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Parenchyma-sparing surgery for pancreatic endocrine tumors

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Abstract

Enucleation (EN) and middle pancreatectomy (MP) have been proposed as a treatment for G1 and G2 pancreatic neuroendocrine tumors (PNET). The aim of this study is to analyze the outcomes of parenchyma-sparing surgery (PSS) for PNET in an Italian high-volume center. All patients with a histological diagnosis of PNET who underwent surgical resection in our center between January 2010 and January 2016 were included in the study. Demographic, perioperative, and discharge data were collected in a prospective database. Follow-up was considered until March 31, 2016. 99 patients were included. PSS was performed in 22 cases (22.2 %), 18 EN (82 %), and 4 MP (18 %). 89.8 % patients were staged with CT scan, 69.6 % with endoscopic ultrasonography, 48.4 % with MRI, and 47.4 % with 68Ga-PET. Pre-operative histological diagnosis was obtained in 68.6 %. Most of PSS tumors were G1 (n = 15; 68 %) and there were no G3. Nodal sampling was performed in every PSS. Only two patients showed nodal metastatic disease. The median post-operative length of stay was 7 days after PSS. Eleven (50 %) of these patients developed a complication; two (18.2 %) were major complications. Pancreatic fistula developed in ten patients (45.5 %); two (20 %) were type B. There were no type C fistula and no re-operations after PSS. Readmission rate was 9 %. All patients submitted to PSS are alive and free of recurrence. PSS is a safe technique for G1 and G2 PNETs, but it has to be conducted in experienced centers and an extensive nodal sampling and a long follow-up are required for the best oncologic outcome.

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References

  1. Klimstra DS, Modlin IR, Coppola D, Lloyd RV, Suster S (2010) The pathologic classification of neuroendocrine tumors, a review of nomenclature, grading, and staging systems. Pancreas 39:707–712. doi:10.1097/MPA.0b013e3181ec124e

    Article  PubMed  Google Scholar 

  2. 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 Conference, European Neuroendocrine Tumor Society (2006) Well-differentiated pancreatic nonfunctioning tumors/carcinoma. Neuroendocrinology 84(3):196–211. doi:10.1159/000098012

    Article  CAS  PubMed  Google Scholar 

  3. Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, Kos-Kudla B, Kwekkeboom D, Rindi G, Klppel G, Reed N, Kianmanesh R, Jensen RT, all other Vienna Consensus Conference participants (2016) Consensus guidelines update for the management of functional p-NETs (F-p-NETs) and non-functional p-NETs (NF-p-NETs). doi:10.1159/000443171

  4. Rindi G, Petrone G, Inzani F (2014) The 2010 WHO classification of digestive neuroendocrine neoplasms: a critical appraisal four years after its introduction. Endocr Pathol 25:186–192. doi:10.1007/s12022-014-9313-z

    Article  CAS  PubMed  Google Scholar 

  5. Falconi M, Zerbi A, Crippa S, Balzano G, Boninsegna L, Capitanio V, Bassi C, Di Carlo V, Pederzoli P (2010) Parenchyma-preserving resections for small nonfunctioning pancreatic endocrine tumors. Ann Surg Oncol 17:1621–1627. doi:10.1245/s10434-010-0949-8

    Article  PubMed  Google Scholar 

  6. Dindo D, Nicolas Demartines N, Clavien P-A (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. doi:10.1097/01.sla.0000133083.54934.ae

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bassi C, Dervenis C, Butturini G, Fingerhut A, Yeo C, Izbicki J, Neoptolemos J, Sarr M, Traverso W, Buchler M, for the International Study Group on Pancreatic Fistula Definition (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13. doi:10.1016/j.surg.2005.05.001

    Article  PubMed  Google Scholar 

  8. Burns J, Freedman-Cass D (2016) NCCN clinical practice guidelines in oncology. Neuroendocrine Tumors, Version 1

    Google Scholar 

  9. Edge SB, Byrd DR, Compton CC et al (2010) American Joint Committee on cancer staging manual, 7th edn. Springer, New York

    Google Scholar 

  10. Rindi G, Arnold R, Bosman FT, Carneiro F, Hruban RH, Theise ND (2010) Nomenclature and classification of neuroendocrine neoplasms of the digestive system. WHO Classification of Tumours of the Digestive System, 4th edn. International Agency for Research on cancer (IARC), Lyon, p 13

    Google Scholar 

  11. Sandvik OM, Søreide K, Gudlaugsson E, Kvaløy JT, Søreide A (2016) Epidemiology and classification of gastroenteropancreatic neuroendocrine neoplasms using current coding criteria. BJS 103:226–232. doi:10.1002/bjs.10034

    Article  CAS  Google Scholar 

  12. Ito T, Igarashi H, Nakamura K, Sasano H, Okusaka T, Takano K, Komoto I, Tanaka M, Imamura M, Jensen RT, Takayanagi R, Shimatsu A (2015) Epidemiological trends of pancreatic and gastrointestinal neuroendocrine tumors in Japan: a nationwide survey analysis. J Gastroenterol 50:58–64. doi:10.1007/s00535-014-0934-2

    Article  PubMed  Google Scholar 

  13. Scherübl H, Streller B, Stabenow R, Herbst H, Höpfner M, Schwertner C, Steinberg J, Eick J, Ring W, Tiwari K, Zappe SM (2013) Clinically detected gastroenteropancreatic neuroendocrine tumors are on the rise: epidemiological changes in Germany. World J Gastroenterol 19(47):9012–9019. doi:10.3748/wjg.v19.i47.9012

    Article  PubMed  PubMed Central  Google Scholar 

  14. Mehrabi A, Fischer L, Hafezi M, Dirlewanger A, Grenacher L, Diener MK, Fonouni H, Golriz M, Garoussi C, Fard N, Rahbari NN, Werner J, Büchler MW (2014) A systematic review of localization, surgical treatment options, and outcome of insulinoma. Pancreas 43:675–686. doi:10.1097/MPA.0000000000000110

    Article  PubMed  Google Scholar 

  15. Knigge U, Hansen CP (2012) Surgery for GEP-NETs. Best Pract Res Clin Gastroenterol 26:819–831. doi:10.1016/j.bpg.2012.12.005

    Article  PubMed  Google Scholar 

  16. Al-Kurd A, Chapchay K, Grozinsky-Glasberg S, Mazeh H (2014) Laparoscopic resection of pancreatic neuroendocrine tumors. World J Gastroenterol 20(17):4908–4916. doi:10.3748/wjg.v20.i17.4908

    Article  PubMed  PubMed Central  Google Scholar 

  17. Sven-Petter Haugvik S-P, Marangos IP, Røsok BI, Pomianowska E, Gladhaug IP, Mathisen Ø, Edwin B (2013) Long-term outcome of laparoscopic surgery for pancreatic neuroendocrine tumors. World J Surg 37:582–590. doi:10.1007/s00268-012-1893-5

    Article  PubMed  Google Scholar 

  18. Casadei R, Ricci C, D’Ambra M, Marrano N, Alagna V, Rega D, Monari F, Minni F (2010) Laparoscopic versus open distal pancreatectomy in pancreatic tumors: a case-control study. Updates Surg 62:171–174. doi:10.1007/s13304-010-0027-6

    Article  PubMed  Google Scholar 

  19. Braga M, Ridolfi C, Balzano G, Castoldi R, Pecorelli N, Di Carlo V (2012) Learning curve for laparoscopic distal pancreatectomy in a high-volume hospital. Updates Surg 64:179–183. doi:10.1007/s13304-012-0163-2

    Article  PubMed  Google Scholar 

  20. Hashim YM, Trinkaus KM, Linehan DC, Strasberg SS, Fields RC, Dengfeng C, Hawkins WG (2014) Regional lymphadenectomy is indicated in the surgical treatment of pancreatic neuroendocrine tumors (PNETs). Ann Surg 259(2):197–203. doi:10.1097/SLA.0000000000000348

    Article  PubMed  PubMed Central  Google Scholar 

  21. Bilimoria KY, Talamonti MS, Tomlinson JS et al (2008) Prognostic score predicting survival after resection of pancreatic neuroendocrine tumors: analysis of 3851 patients. Ann Surg 247:490–500. doi:10.1097/SLA.0b013e31815b9cae

    Article  PubMed  Google Scholar 

  22. Yoo YJ, Yang SJ, Hwang HK, Kang CM, Kim H, Lee WJ (2015) Overestimated oncologic significance of lymph node metastasis in G1 nonfunctioning neuroendocrine tumor in the left side of the pancreas. Medicine 94(36):e1404. doi:10.1097/MD.0000000000001404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Parekh JR, Wang SC, Bergsland EK, Venook AP, Warren RS, Kim GE, Nakakura EK (2012) Lymph node sampling rates and predictors of nodal metastasis in pancreatic neuroendocrine tumor resections the UCSF experience with 149 patients. Pancreas 41:840–844. doi:10.1097/MPA.0b013e31823cdaa0

    Article  PubMed  Google Scholar 

  24. DiNorcia J, Lee MK, Reavey PL, Genkinger JM, Lee JA, Schrope BA, Chabot JA, Allendorf JD (2010) One hundred thirty resections for pancreatic neuroendocrine tumor: evaluating the impact of minimally invasive and parenchyma-sparing techniques. J Gastrointest Surg 14:1536–1546. doi:10.1007/s11605-010-1319-3

    Article  PubMed  Google Scholar 

  25. Reber HA (2007) Middle pancreatectomy: why I rarely do it. J Gastrointest Surg 11(6):730–732. doi:10.1007/s11605-007-0188-x

    Article  PubMed  Google Scholar 

  26. Jilesen APJ, van Eijck CHJ, in’t Hof KH, van Dieren S, Gouma DJ, Nieveen van Dijkum EJM (2016) Postoperative complications, in-hospital mortality and 5-year survival after surgical resection for patients with a pancreatic neuroendocrine tumor: a systematic review. World J Surg 40:729–748. doi:10.1007/s00268-015-3328-6

    Article  PubMed  Google Scholar 

  27. 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. BJS 102:1026–1036. doi:10.1002/bjs.9819

    Article  Google Scholar 

  28. Beger HG, Siech M, Poch B, Mayer B, Schoenberg MH (2015) Limited surgery for benign tumours of the pancreas: a systematic review. World J Surg 39:1557–1566. doi:10.1007/s00268-015-2976-x

    Article  CAS  PubMed  Google Scholar 

  29. Pitt SC, Pitt HA, Baker MS et al (2009) Small pancreatic and periampullary neuroendocrine tumors: resect or enucleate? J Gastrointest Surg 13:1692–1698. doi:10.1007/s11605-009-0946-z

    Article  PubMed  PubMed Central  Google Scholar 

  30. Casadei R, Ricci C, Rega D et al (2010) Pancreatic endocrine tumors less than 4 cm in diameter: resect or enucleate? A singlecenter experience. Pancreas 39:825–828. doi:10.1097/MPA.0b013e3181cf155c

    Article  PubMed  Google Scholar 

  31. Mauriello C, Napolitano S, Gambardella C, Candela G, De Vita F, Orditura M, Sciascia V, Tartaglia E, Lanza M, Santini L, Conzo G (2015) Conservative management and parenchyma-sparing resections of pancreatic neuroendocrine tumors: literature review. Int J Surg 21:S10–S14. doi:10.1016/j.ijsu.2015.04.089

    Article  PubMed  Google Scholar 

  32. Crippa S, Bassi C, Warshaw AL, Falconi M, Partelli S, Thayer SP, Pederzoli P, Fernandez-del Castillo C (2007) Middle pancreatectomy indications, short- and long-term operative outcomes. Ann Surg 246:69–76. doi:10.1097/01.sla.0000262790.51512.57

    Article  PubMed  PubMed Central  Google Scholar 

  33. Orditura M, Petrillo A, Ventriglia J, Diana A, Laterza MM, Fabozzi A, Savastano B, Franzese E, Conzo G, Santini L, Ciardiello F, De Vita F (2016) Pancreatic neuroendocrine tumors: nosography, management and treatment. Int J Surg 28:S156–S162. doi:10.1016/j.ijsu.2015.12.052

    Article  PubMed  Google Scholar 

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Correspondence to Fara Uccelli.

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The authors declare that there is no conflict of interests regarding the publication of this paper.

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The present study received our local ethical committee approval and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

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This article does not contain any studies with animals performed by any of the authors. This article is also compliant with ethical standard for research involving human participants.

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All patients gave their informed consent for data collection prior to their inclusion in this study.

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Uccelli, F., Gavazzi, F., Capretti, G. et al. Parenchyma-sparing surgery for pancreatic endocrine tumors. Updates Surg 68, 313–319 (2016). https://doi.org/10.1007/s13304-016-0400-1

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