World Journal of Surgery

, Volume 43, Issue 1, pp 175–182 | Cite as

Implementation of Current ENETS Guidelines for Surgery of Small (≤2 cm) Pancreatic Neuroendocrine Neoplasms in the German Surgical Community: An Analysis of the Prospective DGAV StuDoQ|Pancreas Registry

  • Ioannis MintzirasEmail author
  • Tobias Keck
  • Jens Werner
  • Stefan Fichtner-Feigl
  • Uwe Wittel
  • Norbert Senninger
  • Thorsten Vowinkel
  • Jörg Köninger
  • Matthias Anthuber
  • Bernd Geißler
  • Detlef Klaus Bartsch
  • for the StuDoQ|Pancreas study group of the German Society for General and Visceral Surgery (DGAV)
Original Scientific Report



ENETS guidelines recommend parenchyma-sparing procedures without formal lymphadenectomy, ideally with a minimally invasive laparoscopic approach for sporadic small pNENs (≤2 cm). Non-functioning (NF) small pNENs can also be observed. The aim of the study was to evaluate how these recommendations are implemented in the German surgical community.


Data from the prospective StuDoQ|Pancreas registry of the German Society of General and Visceral Surgery were analyzed regarding patient’s demographics, tumor characteristics, surgical procedures, histology and perioperative outcomes.


Eighty-four (29.2%) of 287 patients had sporadic pNENs ≤2 cm. Forty-three (51.2%) patients were male, and the mean age at diagnosis was 58.8 ± 15.6 years. Twenty-five (29.8%) pNENs were located in the pancreatic head. The diagnosis pNEN was preoperatively established in 53 (65%) of 84 patients. Sixty-two (73.8%) patients had formal pancreatic resections, including partial pancreaticoduodenectomy or total pancreatectomy (21.4%). Only 22 (26.2%) patients underwent parenchyma-sparing resections and 23 (27.4%) patients had minimally invasive procedures. A lymphadenectomy was performed in 63 (75.4%) patients, and lymph node metastases were diagnosed in 6 (7.2%) patients. Eighty-two (97.7%) patients had an R0 resection. Sixty (72%) tumors were classified G1, 24 (28%) tumors G2. Twenty-seven (32.2%) of 84 patients had postoperative relevant Clavien–Dindo grade ≥3 complications. Thirty- and 90-day mortalities were 2.4% and 3.6%.


ENETS guidelines for surgery of small pNENs are yet not well accepted in the German surgical community, since the rate of formal resections with standard lymphadenectomy is high and the minimally invasive approach is underused. The attitude to operate small NF tumors seems to be rather aggressive.



This study has been conducted using the StuDoQ|Pancreas registry provided by the Study, Documentation, and Quality Center (Studien, Dokumentations- und Qualitätszentrum, StuDoQ) of the German Society for General and Visceral Surgery (Deutsche Gesellschaft für Allgemein- und Viszeralchirurgie, DGAV) with the ID StuDoQ-2017-0003. We would like to thank the following colleagues who actively participated in the StuDoQ|Pancreas registry and enrolled patients with pNENs.

StuDoQ|Pancreas study group of the German Society for General and Visceral Surgery (DGAV)

Prof. Dr. Michael Ghadimi, Klinik für Allgemein-, Viszeral- und Kinderchirurgie, Universitätsmedizin Göttingen, Göttingen, Germany, Prof. Dr. Stefan Post, PD Dr. Torsten J. Wilhelm, Chirurgische Klinik, Universitätsmedizin Mannheim, Mannheim, Germany, Prof. Dr. Christoph-Thomas Germer, Klinik & Poliklinik für Allgemein-, Viszeral-, Gefäß- und Kinderchirurgie, Universitätsklinik Würzburg, Würzburg, Germany, Prof. Dr. Waldemar Uhl, PD Dr. med. Orlin Belyaev, Klinik für Allgemein- und Viszeralchirurgie, St. Josef-Hospital, Bochum, Germany, Prof. Dr. Thomas Kraus, Allgemeine, Viszeral und Minimalinvasive Chirurgie, Nordwestkrankenhaus Frankfurt, Frankfurt, Germany, Prof. Dr. Helmut Witzigmann, Allgemein- und Viszeralchirurgie, Städtisches Klinikum Dresden Friedrichstadt, Dresden, Germany, Prof. Dr. Merten Hommann, Zentralklinik Bad Berka, Bad Berka, Germany, Prof. Dr. Ernst Klar, Allgemeine-, Thorax-, Gefäß- und Transplantationschirurgie, Universitätsmedizin Rostock, Rostock, Germany, Prof. Dr. Matthias Glanemann, Klinik für Allgemein-, Viszeral-, Gefäß- und Kinderchirurgie, Universitätsklinikum des Saarlandes, Homburg an der Saar, Germany, Prof. Dr. Carsten Gutt, Allgemein-, Visceral-, Gefäß- und Thoraxchirurgie, Klinikum Memmingen, Memmingen, Germany, Prof. Dr. Thomas Manger, Abteilung für Allgemeine-, Viszeral- und Kinderchirurgie, SRH Waldklinikum Gera, Gera, Germany, Prof. Dr. Hans-Jörg Krämling, Klinik für Allgemein-, Viszeral- und Gefäßchirurgie, EvK Düsseldorf, Düsseldorf, Germany, Prof. Dr. Jörg C. Kalff, PD Dr. Tim R. Glowka, Klinik und Poliklinik für Allgemein-, Viszeral-, Thorax- und Gefäßchirurgie, Universitätsklinikum Bonn, Bonn, Germany, Prof. Dr. Natascha C. Nüssler, Klinik für Allgemein- und Viszeralchirurgie, Endokrine Chirurgie und Coloproktologie, Städt. Klinikum München GmbH, Klinikum Neuperlach, München, Germany, Prof. Dr. Jörg-Peter Ritz, Klinik für Allgemein- und Viszeralchirurgie, Helios Kliniken Schwerin, Schwerin, Germany, Prof. Dr. Winfried Padberg, Allgemein-, Viszeral-, Thorax-, Transplantations- und Kinderchirurgie, Universitätsklinikum Gießen Marburg Standort Gießen, Giessen, Germany, Prof. Dr. Anton J. Kroesen, Klinik für Allgemein-, Viszeral- und Unfallchirurgie, Krankenhaus Porz am Rhein, Köln, Germany, Prof. Dr. Albrecht Stier, Klinik für Allgemein- und Viszeralchirurgie, Helios-Klinik Erfurt, Erfurt, Germany, Prof. Dr. Dietmar Lorenz, Chirurgische Klinik I, Sana Klinikum Offenbach, Offenbach, Germany, Prof. Dr. Wolf Otto Bechstein, Kllinik für Allgemein- und Viszeralchirurgie, Universitätsklinikum Frankfurt, Frankfurt, Germany, Prof. Karl-Jürgen Oldhafer, Allgemein- und Viszeralchirurgie, Asklepios Klinik Barmbek, Hamburg, Germany, PD Dr. Sven Eisold, Klinik für Allgemein- und Viszeralchirurgie, Sana Kliniken Lübeck GmbH, Lübeck, Germany, Dr. med. Ute Tröbs, Allgemein- und Viszeralchirurgie, Kreiskrankenhaus Delitzsch, Delitzsch, Germany, Prof. Dr. Hans-Bernd Reith, Allgemein- und Viszeralchirurgie, Agaplesion Diakoniekliniken Kassel, Kassel, Germany, Franz-Josef Schumacher, Klinik für Allgemein- und Viszeralchirurgie, Katholische Kliniken Oberhausen, Oberhausen, Germany, Prof. Dr. Elke Wagler, Allgemein-, Visceral- und Onkochirurgie, Pleißental-Klinik GmbH, Werdau, Germany, Prof. Dr. Stefan Farkas, Klinik für Allgemein- und Visceralchirurgie, Wiesbaden, Germany, Dr. med. Frank Klammer, Allgemein-, Viszeral- und Thoraxchirurgie, St. Franziskus-Hospital, Ahlen, Germany, Prof. Dr. Matthias Schwarzbach, Klinik für Allgemein-, Viszeral-, Gefäß- und Thoraxchirurgie, Klinikum Frankfurt-Höchst, Frankfurt, Germany, Prof. Dr. Marco Niedergethmann, Klinik für Allgemein- und Viszeralchirurgie, Alfried-Krupp-Krankenhaus, Essen, Germany, Prof. Dr. Norbert Runkel, Allgemein-, Viszeral- und Kinderchirurgie, Schwarzwald-Baar-Klinikum, Villingen-Schwenningen, Germany, Prof. Dr. Pompiliu Piso, Chirurgie I, Barmherzige Brüder Regensburg, Regensburg, Germany, Dr. med. Eric P.M. Lorenz, Viszeralchirurgie, Alexianer KH Hedwigshöhe, Berlin, Germany, PD Dr. Christian Mönch, Dr. Steffanie Bieck, Klinik für Allgemein-, Viszeral- und Transplantationschirurgie, Westpfalz-Klinikum Kaiserslautern, Kaiserslautern, Germany, Prof. Dr. Robert Grützmann, Dr. Max Brunner, Chirurgische Klinik, Universitätsklinikum Erlangen, Erlangen, Germany, Prof. Dr. Helmut Friess, Klinik und Poliklinik für Chirurgie, Klinikum rechts der Isar, TUM, München, Germany.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 1.
    Yao JC, Hassan M, Phan A et al (2008) One hundred years after « carcinoid » : epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol 26:3063–3072CrossRefGoogle Scholar
  2. 2.
    Ito T, Lee L, Hijioka M et al (2015) The up-to-date review of epidemiological pancreatic neuroendocrine tumors in Japan. J Hepatobiliary Pancreat Sci 22:574–577CrossRefGoogle Scholar
  3. 3.
    Metz DC, Jensen RT (2008) Gastrointestinal neuroendocrine tumors: pancreatic endocrine tumors. Gastroenterology 135:1469–1492CrossRefGoogle Scholar
  4. 4.
    Halfdanarson TR, Rabe KG, Rubin J et al (2008) Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis, and recent trend toward improved survival. Ann Oncol 19:1727–1733CrossRefGoogle Scholar
  5. 5.
    Kulke MH, Anthony LB, Bushnell DL et al (2010) NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas 39:735–752CrossRefGoogle Scholar
  6. 6.
    Falconi M, Bartsch DK, Eriksson B et al (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):120–134CrossRefGoogle Scholar
  7. 7.
    Falconi M, Eriksson B, Kaltsas G et al (2016) ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology 103(2):153–171CrossRefGoogle Scholar
  8. 8.
    Partelli S, Bartsch DK, Capdevila J et al (2017) ENETS consensus guidelines for standard of care in neuroendocrine tumours: surgery for small intestinal and pancreatic neuroendocrine tumours. Neuroendocrinology 105(3):255–265CrossRefGoogle Scholar
  9. 9.
    Wellner UF, Klinger C, Lehmann K et al (2017) The pancreatic surgery registry (StuDoQ|Pancreas) of the German society for general and visceral Surgery (DGAV)—presentation and systematic quality evaluation. Trials 18(1):163CrossRefGoogle Scholar
  10. 10.
    Krautz C, Nimptsch U, Weber GF et al (2018) Effect of hospital volume on in-hospital morbidity and mortality following pancreatic surgery in Germany. Ann Surg 267(3):411–417CrossRefGoogle Scholar
  11. 11.
    Klöppel G, Rindi G, Perren A et al (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):595–597CrossRefGoogle Scholar
  12. 12.
    Bassi C, Dervenis C, Butturini G et al (2005) Postoperative pancreatic fistula: an international study group (ISGPF) definition. Surgery 138:8–13CrossRefGoogle Scholar
  13. 13.
    Wente MN, Veit JA, Bassi C et al (2007) Postpancreatectomy hemorrhage (PPH)—an international study group of pancreatic surgery (ISGPS) definition. Surgery 142:20–25CrossRefGoogle Scholar
  14. 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 142:761–768CrossRefGoogle Scholar
  15. 15.
    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):205–213CrossRefGoogle Scholar
  16. 16.
    Plöckinger U, Rindi G, Arnold R et al (2004) Guidelines for the diagnosis and treatment of neuroendocrine gastrointestinal tumours. A consensus statement on behalf of the European neuroendocrine tumour Society (ENETS. Neuroendocrinology 80(6):394–424CrossRefGoogle Scholar
  17. 17.
    Lee LC, Grant CS, Salomao DR et al (2012) Small, nonfunctioning, asymptomatic pancreatic neuroendocrine tumors (PNETs): role for nonoperative management. Surgery 152:965–974CrossRefGoogle Scholar
  18. 18.
    Gaujoux S, Partelli S, Maire F et al (2013) Observational study of natural history of small sporadic nonfunctioning pancreatic neuroendocrine tumors. J Clin Endocrinol Metab 98:4784–4789CrossRefGoogle Scholar
  19. 19.
    Partelli S, Cirocchi R, Crippa S et al (2017) Systematic review of active surveillance versus surgical management of asymptomatic small non-functioning pancreatic neuroendocrine neoplasms. Br J Surg 104(1):34–41CrossRefGoogle Scholar
  20. 20.
    Sharpe SM, In H, Winchester DJ et al (2015) Surgical resection provides an overall survival benefit for patients with small pancreatic neuroendocrine tumors. J Gastrointest Surg 19(1):117–123CrossRefGoogle Scholar
  21. 21.
    Haynes AB, Deshpande V, Ingkakul T et al (2011) Implications of incidentally discovered, non-functioning pancreatic endocrine tumors: short-term and long-term patient outcomes. Arch Surg 146:534–538CrossRefGoogle Scholar
  22. 22.
    Jutric Z, Grendar J, Hoen HM et al (2017) Regional metastatic behavior of nonfunctional pancreatic neuroendocrine tumors: impact of lymph node positivity on survival. Pancreas 46(7):898–903CrossRefGoogle Scholar
  23. 23.
    Manta R, Nardi E, Pagano N et al (2016) Pre-operative diagnosis of pancreatic neuroendocrine tumors with endoscopic ultrasonography and computed tomography in a large series. J Gastrointestin Liver Dis 25(3):317–321Google Scholar
  24. 24.
    Boutsen L, Jouret-Mourin A, Borbath I et al (2018) Accuracy of pancreatic neuroendocrine tumour grading by endoscopic ultrasound-guided fine needle aspiration: analysis of a large cohort and perspectives for improvement. Neuroendocrinology 106(2):158–166CrossRefGoogle Scholar
  25. 25.
    Polenta V, Slater EP, Kann PH et al (2017) Preoperative imaging overestimates the tumor size in pancreatic neuroendocrine neoplasms associated with multiple endocrine neoplasia type 1. World J Surg 42:1440–1447. CrossRefGoogle Scholar
  26. 26.
    Sallinen VJ, Le Large TTY, Tieftrunk E et al (2017) Prognosis of sporadic resected small (≤2 cm) nonfunctional pancreatic neuroendocrine tumors—a multi-institutional study. HPB (Oxford) 20:251–259CrossRefGoogle Scholar
  27. 27.
    Chua TC, Yang TX, Gill AJ et al (2016) Systematic review and meta-analysis of enucleation versus standardized resection for small pancreatic lesions. Ann Surg Oncol 23(2):592–599CrossRefGoogle Scholar
  28. 28.
    Nimptsch U, Krautz C, Weber GF et al (2016) Nationwide in-hospital mortality following pancreatic surgery in Germany is higher than anticipated. Ann Surg 264(6):1082–1090CrossRefGoogle Scholar
  29. 29.
    Siech M, Bartsch D, Beger HG et al (2012) Indications for laparoscopic pancreas operations: results of a consensus conference and the previous laparoscopic pancreas register. Chirurg 83(3):247–253CrossRefGoogle Scholar
  30. 30.
    Drymousis P, Raptis DA, Spalding D et al (2014) Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford) 16(5):397–406CrossRefGoogle Scholar
  31. 31.
    Scherübl H, Streller B, Stabenow R et al (2013) Clinically detected gastroenteropancreatic neuroendocrine tumors are on the rise: epidemiological changes in Germany. World J Gastroenterol 19(47):9012–9019CrossRefGoogle Scholar
  32. 32.
    Begum N, Maasberg S, Plöckinger U et al (2014) Neuroendocrine tumours of the GI tract—data from the German NET registry. Zentralbl Chir 139(3):276–283Google Scholar
  33. 33.
    Kuo EJ, Salem RR (2013) Population-level analysis of pancreatic neuroendocrine tumors 2 cm or less in size. Ann Surg Oncol 20(9):2815–2821CrossRefGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2018

Authors and Affiliations

  • Ioannis Mintziras
    • 1
    Email author
  • Tobias Keck
    • 2
  • Jens Werner
    • 3
  • Stefan Fichtner-Feigl
    • 4
  • Uwe Wittel
    • 4
  • Norbert Senninger
    • 5
  • Thorsten Vowinkel
    • 5
  • Jörg Köninger
    • 6
  • Matthias Anthuber
    • 7
  • Bernd Geißler
    • 7
  • Detlef Klaus Bartsch
    • 1
  • for the StuDoQ|Pancreas study group of the German Society for General and Visceral Surgery (DGAV)
  1. 1.Department of Visceral-, Thoracic- and Vascular SurgeryPhilipps-University MarburgMarburgGermany
  2. 2.Clinic for SurgeryUniversity Clinic Schleswig-HolsteinLübeckGermany
  3. 3.Department of General, Visceral, Vascular and Transplant SurgeryKlinikum der Universität MünchenMunichGermany
  4. 4.Department of General and Visceral SurgeryUniversity Clinic FreiburgFreiburgGermany
  5. 5.Department of General and Visceral SurgeryUniversity Clinic MünsterMünsterGermany
  6. 6.Department of General and Visceral SurgeryKatharinenhospitalStuttgartGermany
  7. 7.Department of General, Visceral and Transplant SurgeryKlinikum AugsburgAugsburgGermany

Personalised recommendations