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Published in: BMC Surgery 1/2022

Open Access 01-12-2022 | Metastasis | Research

Value of lymphadenectomy in patients with surgically resected pancreatic neuroendocrine tumors

Authors: Zheng Zhang, Fei Wang, Zheng Li, Zeng Ye, Qifeng Zhuo, Wenyan Xu, Wensheng Liu, Mengqi Liu, Guixiong Fan, Yi Qin, Yue Zhang, Xuemin Chen, Xianjun Yu, Xiaowu Xu, Shunrong Ji

Published in: BMC Surgery | Issue 1/2022

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Abstract

Background

Although some factors that predict the prognosis in pancreatic neuroendocrine tumor (pNET) have been confirmed, the predictive value of lymph node metastasis (LNM) in the prognosis of pNETs remains conflicting and it is not clear whether regional lymphadenectomy should be performed in all grades of tumors.

Methods

We included pNET patients undergoing surgery in Shanghai pancreatic cancer institute (SHPCI). The risk factors for survival were investigated by the Kaplan–Meier method and Cox regression model. We evaluated the predictors of LNM using Logistic regression.

Results

For 206 patients in the SHPCI series, LNM was an independent prognostic factor for entire cohort suggested by multivariate Cox regression analysis. LNM (P = 0.002) predicted poorer overall survival (OS) in grade 2/3 cohort, but there is no significant association between LNM and OS in grade 1 cohort. Grade (P < 0.001) and size (P = 0.049) predicted LNM in entire cohort. Grade (P = 0.002) predicted LNM while regardless of size in grade 2/3 cohort.

Conclusions

Based on our own retrospective data obtained from a single center series, LNM seems to be associated with poorer outcome for patients with grade 2/3 and/or grade 1 > 4 cm tumors. On the other way, LNM was seems to be not associated with prognosis in patients with grade 1 tumors less than 4 cm. Moreover, tumor grade and tumor size seem to act as independent predictors of LNM. Thus, regional lymphadenectomy should be performed in grade 2/3 patients but was not mandatory in grade 1 tumors < 4 cm. It is reasonable to perform functional sparing surgery for grade 1 patients or propose a clinical-radiological monitoring.
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Literature
1.
go back to reference Kimura W, Kuroda A, Morioka Y. Clinical pathology of endocrine tumors of the pancreas. Analysis of autopsy cases. Dig Dis Sci. 1991;36(7):933–42.PubMedCrossRef Kimura W, Kuroda A, Morioka Y. Clinical pathology of endocrine tumors of the pancreas. Analysis of autopsy cases. Dig Dis Sci. 1991;36(7):933–42.PubMedCrossRef
2.
go back to reference Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26(18):3063–72.PubMedCrossRef Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, et al. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26(18):3063–72.PubMedCrossRef
3.
go back to reference Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, et al. ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology. 2016;103(2):153–71.PubMedCrossRef Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, et al. ENETS consensus guidelines update for the management of patients with functional pancreatic neuroendocrine tumors and non-functional pancreatic neuroendocrine tumors. Neuroendocrinology. 2016;103(2):153–71.PubMedCrossRef
4.
go back to reference Lee L, Ito T, Jensen RT. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert Rev Anticancer Ther. 2018;18(9):837–60.PubMedPubMedCentralCrossRef Lee L, Ito T, Jensen RT. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert Rev Anticancer Ther. 2018;18(9):837–60.PubMedPubMedCentralCrossRef
5.
go back to reference Partelli S, Gaujoux S, Boninsegna L, Cherif R, Crippa S, Couvelard A, et al. Pattern and clinical predictors of lymph node involvement in nonfunctioning pancreatic neuroendocrine tumors (NF-PanNETs). JAMA Surg. 2013;148(10):932–9.PubMedCrossRef Partelli S, Gaujoux S, Boninsegna L, Cherif R, Crippa S, Couvelard A, et al. Pattern and clinical predictors of lymph node involvement in nonfunctioning pancreatic neuroendocrine tumors (NF-PanNETs). JAMA Surg. 2013;148(10):932–9.PubMedCrossRef
6.
go back to reference Hochwald SN, Zee S, Conlon KC, Colleoni R, Louie O, Brennan MF, et al. Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol. 2002;20(11):2633–42.PubMedCrossRef Hochwald SN, Zee S, Conlon KC, Colleoni R, Louie O, Brennan MF, et al. Prognostic factors in pancreatic endocrine neoplasms: an analysis of 136 cases with a proposal for low-grade and intermediate-grade groups. J Clin Oncol. 2002;20(11):2633–42.PubMedCrossRef
7.
go back to reference Muscogiuri G, Altieri B, Albertelli M, Dotto A, Modica R, Barrea L, et al. Epidemiology of pancreatic neuroendocrine neoplasms: a gender perspective. Endocrine. 2020;69(2):441–50.PubMedCrossRef Muscogiuri G, Altieri B, Albertelli M, Dotto A, Modica R, Barrea L, et al. Epidemiology of pancreatic neuroendocrine neoplasms: a gender perspective. Endocrine. 2020;69(2):441–50.PubMedCrossRef
8.
go back to reference Feola T, Puliani G, Sesti F, Modica R, Centello R, Minotta R, et al. Risk factors for gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs): a three-centric case-control study. J Endocrinol Invest. 2022;45(4):849–57.PubMedCrossRef Feola T, Puliani G, Sesti F, Modica R, Centello R, Minotta R, et al. Risk factors for gastroenteropancreatic neuroendocrine neoplasms (GEP-NENs): a three-centric case-control study. J Endocrinol Invest. 2022;45(4):849–57.PubMedCrossRef
9.
go back to reference Dasari A, Shen C, Halperin D, Zhao B, Zhou S, Xu Y, et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–42.PubMedPubMedCentralCrossRef Dasari A, Shen C, Halperin D, Zhao B, Zhou S, Xu Y, et al. Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the United States. JAMA Oncol. 2017;3(10):1335–42.PubMedPubMedCentralCrossRef
10.
go back to reference Partelli S, Bartsch DK, Capdevila J, Chen J, Knigge U, Niederle B, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: surgery for small intestinal and pancreatic neuroendocrine tumours. Neuroendocrinology. 2017;105(3):255–65.PubMedCrossRef Partelli S, Bartsch DK, Capdevila J, Chen J, Knigge U, Niederle B, et al. ENETS consensus guidelines for standard of care in neuroendocrine tumours: surgery for small intestinal and pancreatic neuroendocrine tumours. Neuroendocrinology. 2017;105(3):255–65.PubMedCrossRef
11.
go back to reference Ausania F, Senra Del Rio P. Lymphadenectomy in pancreatic neuroendocrine neoplasms: why are we still debating? Pancreatology. 2018;18(8):855–61.PubMedCrossRef Ausania F, Senra Del Rio P. Lymphadenectomy in pancreatic neuroendocrine neoplasms: why are we still debating? Pancreatology. 2018;18(8):855–61.PubMedCrossRef
12.
go back to reference Bilimoria KY, Talamonti MS, Tomlinson JS, Stewart AK, Winchester DP, Ko CY, et al. Prognostic score predicting survival after resection of pancreatic neuroendocrine tumors: analysis of 3851 patients. Ann Surg. 2008;247(3):490–500.PubMedCrossRef Bilimoria KY, Talamonti MS, Tomlinson JS, Stewart AK, Winchester DP, Ko CY, et al. Prognostic score predicting survival after resection of pancreatic neuroendocrine tumors: analysis of 3851 patients. Ann Surg. 2008;247(3):490–500.PubMedCrossRef
13.
go back to reference Wong J, Fulp WJ, Strosberg JR, Kvols LK, Centeno BA, Hodul PJ. Predictors of lymph node metastases and impact on survival in resected pancreatic neuroendocrine tumors: a single-center experience. Am J Surg. 2014;208(5):775–80.PubMedCrossRef Wong J, Fulp WJ, Strosberg JR, Kvols LK, Centeno BA, Hodul PJ. Predictors of lymph node metastases and impact on survival in resected pancreatic neuroendocrine tumors: a single-center experience. Am J Surg. 2014;208(5):775–80.PubMedCrossRef
14.
go back to reference Hashim YM, Trinkaus KM, Linehan DC, Strasberg SS, Fields RC, Cao D, et al. Regional lymphadenectomy is indicated in the surgical treatment of pancreatic neuroendocrine tumors (PNETs). Ann Surg. 2014;259(2):197–203.PubMedCrossRef Hashim YM, Trinkaus KM, Linehan DC, Strasberg SS, Fields RC, Cao D, et al. Regional lymphadenectomy is indicated in the surgical treatment of pancreatic neuroendocrine tumors (PNETs). Ann Surg. 2014;259(2):197–203.PubMedCrossRef
15.
go back to reference Jutric Z, Grendar J, Hoen HM, Cho SW, Cassera MA, Newell PH, et al. Regional metastatic behavior of nonfunctional pancreatic neuroendocrine tumors: impact of lymph node positivity on survival. Pancreas. 2017;46(7):898–903.PubMedCrossRef Jutric Z, Grendar J, Hoen HM, Cho SW, Cassera MA, Newell PH, et al. Regional metastatic behavior of nonfunctional pancreatic neuroendocrine tumors: impact of lymph node positivity on survival. Pancreas. 2017;46(7):898–903.PubMedCrossRef
16.
go back to reference Partelli S, Javed AA, Andreasi V, He J, Muffatti F, Weiss MJ, et al. The number of positive nodes accurately predicts recurrence after pancreaticoduodenectomy for nonfunctioning neuroendocrine neoplasms. Eur J Surg Oncol. 2018;44(6):778–83.PubMedCrossRef Partelli S, Javed AA, Andreasi V, He J, Muffatti F, Weiss MJ, et al. The number of positive nodes accurately predicts recurrence after pancreaticoduodenectomy for nonfunctioning neuroendocrine neoplasms. Eur J Surg Oncol. 2018;44(6):778–83.PubMedCrossRef
17.
go back to reference Capretti G, Nappo G, Smiroldo V, Cereda M, Branciforte B, Spaggiari P, et al. The number of metastatic lymph nodes is a useful predictive factor for recurrence after surgery for nonmetastatic nonfunctional neuroendocrine neoplasm of the pancreas. Gastroenterol Res Pract. 2019;2019:6856329.PubMedPubMedCentralCrossRef Capretti G, Nappo G, Smiroldo V, Cereda M, Branciforte B, Spaggiari P, et al. The number of metastatic lymph nodes is a useful predictive factor for recurrence after surgery for nonmetastatic nonfunctional neuroendocrine neoplasm of the pancreas. Gastroenterol Res Pract. 2019;2019:6856329.PubMedPubMedCentralCrossRef
18.
go back to reference Zatelli MC, Guadagno E, Messina E, Lo Calzo F, Faggiano A, Colao A. Open issues on G3 neuroendocrine neoplasms: back to the future. Endocr Relat Cancer. 2018;25(6):R375–84.PubMedCrossRef Zatelli MC, Guadagno E, Messina E, Lo Calzo F, Faggiano A, Colao A. Open issues on G3 neuroendocrine neoplasms: back to the future. Endocr Relat Cancer. 2018;25(6):R375–84.PubMedCrossRef
19.
go back to reference Soczomski P, Jurecka-Lubieniecka B, Krzywon A, Cortez AJ, Zgliczynski S, Rogozik N, et al. A direct comparison of patients with hereditary and sporadic pancreatic neuroendocrine tumors: evaluation of clinical course, prognostic factors and genotype-phenotype correlations. Front Endocrinol (Lausanne). 2021;12: 681013.CrossRef Soczomski P, Jurecka-Lubieniecka B, Krzywon A, Cortez AJ, Zgliczynski S, Rogozik N, et al. A direct comparison of patients with hereditary and sporadic pancreatic neuroendocrine tumors: evaluation of clinical course, prognostic factors and genotype-phenotype correlations. Front Endocrinol (Lausanne). 2021;12: 681013.CrossRef
20.
go back to reference Oberg KE, Reubi JC, Kwekkeboom DJ, Krenning EP. Role of somatostatins in gastroenteropancreatic neuroendocrine tumor development and therapy. Gastroenterology. 2010;139(3):742–53.PubMedCrossRef Oberg KE, Reubi JC, Kwekkeboom DJ, Krenning EP. Role of somatostatins in gastroenteropancreatic neuroendocrine tumor development and therapy. Gastroenterology. 2010;139(3):742–53.PubMedCrossRef
21.
go back to reference Ito T, Igarashi H, Jensen RT. Therapy of metastatic pancreatic neuroendocrine tumors (pNETs): recent insights and advances. J Gastroenterol. 2012;47(9):941–60.PubMedPubMedCentralCrossRef Ito T, Igarashi H, Jensen RT. Therapy of metastatic pancreatic neuroendocrine tumors (pNETs): recent insights and advances. J Gastroenterol. 2012;47(9):941–60.PubMedPubMedCentralCrossRef
22.
go back to reference Valle JW, Eatock M, Clueit B, Gabriel Z, Ferdinand R, Mitchell S. A systematic review of non-surgical treatments for pancreatic neuroendocrine tumours. Cancer Treat Rev. 2014;40(3):376–89.PubMedCrossRef Valle JW, Eatock M, Clueit B, Gabriel Z, Ferdinand R, Mitchell S. A systematic review of non-surgical treatments for pancreatic neuroendocrine tumours. Cancer Treat Rev. 2014;40(3):376–89.PubMedCrossRef
23.
go back to reference Drymousis P, Raptis DA, Spalding D, Fernandez-Cruz L, Menon D, Breitenstein S, et al. Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford). 2014;16(5):397–406.CrossRef Drymousis P, Raptis DA, Spalding D, Fernandez-Cruz L, Menon D, Breitenstein S, et al. Laparoscopic versus open pancreas resection for pancreatic neuroendocrine tumours: a systematic review and meta-analysis. HPB (Oxford). 2014;16(5):397–406.CrossRef
24.
go back to reference Kurita Y, Hara K, Kuwahara T, Mizuno N, Okuno N, Haba S, et al. Comparison of prognosis between observation and surgical resection groups with small sporadic non-functional pancreatic neuroendocrine neoplasms without distant metastasis. J Gastroenterol. 2020;55(5):543–52.PubMedCrossRef Kurita Y, Hara K, Kuwahara T, Mizuno N, Okuno N, Haba S, et al. Comparison of prognosis between observation and surgical resection groups with small sporadic non-functional pancreatic neuroendocrine neoplasms without distant metastasis. J Gastroenterol. 2020;55(5):543–52.PubMedCrossRef
25.
go back to reference Barenboim A, Lahat G, Nachmany I, Nakache R, Goykhman Y, Geva R, et al. Resection versus observation of small asymptomatic nonfunctioning pancreatic neuroendocrine tumors. J Gastrointest Surg. 2020;24(6):1366–74.PubMedCrossRef Barenboim A, Lahat G, Nachmany I, Nakache R, Goykhman Y, Geva R, et al. Resection versus observation of small asymptomatic nonfunctioning pancreatic neuroendocrine tumors. J Gastrointest Surg. 2020;24(6):1366–74.PubMedCrossRef
26.
go back to reference Shah MH, Goldner WS, Halfdanarson TR, Bergsland E, Berlin JD, Halperin D, et al. NCCN guidelines insights: neuroendocrine and Adrenal Tumors, Version 2.2018. J Natl Compr Canc Netw. 2018;16(6):693–702.PubMedCrossRef Shah MH, Goldner WS, Halfdanarson TR, Bergsland E, Berlin JD, Halperin D, et al. NCCN guidelines insights: neuroendocrine and Adrenal Tumors, Version 2.2018. J Natl Compr Canc Netw. 2018;16(6):693–702.PubMedCrossRef
27.
go back to reference Mao R, Zhao H, Li K, Luo S, Turner M, Cai JQ, et al. Outcomes of lymph node dissection for non-metastatic pancreatic neuroendocrine tumors: a propensity score-weighted analysis of the national cancer database. Ann Surg Oncol. 2019;26(9):2722–9.PubMedPubMedCentralCrossRef Mao R, Zhao H, Li K, Luo S, Turner M, Cai JQ, et al. Outcomes of lymph node dissection for non-metastatic pancreatic neuroendocrine tumors: a propensity score-weighted analysis of the national cancer database. Ann Surg Oncol. 2019;26(9):2722–9.PubMedPubMedCentralCrossRef
28.
go back to reference Postlewait LM, Ethun CG, Baptiste GG, Le N, McInnis MR, Cardona K, et al. Pancreatic neuroendocrine tumors: preoperative factors that predict lymph node metastases to guide operative strategy. J Surg Oncol. 2016;114(4):440–5.PubMedCrossRef Postlewait LM, Ethun CG, Baptiste GG, Le N, McInnis MR, Cardona K, et al. Pancreatic neuroendocrine tumors: preoperative factors that predict lymph node metastases to guide operative strategy. J Surg Oncol. 2016;114(4):440–5.PubMedCrossRef
29.
go back to reference Parekh JR, Wang SC, Bergsland EK, Venook AP, Warren RS, Kim GE, et al. Lymph node sampling rates and predictors of nodal metastasis in pancreatic neuroendocrine tumor resections: the UCSF experience with 149 patients. Pancreas. 2012;41(6):840–4.PubMedCrossRef Parekh JR, Wang SC, Bergsland EK, Venook AP, Warren RS, Kim GE, et al. Lymph node sampling rates and predictors of nodal metastasis in pancreatic neuroendocrine tumor resections: the UCSF experience with 149 patients. Pancreas. 2012;41(6):840–4.PubMedCrossRef
30.
go back to reference Brunner SM, Weber F, Werner JM, Agha A, Farkas SA, Schlitt HJ, et al. Neuroendocrine tumors of the pancreas: a retrospective single-center analysis using the ENETS TNM-classification and immunohistochemical markers for risk stratification. BMC Surg. 2015;15:49.PubMedPubMedCentralCrossRef Brunner SM, Weber F, Werner JM, Agha A, Farkas SA, Schlitt HJ, et al. Neuroendocrine tumors of the pancreas: a retrospective single-center analysis using the ENETS TNM-classification and immunohistochemical markers for risk stratification. BMC Surg. 2015;15:49.PubMedPubMedCentralCrossRef
31.
go back to reference Fischer L, Bergmann F, Schimmack S, Hinz U, Prieß S, Müller-Stich BP, et al. Outcome of surgery for pancreatic neuroendocrine neoplasms. Br J Surg. 2014;101(11):1405–12.PubMedCrossRef Fischer L, Bergmann F, Schimmack S, Hinz U, Prieß S, Müller-Stich BP, et al. Outcome of surgery for pancreatic neuroendocrine neoplasms. Br J Surg. 2014;101(11):1405–12.PubMedCrossRef
32.
go back to reference Ballian N, Loeffler AG, Rajamanickam V, Norstedt PA, Weber SM, Cho CS. A simplified prognostic system for resected pancreatic neuroendocrine neoplasms. HPB (Oxford). 2009;11(5):422–8.CrossRef Ballian N, Loeffler AG, Rajamanickam V, Norstedt PA, Weber SM, Cho CS. A simplified prognostic system for resected pancreatic neuroendocrine neoplasms. HPB (Oxford). 2009;11(5):422–8.CrossRef
33.
go back to reference Gratian L, Pura J, Dinan M, Roman S, Reed S, Sosa JA. Impact of extent of surgery on survival in patients with small nonfunctional pancreatic neuroendocrine tumors in the United States. Ann Surg Oncol. 2014;21(11):3515–21.PubMedPubMedCentralCrossRef Gratian L, Pura J, Dinan M, Roman S, Reed S, Sosa JA. Impact of extent of surgery on survival in patients with small nonfunctional pancreatic neuroendocrine tumors in the United States. Ann Surg Oncol. 2014;21(11):3515–21.PubMedPubMedCentralCrossRef
34.
go back to reference Kazanjian KK, Reber HA, Hines OJ. Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg. 2006;141(8):765–9.PubMedCrossRef Kazanjian KK, Reber HA, Hines OJ. Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg. 2006;141(8):765–9.PubMedCrossRef
35.
go back to reference Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The Eighth edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93–9.PubMedCrossRef Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The Eighth edition AJCC Cancer Staging Manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93–9.PubMedCrossRef
36.
go back to reference Ito H, Abramson M, Ito K, Swanson E, Cho N, Ruan DT, et al. Surgery and staging of pancreatic neuroendocrine tumors: a 14-year experience. J Gastrointest Surg. 2010;14(5):891–8.PubMedCrossRef Ito H, Abramson M, Ito K, Swanson E, Cho N, Ruan DT, et al. Surgery and staging of pancreatic neuroendocrine tumors: a 14-year experience. J Gastrointest Surg. 2010;14(5):891–8.PubMedCrossRef
37.
go back to reference Lopez-Aguiar AG, Zaidi MY, Beal EW, Dillhoff M, Cannon JGD, Poultsides GA, et al. Defining the role of lymphadenectomy for pancreatic neuroendocrine tumors: an eight-institution study of 695 patients from the US neuroendocrine tumor study group. Ann Surg Oncol. 2019;26(8):2517–24.PubMedCrossRef Lopez-Aguiar AG, Zaidi MY, Beal EW, Dillhoff M, Cannon JGD, Poultsides GA, et al. Defining the role of lymphadenectomy for pancreatic neuroendocrine tumors: an eight-institution study of 695 patients from the US neuroendocrine tumor study group. Ann Surg Oncol. 2019;26(8):2517–24.PubMedCrossRef
38.
go back to reference Haynes AB, Deshpande V, Ingkakul T, Vagefi PA, Szymonifka J, Thayer SP, et al. Implications of incidentally discovered, nonfunctioning pancreatic endocrine tumors: short-term and long-term patient outcomes. Arch Surg. 2011;146(5):534–8.PubMedPubMedCentralCrossRef Haynes AB, Deshpande V, Ingkakul T, Vagefi PA, Szymonifka J, Thayer SP, et al. Implications of incidentally discovered, nonfunctioning pancreatic endocrine tumors: short-term and long-term patient outcomes. Arch Surg. 2011;146(5):534–8.PubMedPubMedCentralCrossRef
39.
go back to reference Piani C, Franchi GM, Cappelletti C, Scavini M, Albarello L, Zerbi A, et al. Cytological Ki-67 in pancreatic endocrine tumours: an opportunity for pre-operative grading. Endocr Relat Cancer. 2008;15(1):175–81.PubMedCrossRef Piani C, Franchi GM, Cappelletti C, Scavini M, Albarello L, Zerbi A, et al. Cytological Ki-67 in pancreatic endocrine tumours: an opportunity for pre-operative grading. Endocr Relat Cancer. 2008;15(1):175–81.PubMedCrossRef
40.
go back to reference Hasegawa T, Yamao K, Hijioka S, Bhatia V, Mizuno N, Hara K, et al. Evaluation of Ki-67 index in EUS-FNA specimens for the assessment of malignancy risk in pancreatic neuroendocrine tumors. Endoscopy. 2014;46(1):32–8.PubMed Hasegawa T, Yamao K, Hijioka S, Bhatia V, Mizuno N, Hara K, et al. Evaluation of Ki-67 index in EUS-FNA specimens for the assessment of malignancy risk in pancreatic neuroendocrine tumors. Endoscopy. 2014;46(1):32–8.PubMed
41.
go back to reference Weynand B, Borbath I, Bernard V, Sempoux C, Gigot JF, Hubert C, et al. Pancreatic neuroendocrine tumour grading on endoscopic ultrasound-guided fine needle aspiration: high reproducibility and inter-observer agreement of the Ki-67 labelling index. Cytopathology. 2014;25(6):389–95.PubMed Weynand B, Borbath I, Bernard V, Sempoux C, Gigot JF, Hubert C, et al. Pancreatic neuroendocrine tumour grading on endoscopic ultrasound-guided fine needle aspiration: high reproducibility and inter-observer agreement of the Ki-67 labelling index. Cytopathology. 2014;25(6):389–95.PubMed
Metadata
Title
Value of lymphadenectomy in patients with surgically resected pancreatic neuroendocrine tumors
Authors
Zheng Zhang
Fei Wang
Zheng Li
Zeng Ye
Qifeng Zhuo
Wenyan Xu
Wensheng Liu
Mengqi Liu
Guixiong Fan
Yi Qin
Yue Zhang
Xuemin Chen
Xianjun Yu
Xiaowu Xu
Shunrong Ji
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2022
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/s12893-022-01595-y

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