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Published in: World Journal of Surgical Oncology 1/2016

Open Access 01-12-2016 | Research

Number of evaluated lymph nodes and positive lymph nodes, lymph node ratio, and log odds evaluation in early-stage pancreatic ductal adenocarcinoma: numerology or valid indicators of patient outcome?

Authors: G. Lahat, N. Lubezky, F. Gerstenhaber, E. Nizri, M. Gysi, M. Rozenek, Y. Goichman, I. Nachmany, R. Nakache, I. Wolf, J. M. Klausner

Published in: World Journal of Surgical Oncology | Issue 1/2016

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Abstract

Background

We evaluated the prognostic significance and universal validity of the total number of evaluated lymph nodes (ELN), number of positive lymph nodes (PLN), lymph node ratio (LNR), and log odds of positive lymph nodes (LODDS) in a relatively large and homogenous cohort of surgically treated pancreatic ductal adenocarcinoma (PDAC) patients.

Methods

Prospectively accrued data were retrospectively analyzed for 282 PDAC patients who had pancreaticoduodenectomy (PD) at our institution. Long-term survival was analyzed according to the ELN, PLN, LNR, and LODDS.

Results

Of these patients, 168 patients (59.5 %) had LN metastasis (N1). Mean ELN and PLN were 13.5 and 1.6, respectively. LN positivity correlated with a greater number of evaluated lymph nodes; positive lymph nodes were identified in 61.4 % of the patients with ELN ≥ 13 compared with 44.9 % of the patients with ELN < 13 (p = 0.014). Median overall survival (OS) and 5-year OS rate were higher in N0 than in N1 patients, 22.4 vs. 18.7 months and 35 vs. 11 %, respectively (p = 0.008). Mean LNR was 0.12; 91 patients (54.1 %) had LNR < 0.3. Among the N1 patients, median OS was comparable in those with LNR ≥ 0.3 vs. LNR < 0.3 (16.7 vs. 14.1 months, p = 0.950). Neither LODDS nor various ELN and PLN cutoff values provided more discriminative information within the group of N1 patients.

Conclusions

Our data confirms that lymph node positivity strongly reflects PDAC biology and thus patient outcome. While a higher number of evaluated lymph nodes may provide a more accurate nodal staging, it does not have any prognostic value among N1 patients. Similarly, PLN, LNR, and LODDS had limited prognostic relevance.
Literature
2.
go back to reference Hsu CC, Herman JM, Corsini MM, et al. Adjuvant chemoradiation for pancreatic adenocarcinoma: the Johns Hopkins Hospital-Mayo Clinic collaborative study. Ann Surg Oncol. 2010;17:981–90.CrossRefPubMedPubMedCentral Hsu CC, Herman JM, Corsini MM, et al. Adjuvant chemoradiation for pancreatic adenocarcinoma: the Johns Hopkins Hospital-Mayo Clinic collaborative study. Ann Surg Oncol. 2010;17:981–90.CrossRefPubMedPubMedCentral
3.
go back to reference Sinn M, Striefler JK, Sinn BV, et al. Does long-term survival in patients with pancreatic cancer really exist? Results from the CONKO-001 study. J Surg Oncol. 2013;108:398–402.CrossRefPubMed Sinn M, Striefler JK, Sinn BV, et al. Does long-term survival in patients with pancreatic cancer really exist? Results from the CONKO-001 study. J Surg Oncol. 2013;108:398–402.CrossRefPubMed
4.
go back to reference Buc E, Couvelard A, Kwiatkowski F, et al. Adenocarcinoma of the pancreas: does prognosis depend on mode of lymph node invasion? Eur J Surg Oncol. 2014;40:1578–85.CrossRefPubMed Buc E, Couvelard A, Kwiatkowski F, et al. Adenocarcinoma of the pancreas: does prognosis depend on mode of lymph node invasion? Eur J Surg Oncol. 2014;40:1578–85.CrossRefPubMed
5.
go back to reference Dusch N, Weiss C, Strobel P, et al. Factors predicting long-term survival following pancreatic resection for ductal adenocarcinoma of the pancreas: 40 years of experience. J Gastrointest Surg. 2014;18:674–81.CrossRefPubMed Dusch N, Weiss C, Strobel P, et al. Factors predicting long-term survival following pancreatic resection for ductal adenocarcinoma of the pancreas: 40 years of experience. J Gastrointest Surg. 2014;18:674–81.CrossRefPubMed
6.
go back to reference Valsangkar NP, Bush DM, Michaelson JS, et al. N0/N1, PNL, or LNR? The effect of lymph node number on accurate survival prediction in pancreatic ductal adenocarcinoma. J Gastrointest Surg. 2013;17:257–66.CrossRefPubMed Valsangkar NP, Bush DM, Michaelson JS, et al. N0/N1, PNL, or LNR? The effect of lymph node number on accurate survival prediction in pancreatic ductal adenocarcinoma. J Gastrointest Surg. 2013;17:257–66.CrossRefPubMed
7.
go back to reference Vuarnesson H, Lupinacci RM, Semoun O, et al. Number of examined lymph nodes and nodal status assessment in pancreaticoduodenectomy for pancreatic adenocarcinoma. Eur J Surg Oncol. 2013;39:1116–21.CrossRefPubMed Vuarnesson H, Lupinacci RM, Semoun O, et al. Number of examined lymph nodes and nodal status assessment in pancreaticoduodenectomy for pancreatic adenocarcinoma. Eur J Surg Oncol. 2013;39:1116–21.CrossRefPubMed
8.
go back to reference Benassai G, Mastrorilli M, Quarto G, et al. Factors influencing survival after resection for ductal adenocarcinoma of the head of the pancreas. J Surg Oncol. 2000;73:212–8.CrossRefPubMed Benassai G, Mastrorilli M, Quarto G, et al. Factors influencing survival after resection for ductal adenocarcinoma of the head of the pancreas. J Surg Oncol. 2000;73:212–8.CrossRefPubMed
9.
go back to reference Kedra B, Popiela T, Sierzega M, Precht A. Prognostic factors of long-term survival after resective procedures for pancreatic cancer. Hepatogastroenterology. 2001;48:1762–6.PubMed Kedra B, Popiela T, Sierzega M, Precht A. Prognostic factors of long-term survival after resective procedures for pancreatic cancer. Hepatogastroenterology. 2001;48:1762–6.PubMed
10.
go back to reference Lim JE, Chien MW, Earle CC. Prognostic factors following curative resection for pancreatic adenocarcinoma: a population-based, linked database analysis of 396 patients. Ann Surg. 2003;237:74–85.CrossRefPubMedPubMedCentral Lim JE, Chien MW, Earle CC. Prognostic factors following curative resection for pancreatic adenocarcinoma: a population-based, linked database analysis of 396 patients. Ann Surg. 2003;237:74–85.CrossRefPubMedPubMedCentral
11.
go back to reference Raut CP, Tseng JF, Sun CC, et al. Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg. 2007;246:52–60.CrossRefPubMedPubMedCentral Raut CP, Tseng JF, Sun CC, et al. Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg. 2007;246:52–60.CrossRefPubMedPubMedCentral
12.
go back to reference Ashfaq A, Pockaj BA, Gray RJ, et al. Nodal counts and lymph node ratio impact survival after distal pancreatectomy for pancreatic adenocarcinoma. J Gastrointest Surg. 2014;18:1929–35.CrossRefPubMed Ashfaq A, Pockaj BA, Gray RJ, et al. Nodal counts and lymph node ratio impact survival after distal pancreatectomy for pancreatic adenocarcinoma. J Gastrointest Surg. 2014;18:1929–35.CrossRefPubMed
13.
go back to reference Liu ZQ, Xiao ZW, Luo GP, et al. Effect of the number of positive lymph nodes and lymph node ratio on prognosis of patients after resection of pancreatic adenocarcinoma. Hepatobiliary Pancreat Dis Int. 2014;13:634–41.CrossRefPubMed Liu ZQ, Xiao ZW, Luo GP, et al. Effect of the number of positive lymph nodes and lymph node ratio on prognosis of patients after resection of pancreatic adenocarcinoma. Hepatobiliary Pancreat Dis Int. 2014;13:634–41.CrossRefPubMed
14.
go back to reference Gleisner AL, Spolverato G, Ejaz A, Pawlik TM. 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;110:858–63.CrossRefPubMed Gleisner AL, Spolverato G, Ejaz A, Pawlik TM. 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;110:858–63.CrossRefPubMed
15.
go back to reference Kang MJ, Jang JY, Chang YR, et al. 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;21:1545–51.CrossRefPubMed Kang MJ, Jang JY, Chang YR, et al. 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;21:1545–51.CrossRefPubMed
16.
go back to reference Showalter TN, Winter KA, Berger AC, et al. The influence of total nodes examined, number of positive nodes, and lymph node ratio on survival after surgical resection and adjuvant chemoradiation for pancreatic cancer: a secondary analysis of RTOG 9704. Int J Radiat Oncol Biol Phys. 2011;81:1328–35.CrossRefPubMed Showalter TN, Winter KA, Berger AC, et al. The influence of total nodes examined, number of positive nodes, and lymph node ratio on survival after surgical resection and adjuvant chemoradiation for pancreatic cancer: a secondary analysis of RTOG 9704. Int J Radiat Oncol Biol Phys. 2011;81:1328–35.CrossRefPubMed
17.
go back to reference Massucco P, Ribero D, Sgotto E, et al. Prognostic significance of lymph node metastases in pancreatic head cancer treated with extended lymphadenectomy: not just a matter of numbers. Ann Surg Oncol. 2009;16:3323–32.CrossRefPubMed Massucco P, Ribero D, Sgotto E, et al. Prognostic significance of lymph node metastases in pancreatic head cancer treated with extended lymphadenectomy: not just a matter of numbers. Ann Surg Oncol. 2009;16:3323–32.CrossRefPubMed
18.
go back to reference Strobel O, Hinz U, Gluth A, et al. Pancreatic adenocarcinoma: number of positive nodes allows to distinguish several N categories. Ann Surg. 2015;261:961–9.CrossRefPubMed Strobel O, Hinz U, Gluth A, et al. Pancreatic adenocarcinoma: number of positive nodes allows to distinguish several N categories. Ann Surg. 2015;261:961–9.CrossRefPubMed
19.
go back to reference La Torre M, Nigri G, Petrucciani N, et al. Prognostic assessment of different lymph node staging methods for pancreatic cancer with R0 resection: pN staging, lymph node ratio, log odds of positive lymph nodes. Pancreatology. 2014;14:289–94.CrossRefPubMed La Torre M, Nigri G, Petrucciani N, et al. Prognostic assessment of different lymph node staging methods for pancreatic cancer with R0 resection: pN staging, lymph node ratio, log odds of positive lymph nodes. Pancreatology. 2014;14:289–94.CrossRefPubMed
20.
go back to reference Tol JA, Brosens LA, van Dieren S, et al. Impact of lymph node ratio on survival in patients with pancreatic and periampullary cancer. Br J Surg. 2015;102:237–45.CrossRefPubMed Tol JA, Brosens LA, van Dieren S, et al. Impact of lymph node ratio on survival in patients with pancreatic and periampullary cancer. Br J Surg. 2015;102:237–45.CrossRefPubMed
21.
go back to reference Yamamoto Y, Ikoma H, Morimura R, et al. The clinical impact of the lymph node ratio as a prognostic factor after resection of pancreatic cancer. Anticancer Res. 2014;34:2389–94.PubMed Yamamoto Y, Ikoma H, Morimura R, et al. The clinical impact of the lymph node ratio as a prognostic factor after resection of pancreatic cancer. Anticancer Res. 2014;34:2389–94.PubMed
22.
go back to reference Sobin LHGM, Wittekind C. TNM classification of malignant tumors. 7th ed. Hoboken: Wiley; 2009. Sobin LHGM, Wittekind C. TNM classification of malignant tumors. 7th ed. Hoboken: Wiley; 2009.
23.
go back to reference Aurello P, Petrucciani N, Nigri GR, et al. Log odds of positive lymph nodes (LODDS): what are their role in the prognostic assessment of gastric adenocarcinoma? J Gastrointest Surg. 2014;18:1254–60.CrossRefPubMed Aurello P, Petrucciani N, Nigri GR, et al. Log odds of positive lymph nodes (LODDS): what are their role in the prognostic assessment of gastric adenocarcinoma? J Gastrointest Surg. 2014;18:1254–60.CrossRefPubMed
24.
go back to reference Sun Z, Xu Y, de Li M, et al. Log odds of positive lymph nodes: a novel prognostic indicator superior to the number-based and the ratio-based N category for gastric cancer patients with R0 resection. Cancer. 2010;116:2571–80.CrossRefPubMed Sun Z, Xu Y, de Li M, et al. Log odds of positive lymph nodes: a novel prognostic indicator superior to the number-based and the ratio-based N category for gastric cancer patients with R0 resection. Cancer. 2010;116:2571–80.CrossRefPubMed
25.
go back to reference Nagakawa T, Nagamori M, Futakami F, et al. Results of extensive surgery for pancreatic carcinoma. Cancer. 1996;77:640–5.CrossRefPubMed Nagakawa T, Nagamori M, Futakami F, et al. Results of extensive surgery for pancreatic carcinoma. Cancer. 1996;77:640–5.CrossRefPubMed
26.
go back to reference Ishikawa O, Ohhigashi H, Sasaki Y, et al. Practical usefulness of lymphatic and connective tissue clearance for the carcinoma of the pancreas head. Ann Surg. 1988;208:215–20.CrossRefPubMedPubMedCentral Ishikawa O, Ohhigashi H, Sasaki Y, et al. Practical usefulness of lymphatic and connective tissue clearance for the carcinoma of the pancreas head. Ann Surg. 1988;208:215–20.CrossRefPubMedPubMedCentral
27.
go back to reference Manabe T, Ohshio G, Baba N, et al. Radical pancreatectomy for ductal cell carcinoma of the head of the pancreas. Cancer. 1989;64:1132–7.CrossRefPubMed Manabe T, Ohshio G, Baba N, et al. Radical pancreatectomy for ductal cell carcinoma of the head of the pancreas. Cancer. 1989;64:1132–7.CrossRefPubMed
28.
go back to reference Pedrazzoli S, DiCarlo V, Dionigi R, et al. Standard versus extended lymphadenectomy associated with pancreatoduodenectomy in the surgical treatment of adenocarcinoma of the head of the pancreas: a multicenter, prospective, randomized study. Lymphadenectomy Study Group. Ann Surg. 1998;228:508–17.CrossRefPubMedPubMedCentral Pedrazzoli S, DiCarlo V, Dionigi R, et al. Standard versus extended lymphadenectomy associated with pancreatoduodenectomy in the surgical treatment of adenocarcinoma of the head of the pancreas: a multicenter, prospective, randomized study. Lymphadenectomy Study Group. Ann Surg. 1998;228:508–17.CrossRefPubMedPubMedCentral
29.
go back to reference Farnell MB, Pearson RK, Sarr MG, et al. A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery. 2005;138:618–28. discussion 628-630.CrossRefPubMed Farnell MB, Pearson RK, Sarr MG, et al. A prospective randomized trial comparing standard pancreatoduodenectomy with pancreatoduodenectomy with extended lymphadenectomy in resectable pancreatic head adenocarcinoma. Surgery. 2005;138:618–28. discussion 628-630.CrossRefPubMed
30.
go back to reference Nimura Y, Nagino M, Takao S, et al. Standard versus extended lymphadenectomy in radical pancreatoduodenectomy for ductal adenocarcinoma of the head of the pancreas: long-term results of a Japanese multicenter randomized controlled trial. J Hepatobiliary Pancreat Sci. 2012;19:230–41.CrossRefPubMed Nimura Y, Nagino M, Takao S, et al. Standard versus extended lymphadenectomy in radical pancreatoduodenectomy for ductal adenocarcinoma of the head of the pancreas: long-term results of a Japanese multicenter randomized controlled trial. J Hepatobiliary Pancreat Sci. 2012;19:230–41.CrossRefPubMed
31.
go back to reference Yeo CJ, Cameron JL, Sohn TA, et al. Pancreaticoduodenectomy with or without extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma: comparison of morbidity and mortality and short-term outcome. Ann Surg. 1999;229:613–22. discussion 622-614.CrossRefPubMedPubMedCentral Yeo CJ, Cameron JL, Sohn TA, et al. Pancreaticoduodenectomy with or without extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma: comparison of morbidity and mortality and short-term outcome. Ann Surg. 1999;229:613–22. discussion 622-614.CrossRefPubMedPubMedCentral
32.
go back to reference Petrelli F, Borgonovo K, Barni S. The emerging issue of ratio of metastatic to resected lymph nodes in gastrointestinal cancers: an overview of literature. Eur J Surg Oncol. 2011;37:836–47.CrossRefPubMed Petrelli F, Borgonovo K, Barni S. The emerging issue of ratio of metastatic to resected lymph nodes in gastrointestinal cancers: an overview of literature. Eur J Surg Oncol. 2011;37:836–47.CrossRefPubMed
33.
go back to reference Spolverato G, Ejaz A, Kim Y, et al. Prognostic performance of different lymph node staging systems after curative intent resection for gastric adenocarcinoma. Ann Surg. 2015;262:991–8.CrossRefPubMed Spolverato G, Ejaz A, Kim Y, et al. Prognostic performance of different lymph node staging systems after curative intent resection for gastric adenocarcinoma. Ann Surg. 2015;262:991–8.CrossRefPubMed
34.
go back to reference La Torre M, Cavallini M, Ramacciato G, et al. Role of the lymph node ratio in pancreatic ductal adenocarcinoma. Impact on patient stratification and prognosis. J Surg Oncol. 2011;104:629–33.CrossRefPubMed La Torre M, Cavallini M, Ramacciato G, et al. Role of the lymph node ratio in pancreatic ductal adenocarcinoma. Impact on patient stratification and prognosis. J Surg Oncol. 2011;104:629–33.CrossRefPubMed
35.
go back to reference Partelli S, Fernandez-Del Castillo C, Bassi C, et al. Invasive intraductal papillary mucinous carcinomas of the pancreas: predictors of survival and the role of lymph node ratio. Ann Surg. 2010;251:477–82.CrossRefPubMedPubMedCentral Partelli S, Fernandez-Del Castillo C, Bassi C, et al. Invasive intraductal papillary mucinous carcinomas of the pancreas: predictors of survival and the role of lymph node ratio. Ann Surg. 2010;251:477–82.CrossRefPubMedPubMedCentral
36.
go back to reference Pawlik TM, Gleisner AL, Cameron JL, et al. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery. 2007;141:610–8.CrossRefPubMed Pawlik TM, Gleisner AL, Cameron JL, et al. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery. 2007;141:610–8.CrossRefPubMed
37.
go back to reference Slidell MB, Chang DC, Cameron JL, 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;15:165–74.CrossRefPubMed Slidell MB, Chang DC, Cameron JL, 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;15:165–74.CrossRefPubMed
38.
go back to reference Falconi M, Crippa S, Dominguez I, et al. Prognostic relevance of lymph node ratio and number of resected nodes after curative resection of ampulla of Vater carcinoma. Ann Surg Oncol. 2008;15:3178–86.CrossRefPubMed Falconi M, Crippa S, Dominguez I, et al. Prognostic relevance of lymph node ratio and number of resected nodes after curative resection of ampulla of Vater carcinoma. Ann Surg Oncol. 2008;15:3178–86.CrossRefPubMed
39.
go back to reference Calero A, Escrig-Sos J, Mingol F, et al. Usefulness of the log odds of positive lymph nodes to predict and discriminate prognosis in gastric carcinomas. J Gastrointest Surg. 2015;19:813–20.CrossRefPubMed Calero A, Escrig-Sos J, Mingol F, et al. Usefulness of the log odds of positive lymph nodes to predict and discriminate prognosis in gastric carcinomas. J Gastrointest Surg. 2015;19:813–20.CrossRefPubMed
40.
go back to reference Song YX, Gao P, Wang ZN, et al. Which is the most suitable classification for colorectal cancer, log odds, the number or the ratio of positive lymph nodes? PLoS One. 2011;6:e28937.CrossRefPubMedPubMedCentral Song YX, Gao P, Wang ZN, et al. Which is the most suitable classification for colorectal cancer, log odds, the number or the ratio of positive lymph nodes? PLoS One. 2011;6:e28937.CrossRefPubMedPubMedCentral
41.
go back to reference Persiani R, Cananzi FC, Biondi A, et al. Log odds of positive lymph nodes in colon cancer: a meaningful ratio-based lymph node classification system. World J Surg. 2012;36:667–74.CrossRefPubMed Persiani R, Cananzi FC, Biondi A, et al. Log odds of positive lymph nodes in colon cancer: a meaningful ratio-based lymph node classification system. World J Surg. 2012;36:667–74.CrossRefPubMed
42.
go back to reference Yildirim E, Berberoglu U. Lymph node ratio is more valuable than level III involvement for prediction of outcome in node-positive breast carcinoma patients. World J Surg. 2007;31:276–89.CrossRefPubMed Yildirim E, Berberoglu U. Lymph node ratio is more valuable than level III involvement for prediction of outcome in node-positive breast carcinoma patients. World J Surg. 2007;31:276–89.CrossRefPubMed
43.
go back to reference Wang J, Hassett JM, Dayton MT, Kulaylat MN. The prognostic superiority of log odds of positive lymph nodes in stage III colon cancer. J Gastrointest Surg. 2008;12:1790–6.CrossRefPubMed Wang J, Hassett JM, Dayton MT, Kulaylat MN. The prognostic superiority of log odds of positive lymph nodes in stage III colon cancer. J Gastrointest Surg. 2008;12:1790–6.CrossRefPubMed
Metadata
Title
Number of evaluated lymph nodes and positive lymph nodes, lymph node ratio, and log odds evaluation in early-stage pancreatic ductal adenocarcinoma: numerology or valid indicators of patient outcome?
Authors
G. Lahat
N. Lubezky
F. Gerstenhaber
E. Nizri
M. Gysi
M. Rozenek
Y. Goichman
I. Nachmany
R. Nakache
I. Wolf
J. M. Klausner
Publication date
01-12-2016
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2016
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-016-0983-5

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