45.5 %, p = 1.000), grade B/C pancreatic fistula rates (20.0 vs. 13.6 %, p = 0.874), and mortality, were similar in the two groups. The median follow-up period was 47 months (range 7–163 months). No local recurrence or distant metastasis was detected in either group. Only one patient (4.8 %) underwent OE developed new-onset diabetes, in comparison with none in the LE group. One patient (7.1 %) had weight loss and received pancreatic enzyme supplementation in the LE group, in comparison with two patients (9.5 %) in the OE group.


LE is a safe and feasible technique for the benign or low malignant-potential pancreatic neoplasms. Compared to OE, LE had shorter operating time, lower estimated blood loss, and faster recovery. LE could preserve the pancreatic function as the OE.

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  1. 1.

    Al-Haddad M, Schmidt MC, Sandrasegaran K, Dewitt J (2011) Diagnosis and treatment of cystic pancreatic tumors. Clin Gastroenterol Hepatol 9(8):635–648

  2. 2.

    Sahani DV, Bonaffini PA, Fernandez-Del Castillo C, Blake MA (2013) Gastroenteropancreatic neuroendocrine tumors: role of imaging in diagnosis and management. Radiology 266(1):38–61

  3. 3.

    Falconi M, Mantovani W, Crippa S, Mascetta G, Salvia R, Pederzoli P (2008) Pancreatic insufficiency after different resections for benign tumours. Br J Surg 95(1):85–91

  4. 4.

    Nakamura H, Murakami Y, Uemura K, Hayashidani Y, Sudo T, Ohge H, Sueda T (2009) Predictive factors for exocrine pancreatic insufficiency after pancreatoduodenectomy with pancreaticogastrostomy. J Gastrointest Surg 13(7):1321–1327

  5. 5.

    Shibata S, Sato T, Andoh H, Yasui O, Yoshioka M, Kurokawa T, Watanabe G, Ise N, Kotanagi H, Asanuma Y (2004) Outcomes and indications of segmental pancreatectomy. Dig Surg 21(1):48–53

  6. 6.

    Aranha GV, Shoup M (2005) Nonstandard pancreatic resections for unusual lesions. Am J Surg 189(2):223–228

  7. 7.

    Crippa S, Boninsegna L, Partelli S, Falconi M (2010) Parenchyma-sparing resections for pancreatic neoplasms. J Hepatobiliary Pancreat Sci 17(6):782–787

  8. 8.

    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. Langenbecks Arch Surg 396(8):1197–1203

  9. 9.

    Venkat R, Edil BH, Schulick RD, Lidor AO, Makary MA, Wolfgang CL (2012) Laparoscopic distal pancreatectomy is associated with significantly less overall morbidity compared to the open technique: a systematic review and meta-analysis. Ann Surg 255(6):1048–1059

  10. 10.

    Asbun HJ, Stauffer JA (2012) Laparoscopic vs open pancreaticoduodenectomy: overall outcomes and severity of complications using the Accordion Severity Grading System. J Am Coll Surg 215(6):810–819

  11. 11.

    Ayav A, Bresler L, Brunaud L, Boissel P (2005) Laparoscopic approach for solitary insulinoma: a multicentre study. Langenbecks Arch Surg 390(2):134–140

  12. 12.

    Mabrut JY, Fernandez-Cruz L, Azagra JS, Bassi C, Delvaux G, Weerts J, Fabre JM, Boulez J, Baulieux J, Peix JL, Gigot JF, Hepatobiliary and Pancreatic Section (HBPS) of the Royal Belgian Society of Surgery, Belgian Group for Endoscopic Surgery (BGES), Club Coelio (2005) Laparoscopic pancreatic resection: results of a multicenter European study of 127 patients. Surgery 137(6):597–605

  13. 13.

    Fernandez-Cruz L, Blanco L, Cosa R, Rendon H (2008) Is laparoscopic resection adequate in patients with neuroendocrine pancreatic tumors? World J Surg 32(5):904–917

  14. 14.

    Luo Y, Liu R, Hu MG, Mu YM, An LC, Huang ZQ (2009) Laparoscopic surgery for pancreatic insulinomas: a single-institution experience of 29 cases. J Gastrointest Surg 13(5):945–950

  15. 15.

    Rosok BI, Marangos IP, Kazaryan AM, Rosseland AR, Buanes T, Mathisen O, Edwin B (2010) Single-centre experience of laparoscopic pancreatic surgery. Br J Surg 97(6):902–909

  16. 16.

    Dedieu A, Rault A, Collet D, Masson B, Sa Cunha A (2011) Laparoscopic enucleation of pancreatic neoplasm. Surg Endosc 25(2):572–576

  17. 17.

    Costi R, Randone B, Mal F, Basato S, Levard 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

  18. 18.

    Karaliotas C, Sgourakis G (2009) Laparoscopic versus open enucleation for solitary insulinoma in the body and tail of the pancreas. J Gastrointest Surg 13(10):1869

  19. 19.

    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

  20. 20.

    Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138(1):8–13

  21. 21.

    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

  22. 22.

    Hirono S, Tani M, Kawai M, Ina S, Nishioka R, Miyazawa M, Shimizu A, Uchiyama K, Yamaue H (2009) A central pancreatectomy for benign or low-grade malignant neoplasms. J Gastrointest Surg 13(9):1659–1665

  23. 23.

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

  24. 24.

    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(12):2099–2104

  25. 25.

    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 6(2):140–142

  26. 26.

    Zhao YP, Zhan HX, Cong L, Zhang TP, Liao Q, Dai MH, Cai LX, Zhu Y (2012) Risk factors for postoperative pancreatic fistula in patients with insulinomas: analysis of 292 consecutive cases. Hepatobiliary Pancreat Dis Int 11(1):102–106

  27. 27.

    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

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This study was supported by Zhejiang Provincial Key Subject of Medical Science Foundation (Grant No. 11-CX-21) and the project grant from Zhejiang Provincial Education Department (Grant No. Y201432761).

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Correspondence to Yi-Ping Mou.

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Ren-Chao Zhang, Yu-Cheng Zhou, Yi-Ping Mou, Chao-Jie Huang, Wei-Wei Jin, Jia-Fei Yan, Yong-Xiang Wang, and Yi Liao have no conflict of interest or financial ties to disclose.

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Ren-Chao Zhang and Yu-Cheng Zhou have contributed equally to this work.

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Zhang, R., Zhou, Y., Mou, Y. et al. Laparoscopic versus open enucleation for pancreatic neoplasms: clinical outcomes and pancreatic function analysis. Surg Endosc 30, 2657–2665 (2016).

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  • Laparoscopy
  • Enucleation
  • Pancreas
  • Pancreatic function