Pancreas Presented at the Academic Surgical Congress 2016| Volume 161, ISSUE 4, P968-976, April 2017

Evolution and impact of lymph node dissection during pancreaticoduodenectomy for pancreatic cancer

Published:November 16, 2016DOI:


      Insufficient examination of lymph nodes after pancreaticoduodenectomy can lead some pancreatic cancer patients with N1 disease to be misclassified as N0. We examined trends in lymph node dissection throughout time and investigated how these changes affect lymph node status and its prognostic value.


      The National Cancer Data Base was queried for patients with nonmetastatic pancreatic adenocarcinoma (2004–2013) who underwent classic pancreaticoduodenectomy with antrectomy. Logistic regression was performed for odds of node positivity. Kaplan-Meier curves and Cox proportional hazards models were used to assess the impact of lymph node status on overall survival for patients diagnosed during 2-year intervals from 2004–2012.


      Median number of examined lymph nodes was 10 (interquartile range 6–15) in 2004 vs 17 (interquartile range 12–24) in 2013. Number of lymph nodes examined was a significant predictor of N1 disease (P < .0001), with a plateau at 30 nodes. N1 disease increased from 64.4% to 68.0% (P < .0001). Survival for both N1 and N0 subgroups improved. In successive multivariate models, N0 versus N1 status was consistently protective for overall survival (P < .0001), but there was no change in the magnitude of its hazard ratio over time (overall hazard ratio 0.691; 95% confidence interval 0.660–0.723).


      Contemporary patients have an adequate number of nodes examined during standard pancreaticoduodenectomy. This, along with rising rates of N1 cancer detection and improved survival for both node-positive and node-negative patients, suggest more accurate classification of lymph node status. However, no increased benefit is achieved beyond 30 nodes. Overall, lymph node status remains a strong prognosticator for overall survival.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'


      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect


        • Tol J.A.
        • Gouma D.J.
        • Bassi C.
        • Dervenis C.
        • Montorsi M.
        • Adham M.
        • et al.
        Definition of a standard lymphadenectomy in surgery for pancreatic ductal adenocarcinoma: a consensus statement by the International Study Group on Pancreatic Surgery (ISGPS).
        Surgery. 2014; 156: 591-600
        • Bilimoria K.Y.
        • Stewart A.K.
        • Winchester D.P.
        • Ko C.Y.
        The National Cancer Data Base: a powerful initiative to improve cancer care in the United States.
        Ann Surg Oncol. 2008; 15: 683-690
      1. Pancreatic adenocarcinoma: NCCN clinical practice guidelines in oncology version 2.2015. National Comprehensive Cancer Network, Fort Washington (PA)2015 (Available from)
        • Marmor S.
        • Burke E.E.
        • Portschy P.R.
        • Virnig B.A.
        • Jensen E.H.
        • Tuttle T.M.
        Lymph node evaluation for treatment of adenocarcinoma of the pancreas.
        Surg Oncol. 2015; 24: 284-291
        • Burke E.E.
        • Marmor S.
        • Virnig B.A.
        • Tuttle T.M.
        • Jensen E.H.
        Lymph node evaluation for pancreatic adenocarcinoma and its value as a quality metric.
        J Gastrointest Surg. 2015; 19: 2162-2170
        • Bilimoria K.Y.
        • Talamonti M.S.
        • Wayne J.D.
        • Tomlinson J.S.
        • Stewart A.K.
        • Winchester D.P.
        • et al.
        Effect of hospital type and volume on lymph node evaluation for gastric and pancreatic cancer.
        Arch Surg. 2008; 143 (discussion 8): 671-678
        • Weber C.E.
        • Bock E.A.
        • Hurtuk M.G.
        • Abood G.J.
        • Pickleman J.
        • Shoup M.
        • et al.
        Clinical and pathologic features influencing survival in patients undergoing pancreaticoduodenectomy for pancreatic adenocarcinoma.
        J Gastrointest Surg. 2014; 18: 340-347
        • Pawlik T.M.
        • Gleisner A.L.
        • Cameron J.L.
        • Winter J.M.
        • Assumpcao L.
        • Lillemoe K.D.
        • et al.
        Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer.
        Surgery. 2007; 141: 610-618
        • Slidell M.B.
        • Chang D.C.
        • Cameron J.L.
        • Wolfgang C.
        • Herman J.M.
        • Schulick R.D.
        • et al.
        Impact of total lymph node count and lymph node ratio on staging and survival after pancreatectomy for pancreatic adenocarcinoma: a large, population-based analysis.
        Ann Surg Oncol. 2008; 15: 165-174
        • Govindarajan A.
        • Tan J.C.
        • Baxter N.N.
        • Coburn N.G.
        • Law C.H.
        Variations in surgical treatment and outcomes of patients with pancreatic cancer: a population-based study.
        Ann Surg Oncol. 2008; 15: 175-185
        • Adsay N.V.
        • Basturk O.
        • Altinel D.
        • Khanani F.
        • Coban I.
        • Weaver D.W.
        • et al.
        The number of lymph nodes identified in a simple pancreatoduodenectomy specimen: comparison of conventional vs orange-peeling approach in pathologic assessment.
        Mod Pathol. 2009; 22: 107-112
        • Basturk O.
        • Saka B.
        • Balci S.
        • Postlewait L.M.
        • Knight J.
        • Goodman M.
        • et al.
        Substaging of lymph node status in resected pancreatic ductal adenocarcinoma has strong prognostic correlations: proposal for a revised N classification for TNM staging.
        Ann Surg Oncol. 2015; 22: 1187-1195
        • Malleo G.
        • Maggino L.
        • Capelli P.
        • Gulino F.
        • Segattini S.
        • Scarpa A.
        • et al.
        Reappraisal of nodal staging and study of lymph node station involvement in pancreaticoduodenectomy with the standard international study group of pancreatic surgery definition of lymphadenectomy for cancer.
        J Am Coll Surg. 2015; 221: 367-379.e4
        • Yamada S.
        • Nakao A.
        • Fujii T.
        • Sugimoto H.
        • Kanazumi N.
        • Nomoto S.
        • et al.
        Pancreatic cancer with paraaortic lymph node metastasis: a contraindication for radical surgery?.
        Pancreas. 2009; 38: e13-e17
        • Vuarnesson H.
        • Lupinacci R.M.
        • Semoun O.
        • Svrcek M.
        • Julie C.
        • Balladur P.
        • et al.
        Number of examined lymph nodes and nodal status assessment in pancreaticoduodenectomy for pancreatic adenocarcinoma.
        Eur J Surg Oncol. 2013; 39: 1116-1121
        • Sormani M.P.
        The Will Rogers phenomenon: the effect of different diagnostic criteria.
        J Neurol Sci. 2009; 287: S46-S49
        • Huebner M.
        • Kendrick M.
        • Reid-Lombardo K.M.
        • Que F.
        • Therneau T.
        • Qin R.
        • et al.
        Number of lymph nodes evaluated: prognostic value in pancreatic adenocarcinoma.
        J Gastrointest Surg. 2012; 16: 920-926
        • Gleisner A.L.
        • Spolverato G.
        • Ejaz A.
        • Pawlik T.M.
        Time-related changes in the prognostic significance of the total number of examined lymph nodes in node-negative pancreatic head cancer.
        J Surg Oncol. 2014; 110: 858-863
        • Birkmeyer J.D.
        • Siewers A.E.
        • Marth N.J.
        • Goodman D.C.
        Regionalization of high-risk surgery and implications for patient travel times.
        JAMA. 2003; 290: 2703-2708
        • Gutierrez J.C.
        • Franceschi D.
        • Koniaris L.G.
        How many lymph nodes properly stage a periampullary malignancy?.
        J Gastrointest Surg. 2008; 12: 77-85
        • Hellan M.
        • Sun C.L.
        • Artinyan A.
        • Mojica-Manosa P.
        • Bhatia S.
        • Ellenhorn J.D.
        • et al.
        The impact of lymph node number on survival in patients with lymph node-negative pancreatic cancer.
        Pancreas. 2008; 37: 19-24
        • Tomlinson J.S.
        • Jain S.
        • Bentrem D.J.
        • Sekeris E.G.
        • Maggard M.A.
        • Hines O.J.
        • et al.
        Accuracy of staging node-negative pancreas cancer: a potential quality measure.
        Arch Surg. 2007; 142 (discussion 73–4): 767-773
        • Sierzega M.
        • Popiela T.
        • Kulig J.
        • Nowak K.
        The ratio of metastatic/resected lymph nodes is an independent prognostic factor in patients with node-positive pancreatic head cancer.
        Pancreas. 2006; 33: 240-245
        • Riediger H.
        • Keck T.
        • Wellner U.
        • zur Hausen A.
        • Adam U.
        • Hopt U.T.
        • et al.
        The lymph node ratio is the strongest prognostic factor after resection of pancreatic cancer.
        J Gastrointest Surg. 2009; 13: 1337-1344
        • House M.G.
        • Gonen M.
        • Jarnagin W.R.
        • D'Angelica M.
        • DeMatteo R.P.
        • Fong Y.
        • et al.
        Prognostic significance of pathologic nodal status in patients with resected pancreatic cancer.
        J Gastrointest Surg. 2007; 11: 1549-1555
        • Kang M.J.
        • Jang J.Y.
        • Chang Y.R.
        • Kwon W.
        • Jung W.
        • Kim S.W.
        Revisiting the concept of lymph node metastases of pancreatic head cancer: number of metastatic lymph nodes and lymph node ratio according to N stage.
        Ann Surg Oncol. 2014; 21: 1545-1551
        • Liu Z.
        • Luo G.
        • Guo M.
        • Jin K.
        • Xiao Z.
        • Liu L.
        • et al.
        Lymph node status predicts the benefit of adjuvant chemoradiotherapy for patients with resected pancreatic cancer.
        Pancreatology. 2015; 15: 253-258
        • de Geus S.W.
        • Bliss L.A.
        • Eskander M.F.
        • Ng S.C.
        • Vahrmeijer A.L.
        • Mahadevan A.
        • et al.
        A tale of two cities: reconsidering adjuvant radiation in pancreatic cancer care.
        J Gastrointest Surg. 2016; 20: 85-92
        • Pedrazzoli S.
        Extent of lymphadenectomy to associate with pancreaticoduodenectomy in patients with pancreatic head cancer for better tumor staging.
        Cancer Treatment Rev. 2015; 41: 577-587
        • Jeyarajah D.R.
        • Khithani A.
        • Siripurapu V.
        • Liu E.
        • Thomas A.
        • Saad A.J.
        Lymph node retrieval in pancreaticoduodenectomy specimens: does educating the pathologist matter?.
        HPB (Oxford). 2014; 16: 263-266