Enucleation and resections short-term operative outcomes for well-differentiated pancreatic neuroendocrine tumors
https://doi.org/10.16931/1995-5464.2025-3-80-89
Abstract
Aim. To evaluate the short-term outcomes of enucleation and resection procedures for G1 and G2 pancreatic neuroendocrine tumors (PNETs).
Materials and Methods. The study included 171 patients diagnosed with G1 and G2 pancreatic neuroendocrine tumors. Pancreatoduodenectomy was performed in 25 patients, distal pancreatic resection in 60, and tumor enucleation in 86 cases.
Results. Neuroendocrine tumors in the head and neck of the pancreas were identified in 79 patients. Enucleation was performed in 54 cases, and pancreatoduodenectomy in 25. Postoperative complications following enucleation occurred in 22 patients (40.7%), with 1 death; complications after pancreatoduodenectomy were observed in 9 patients (36%), also with 1 death. Tumors located in the body and tail were diagnosed in 92 patients. Enucleation was performed in 32 cases, and distal pancreatic resection in 60. Postoperative complications occurred in 5 patients (15.6%) after enucleation and in 27 patients (45.5%) after distal pancreatic resection.
Conclusion. For well-differentiated pancreatic neuroendocrine tumors, enucleation is a feasible surgical option. The choice of surgical procedure depends on tumor size, its anatomic location with respect to the main pancreatic duct, and the surgeon’s clinical judgment.
About the Authors
V. N. GalkinRussian Federation
Vsevolod N. Galkin – Doct. of Sci. (Med.), Professor, Chief Physician
4, Kolomensky Proezd, Moscow, 115446
D. S. Gorin
Russian Federation
David S. Gorin – Doct. of Sci. (Med.), Head of the Department of Surgery No.5
4, Kolomensky Proezd, Moscow, 115446
A. G. Kriger
Russian Federation
Andrey G. Kriger – Doct. of Sci. (Med.), Professor, Chief Researcher; Professor of the Chair of Emergency and General Surgery named after Professor A.S. Ermolov
4, Kolomensky Proezd, Moscow, 115446
2/1, Barrikadnaya str., Moscow, 125993
T. A. Martirosyan
Russian Federation
Tigran A. Martirosyan – Surgeon of the Department of Surgery No.5; Graduate Student of the Department of Abdominal Surgery
4, Kolomensky Proezd, Moscow, 115446
27, Bol'shaya Serpukhovskaia str., Moscow, 117997
P. V. Markov
Russian Federation
Pavel V. Markov – Doct. of Sci. (Med.), Head of the Department of Abdominal Surgery
27, Bol'shaya Serpukhovskaia str., Moscow, 117997
A. A. Goev
Russian Federation
Aleksandr A. Goev – Cand. of Sсi. (Med.), Surgeon of the Department of Surgery No.5; Associate Professor of the Department of Fundamental Medical Disciplines
4, Kolomensky Proezd, Moscow, 115446
10A, Radio str., Moscow, 105005
A. A. Sokolov
Russian Federation
Aleksandr A. Sokolov – Head of the Ultrasound Department
4, Kolomensky Proezd, Moscow, 115446
G. V. Galkin
Russian Federation
Gleb V. Galkin – Surgeon of the Department of Surgery No.5
4, Kolomensky Proezd, Moscow, 115446
V. I. Panteleev
Russian Federation
Vladimir I. Panteleev – Cand. of Sсi. (Med.), Senior Researcher at the Medical Informatics and Healthcare Economics Research Laboratory
36, Stremyanny lane, Moscow, 115054
References
1. Perry R.R., Feliberti E.C., Hughes M.S. Management of pancreatic neuroendocrine tumors: surgical strategies and controversies. Endocr. Pract. 2024; 30 (10): 908–916. https://doi.org/10.1016/j.eprac.2024.07.010
2. Nagtegaal I.D., Odze R.D., Klimstra D., Paradis V., Rugge M., Schirmacher P., Washington K.M., Carneiro F., Cree I.A.; WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020; 76 (2): 182–188. https://doi.org/10.1111/his.13975
3. Kohno S. Diagnosis and surgical treatment of gastroenteropancreatic neuroendocrine neoplasms: a literature review. Cancer Diagn. Progn. 2022; 2 (2): 115–125. https://doi.org/10.21873/cdp.10085.
4. Bolm L., Nebbia M., Wei A.C., Zureikat A.H., Fernández-Del Castillo C., Zheng J., Pulvirenti A., Javed A.A., Sekigami Y., Petruch N., Qadan M., Lillemoe K.D., He J., Ferrone C.R.; PAncreatic Neuroendocrine Disease Alliance (PANDA). Longterm outcomes of parenchyma-sparing and oncologic resections in patients with nonfunctional pancreatic neuroendocrine tumors <3 cm in a large multicenter cohort. Ann. Surg. 2022; 276 (3): 522–531. https://doi.org/10.1097/SLA.0000000000005559
5. Solodkiy V.A., Kriger A.G., Akhaladze G.G., Goey A.A., Goncharov S.V., Gorin D.S., Zagainov V.E., Kuznetsov N.S., Kuchin D.M., Latkina N.V., Lysanuk M.V., Maistrenko N.A., Martirosyan T.A., Romasсhenko P.N., Shuinova E.A., Yukina M.Y. Enucleation of pancreatic tumors: a multiplecenter study. Pirogov Russian Journal of Surgery. 2023; 2: 13–20. https://doi.org/10.17116/hirurgia202302113 (In Russian)
6. Belousova E.L., Karmazanovsky G.G., Kubyshkin V.A., Kalinin D.V., Kriger A.G., Glotov A.V., Kaldarov A.R. CT features predict the optimal therapeutic approach for pancreatic neuroendocrine neoplasms. Medical Visualization. 2015; 5: 73–82. (In Russian)
7. Kolchenogov P.D. K.P. Sapozhkov’s method of abdominal gastrectomy using mesocolon flap. Grekov’s Bulletin of Surgery. 1957; 78 (6): 23–27. (In Russian)
8. Solodkiy V.A., Kriger A.G., Gorin D.S., Zagainov V.E., Kuznetsov N.S., Latkina N.V., Maistrenko N.A., Martirosyan T.A., Shuinova E.A. Pancreaticoduodenectomy – results and prospects (two-center study). Pirogov Russian Journal of Surgery. 2023; 5: 13–21. https://doi.org/10.17116/hirurgia202305113 (In Russian)
9. Claudio B., Giovanni M., Christos D., Micheal S., Mohammad A.H., Mustapha A., Peter A., Roland A., Horacio J.A., Marc G.B., Kevin C., Marco D.C., Massimo F., Laureano F., Carlos F.C., Abe F., Helmut F., Dirk J.G., Thilo H., Jakob I., Keith D.L., John P.N., Attila O., Richard S., Shailesh V.S., Tadahiro T., Kyoichi T., William T., Charles V., Christopher L.W., Charles J.Y., Roberto S., Marcus B. Corrigendum to "The 2016 update of the International Study Group (ISGPF) definition and grading of postoperative pancreatic fistula: eleven years after". Surgery. 2017; 161 (3): 584–591. Surgery. 2024; 176 (3): 988–989. https://doi.org/10.1016/j.surg.2024.05.043
10. Wente M.N., Veit J.A., Bassi C., Dervenis C., Sarr M.G., Abu Hilal M., Adham M., Allen P., Andersson R., Asbun H.J., Besselink M.G., Conlon K., Del Chiaro M., Falconi M., Fernandez-Cruz L., Fernandez-del Castillo C., Fingerhut A., Friess H., Gouma D.J., Hackert T., Izbicki J., Lillemoe K.D., Neoptolemos J.P., Olah A., Schulick R., Shrikhande S.V., Takada T., Takaori K., Traverso W.L., Vollmer C.M., Wolfgang C.L., Yeo C.J., Salvia R., Buchler M.W. Postpancreatectomy hemorrhage (PPH): an International Study Group of Pancreatic Surgery (ISGPS) definition. Surgery. 2007; 142 (1): 20–25. https://10.1016/j.surg.2007.02.001
11. Wente M.N., Bassi C., Dervenis C., Sarr M.G., Abu Hilal M., Adham M., Allen P., Andersson R., Asbun H.J., Besselink M.G., Conlon K., Del Chiaro M., Falconi M., Fernandez-Cruz L., Fingerhut A., Friess H., Gouma D.J., Hackert T., Izbicki J., Lillemoe K.D., Neoptolemos J.P., Olah A., Schulick R., Shrikhande S.V., Takada T., Takaori K., Traverso W.L., Vollmer C.M., Wolfgang C.L., Yeo C.J., Salvia R., Buchler M.W. Delayed gastric emptying (DGE) after pancreatic surgery: a suggested definition by the International Study Group of Pancreatic Surgery (ISGPS). Surgery. 2007; 142 (5): 761–768. https://doi.org/10.1016/j.surg.2007.05.005
12. Gorbunova V.A. Nejroendokrinnye opuholi. Obshchie principy diagnostiki i lecheniya [Neuroendocrine tumors. General guidelines for diagnosis and management.] Moscow: Kodeks, 2015. 455 p. (In Russian)
13. Lloyd R.V., Osamura R.Y., Kloppel G., Rosai J., editors. WHO classification of tumours of endocrine organs. Lyon: World Health Organization; 2017. ISBN 978-92-832-4493-6.
14. Patrone R., Mongardini F.M., Conzo A., Principi M., Mazzella V. Pancreatic neuroendocrine tumors: what is the best surgical option? J. Clin. Med. 2024; 13 (10): 3015. https://doi.org/10.3390/jcm13103015
15. Acher A.W., Hallet J. Advances in management of nonfunctional pancreas neuroendocrine tumors. Surg. Clin. North Am. 2024; 104 (5): 1095–1111. https://doi.org/10.1016/j.suc.2024.03.010
16. Kondrashin S.A., Egorov A.V., Pashkova I.L., Lotov A.N., Silina T.L., Orlov S.Yu., Askenderova E.O. Endoscopic ultrasonography in the preoperative topical diagnosis of organic hyperinsulinism. Ultrasound and Functional Diagnostics. 2006; 2: 21. (In Russian)
17. Okabayashi T., Shima Y., Sumiyoshi T., Kozuki A., Ito S., Ogawa Y., Kobayashi M., Hanazaki K. Diagnosis and treatment of insulinoma. World J. Gastroenterol. 2013; 19 (6): 829–837. https://doi.org/10.3748/wjg.v19.i6.829
18. Lee L., Ito T., Jensen R.T. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert. Rev. Anticancer Ther. 2018; 18 (9): 837–860. https://doi.org/10.1080/14737140.2018.1496822.
19. Hiramoto J.S., Feldstein V.A., Laberge D.M., Norton J.A. Intraoperative ultrasound and preoperative localization reveal all latent insulinomas; discussion 1025–1026. Arch. Surg. 2001; 136 (9): 1020–1025. https://doi.org/10.1001/archsurg.136.9.1020 20. Beane J.D., Borrebach J.D., Billderback A., Wells A., Miller F., Goodman Z. Small pancreatic neuroendocrine tumors: resect or enucleate? Am. J. Surg. 2021; 222 (1): 29–34. https://doi.org/10.1016/j.amjsurg.2020.12.013.
Supplementary files
Review
For citations:
Galkin V.N., Gorin D.S., Kriger A.G., Martirosyan T.A., Markov P.V., Goev A.A., Sokolov A.A., Galkin G.V., Panteleev V.I. Enucleation and resections short-term operative outcomes for well-differentiated pancreatic neuroendocrine tumors. Annaly khirurgicheskoy gepatologii = Annals of HPB Surgery. 2025;30(3):80-89. (In Russ.) https://doi.org/10.16931/1995-5464.2025-3-80-89