Skip to main content
Top
Published in: Journal of Gastrointestinal Surgery 2/2013

01-02-2013 | 2012 SSAT Poster Presentation

N0/N1, PNL, or LNR? The Effect of Lymph Node Number on Accurate Survival Prediction in Pancreatic Ductal Adenocarcinoma

Authors: Nakul P. Valsangkar, Devon M. Bush, James S. Michaelson, Cristina R. Ferrone, Jennifer A. Wargo, Keith D. Lillemoe, Carlos Fernández-del Castillo, Andrew L. Warshaw, Sarah P. Thayer

Published in: Journal of Gastrointestinal Surgery | Issue 2/2013

Login to get access

Abstract

Introduction

We evaluated the prognostic accuracy of LN variables (N0/N1), numbers of positive lymph nodes (PLN), and lymph node ratio (LNR) in the context of the total number of examined lymph nodes (ELN).

Methods

Patients from SEER and a single institution (MGH) were reviewed and survival analyses performed in subgroups based on numbers of ELN to calculate excess risk of death (hazard ratio, HR).

Results

In SEER and MGH, higher numbers of ELN improved the overall survival for N0 patients. The prognostic significance (N0/N1) and PLN were too variable as the importance of a single PLN depended on the total number of LN dissected. LNR consistently correlated with survival once a certain number of lymph nodes were dissected (≥13 in SEER and ≥17 in the MGH dataset).

Conclusions

Better survival for N0 patients with increasing ELN likely represents improved staging. PLN have some predictive value but the ELN strongly influence their impact on survival, suggesting the need for a ratio-based classification. LNR strongly correlates with outcome provided that a certain number of lymph nodes is evaluated, suggesting that the prognostic accuracy of any LN variable depends on the total number of ELN.
Literature
1.
go back to reference Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA: a cancer journal for clinicians. 2010;60(5):277–300. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA: a cancer journal for clinicians. 2010;60(5):277–300.
2.
go back to reference Moon HJ, An JY, Heo JS, Choi SH, Joh JW, Kim YI. Predicting survival after surgical resection for pancreatic ductal adenocarcinoma. Pancreas. 2006 Jan;32(1):37–43. Moon HJ, An JY, Heo JS, Choi SH, Joh JW, Kim YI. Predicting survival after surgical resection for pancreatic ductal adenocarcinoma. Pancreas. 2006 Jan;32(1):37–43.
3.
go back to reference Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (eds). Chapters 10 and 24. In: AJCC cancer staging manual, 7th edn. New York: Springer; 2010. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (eds). Chapters 10 and 24. In: AJCC cancer staging manual, 7th edn. New York: Springer; 2010.
4.
go back to reference Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Büchler MW. Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. The British Journal of Surgery. 2004 May;91(5):586–94. Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Büchler MW. Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. The British Journal of Surgery. 2004 May;91(5):586–94.
5.
go back to reference Brennan MF, Kattan MW, Klimstra D, Conlon K. Prognostic Nomogram for Patients Undergoing Resection for Adenocarcinoma of the Pancreas. Annals of Surgery. 2004 Aug;240(2):293–8. Brennan MF, Kattan MW, Klimstra D, Conlon K. Prognostic Nomogram for Patients Undergoing Resection for Adenocarcinoma of the Pancreas. Annals of Surgery. 2004 Aug;240(2):293–8.
6.
go back to reference Winter JM, Cameron JL, Campbell K a, Arnold M a, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience. Journal of Gastrointestinal Surgery. 2006 Nov;10(9):1199–210; discussion 1210–1. Winter JM, Cameron JL, Campbell K a, Arnold M a, Chang DC, Coleman J, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience. Journal of Gastrointestinal Surgery. 2006 Nov;10(9):1199–210; discussion 1210–1.
7.
go back to reference Richter A, Niedergethmann M, Sturm JW, Lorenz D, Post S, Trede M. Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience. World Journal of Surgery. 2003 Mar;27(3):324–9. Richter A, Niedergethmann M, Sturm JW, Lorenz D, Post S, Trede M. Long-term results of partial pancreaticoduodenectomy for ductal adenocarcinoma of the pancreatic head: 25-year experience. World Journal of Surgery. 2003 Mar;27(3):324–9.
8.
go back to reference Tseng JF, Raut CP, Lee JE, Pisters PWT, Vauthey J-N, Abdalla EK, et al. Pancreaticoduodenectomy with vascular resection: margin status and survival duration. Journal of Gastrointestinal Surgery. 2004 Dec;8(8):935–49; discussion 949–50. Tseng JF, Raut CP, Lee JE, Pisters PWT, Vauthey J-N, Abdalla EK, et al. Pancreaticoduodenectomy with vascular resection: margin status and survival duration. Journal of Gastrointestinal Surgery. 2004 Dec;8(8):935–49; discussion 949–50.
9.
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. Annals of surgery. 2003 Jan;237(1):74–85. Lim JE, Chien MW, Earle CC. Prognostic factors following curative resection for pancreatic adenocarcinoma: a population-based, linked database analysis of 396 patients. Annals of surgery. 2003 Jan;237(1):74–85.
10.
go back to reference House MG, Gönen M, Jarnagin WR, D'Angelica M, DeMatteo RP, Fong Y, et al. Prognostic significance of pathologic nodal status in patients with resected pancreatic cancer. Journal of Gastrointestinal Surgery. 2007 Nov;11(11):1549–55. House MG, Gönen M, Jarnagin WR, D'Angelica M, DeMatteo RP, Fong Y, et al. Prognostic significance of pathologic nodal status in patients with resected pancreatic cancer. Journal of Gastrointestinal Surgery. 2007 Nov;11(11):1549–55.
11.
go back to reference Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, et al. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery. 2007 May;141(5):610–8. Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, et al. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery. 2007 May;141(5):610–8.
12.
go back to reference Berger AC, Watson JC, Ross EA, Hoffman JP. The metastatic/examined lymph node ratio is an important prognostic factor after pancreaticoduodenectomy for pancreatic adenocarcinoma. The American Surgeon. 2004 Mar;70(3):235–40; discussion 240. Berger AC, Watson JC, Ross EA, Hoffman JP. The metastatic/examined lymph node ratio is an important prognostic factor after pancreaticoduodenectomy for pancreatic adenocarcinoma. The American Surgeon. 2004 Mar;70(3):235–40; discussion 240.
13.
go back to reference 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 Oct;33(3):240–5. 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 Oct;33(3):240–5.
14.
go back to reference Mariette C, Piessen G, Briez N, Triboulet JP. The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in esophageal cancer regardless of neoadjuvant chemoradiation or lymphadenectomy extent. Annals of surgery. 2008 Feb;247(2):365–71. Mariette C, Piessen G, Briez N, Triboulet JP. The number of metastatic lymph nodes and the ratio between metastatic and examined lymph nodes are independent prognostic factors in esophageal cancer regardless of neoadjuvant chemoradiation or lymphadenectomy extent. Annals of surgery. 2008 Feb;247(2):365–71.
15.
go back to reference Lee S-Y, Hwang I, Park Y-S, Gardner J, Ro JY. Metastatic lymph node ratio in advanced gastric carcinoma: a better prognostic factor than number of metastatic lymph nodes? International journal of oncology. 2010 Jun;36(6):1461–7. Lee S-Y, Hwang I, Park Y-S, Gardner J, Ro JY. Metastatic lymph node ratio in advanced gastric carcinoma: a better prognostic factor than number of metastatic lymph nodes? International journal of oncology. 2010 Jun;36(6):1461–7.
16.
go back to reference Falconi M, Crippa S, Domínguez I, Barugola G, Capelli P, Marcucci S, et al. Prognostic relevance of lymph node ratio and number of resected nodes after curative resection of ampulla of Vater carcinoma. Annals of surgical oncology. 2008 Nov;15(11):3178–86. Falconi M, Crippa S, Domínguez I, Barugola G, Capelli P, Marcucci S, et al. Prognostic relevance of lymph node ratio and number of resected nodes after curative resection of ampulla of Vater carcinoma. Annals of surgical oncology. 2008 Nov;15(11):3178–86.
17.
go back to reference Lee JH, Lee KG, Ha TK, Jun YJ, Paik SS, Park HK, et al. Pattern analysis of lymph node metastasis and the prognostic importance of number of metastatic nodes in ampullary adenocarcinoma. The American Surgeon. 2011 Mar;77(3):322–9. Lee JH, Lee KG, Ha TK, Jun YJ, Paik SS, Park HK, et al. Pattern analysis of lymph node metastasis and the prognostic importance of number of metastatic nodes in ampullary adenocarcinoma. The American Surgeon. 2011 Mar;77(3):322–9.
18.
go back to reference Chen SL, Steele SR, Eberhardt J, Zhu K, Bilchik A, Stojadinovic A. Lymph node ratio as a quality and prognostic indicator in stage III colon cancer. Annals of surgery. 2011 Jan;253(1):82–7. Chen SL, Steele SR, Eberhardt J, Zhu K, Bilchik A, Stojadinovic A. Lymph node ratio as a quality and prognostic indicator in stage III colon cancer. Annals of surgery. 2011 Jan;253(1):82–7.
19.
go back to reference Peparini N, Chirletti P. Lymph node ratio, number of excised nodes and sentinel-node concepts in breast cancer. Breast cancer research and treatment. 2011 Apr;126(3):829–33. Peparini N, Chirletti P. Lymph node ratio, number of excised nodes and sentinel-node concepts in breast cancer. Breast cancer research and treatment. 2011 Apr;126(3):829–33.
20.
go back to reference Spillane AJ, Cheung BLH, Winstanley J, Thompson JF. Lymph node ratio provides prognostic information in addition to American joint committee on cancer N stage in patients with melanoma, even if quality of surgery is standardized. Annals of surgery. 2011 Jan;253(1):109–15. Spillane AJ, Cheung BLH, Winstanley J, Thompson JF. Lymph node ratio provides prognostic information in addition to American joint committee on cancer N stage in patients with melanoma, even if quality of surgery is standardized. Annals of surgery. 2011 Jan;253(1):109–15.
21.
go back to reference Riediger H, Keck T, Wellner U, zur Hausen A, Adam U, Hopt UT, et al. The lymph node ratio is the strongest prognostic factor after resection of pancreatic cancer. Journal of Gastrointestinal Surgery. 2009 Jul;13(7):1337–44. Riediger H, Keck T, Wellner U, zur Hausen A, Adam U, Hopt UT, et al. The lymph node ratio is the strongest prognostic factor after resection of pancreatic cancer. Journal of Gastrointestinal Surgery. 2009 Jul;13(7):1337–44.
22.
go back to reference Massucco P, Ribero D, Sgotto E, Mellano A, Muratore A, Capussotti L. Prognostic significance of lymph node metastases in pancreatic head cancer treated with extended lymphadenectomy: not just a matter of numbers. Annals of surgical oncology. 2009 Dec;16(12):3323–32. Massucco P, Ribero D, Sgotto E, Mellano A, Muratore A, Capussotti L. Prognostic significance of lymph node metastases in pancreatic head cancer treated with extended lymphadenectomy: not just a matter of numbers. Annals of surgical oncology. 2009 Dec;16(12):3323–32.
23.
go back to reference Murakami Y, Uemura K, Sudo T, Hayashidani Y, Hashimoto Y, Nakashima A, et al. Number of metastatic lymph nodes, but not lymph node ratio, is an independent prognostic factor after resection of pancreatic carcinoma. Journal of the American College of Surgeons. 2010 Aug;211(2):196–204. Murakami Y, Uemura K, Sudo T, Hayashidani Y, Hashimoto Y, Nakashima A, et al. Number of metastatic lymph nodes, but not lymph node ratio, is an independent prognostic factor after resection of pancreatic carcinoma. Journal of the American College of Surgeons. 2010 Aug;211(2):196–204.
24.
go back to reference Xing Y, Badgwell BD, Ross MI, Gershenwald JE, Lee JE, Mansfield PF, et al. Lymph node ratio predicts disease-specific survival in melanoma patients. Cancer. 2009 Jun 1;115(11):2505–13. Xing Y, Badgwell BD, Ross MI, Gershenwald JE, Lee JE, Mansfield PF, et al. Lymph node ratio predicts disease-specific survival in melanoma patients. Cancer. 2009 Jun 1;115(11):2505–13.
25.
go back to reference Tomlinson JS, Jain S, Bentrem DJ, Sekeris EG, Maggard MA, Hines OJ, et al. Accuracy of staging node-negative pancreas cancer: a potential quality measure. Archives of surgery. 2007 Aug;142(8):767–723; discussion 773–4. Tomlinson JS, Jain S, Bentrem DJ, Sekeris EG, Maggard MA, Hines OJ, et al. Accuracy of staging node-negative pancreas cancer: a potential quality measure. Archives of surgery. 2007 Aug;142(8):767–723; discussion 773–4.
26.
go back to reference Schwarz RE, Smith DD. Extent of lymph node retrieval and pancreatic cancer survival: information from a large US population database. Annals of surgical oncology. 2006 Sep;13(9):1189–200. Schwarz RE, Smith DD. Extent of lymph node retrieval and pancreatic cancer survival: information from a large US population database. Annals of surgical oncology. 2006 Sep;13(9):1189–200.
27.
go back to reference Pavlidis TE, Pavlidis ET, Sakantamis AK. Current opinion on lymphadenectomy in pancreatic cancer surgery. Hepatobiliary & pancreatic diseases international. 2011 Feb;10(1):21–5. Pavlidis TE, Pavlidis ET, Sakantamis AK. Current opinion on lymphadenectomy in pancreatic cancer surgery. Hepatobiliary & pancreatic diseases international. 2011 Feb;10(1):21–5.
28.
go back to reference Kooby D a, Chu CK. Laparoscopic management of pancreatic malignancies. The Surgical clinics of North America. 2010 Apr;90(2):427–46. Kooby D a, Chu CK. Laparoscopic management of pancreatic malignancies. The Surgical clinics of North America. 2010 Apr;90(2):427–46.
29.
go back to reference Fernández-Cruz L, Cosa R, Blanco L, Levi S, López-Boado M-A, Navarro S. Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. Journal of Gastrointestinal Surgery. 2007 Dec;11(12):1607–21; discussion 1621–2. Fernández-Cruz L, Cosa R, Blanco L, Levi S, López-Boado M-A, Navarro S. Curative laparoscopic resection for pancreatic neoplasms: a critical analysis from a single institution. Journal of Gastrointestinal Surgery. 2007 Dec;11(12):1607–21; discussion 1621–2.
30.
go back to reference Dulucq JL, Wintringer P, Mahajna A. Laparoscopic pancreaticoduodenectomy for benign and malignant diseases. Surgical endoscopy. 2006 Jul;20(7):1045–50. Dulucq JL, Wintringer P, Mahajna A. Laparoscopic pancreaticoduodenectomy for benign and malignant diseases. Surgical endoscopy. 2006 Jul;20(7):1045–50.
31.
go back to reference Hellan M, Sun C-L, Artinyan A, Mojica-Manosa P, Bhatia S, Ellenhorn JDI, et al. The impact of lymph node number on survival in patients with lymph node-negative pancreatic cancer. Pancreas. 2008 Jul;37(1):19–24. Hellan M, Sun C-L, Artinyan A, Mojica-Manosa P, Bhatia S, Ellenhorn JDI, et al. The impact of lymph node number on survival in patients with lymph node-negative pancreatic cancer. Pancreas. 2008 Jul;37(1):19–24.
32.
go back to reference Slidell MB, Chang DC, Cameron JL, Wolfgang C, Herman JM, Schulick RD, 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. Annals of surgical oncology. 2008 Jan;15(1):165–74. Slidell MB, Chang DC, Cameron JL, Wolfgang C, Herman JM, Schulick RD, 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. Annals of surgical oncology. 2008 Jan;15(1):165–74.
33.
go back to reference Ishikawa O, Ohhigashi H, Sasaki Y, Kabuto T, Fukuda I, Furukawa H, et al. Practical usefulness of lymphatic and connective tissue clearance for the carcinoma of the pancreas head. Annals of surgery. 1988 Aug;208(2):215–20. Ishikawa O, Ohhigashi H, Sasaki Y, Kabuto T, Fukuda I, Furukawa H, et al. Practical usefulness of lymphatic and connective tissue clearance for the carcinoma of the pancreas head. Annals of surgery. 1988 Aug;208(2):215–20.
34.
go back to reference Manabe T, Ohshio G, Baba N, Miyashita T, Asano N, Tamura K, et al. Radical pancreatectomy for ductal cell carcinoma of the head of the pancreas. Cancer. 1989 Sep 1;64(5):1132–7. Manabe T, Ohshio G, Baba N, Miyashita T, Asano N, Tamura K, et al. Radical pancreatectomy for ductal cell carcinoma of the head of the pancreas. Cancer. 1989 Sep 1;64(5):1132–7.
35.
go back to reference Yeo CJ, Cameron JL, Lillemoe KD, Sohn TA, Campbell KA, Sauter PK, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Annals of surgery. 2002 Sep;236(3):355–66; discussion 366–8. Yeo CJ, Cameron JL, Lillemoe KD, Sohn TA, Campbell KA, Sauter PK, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma, part 2: randomized controlled trial evaluating survival, morbidity, and mortality. Annals of surgery. 2002 Sep;236(3):355–66; discussion 366–8.
36.
go back to reference Riall TS, Cameron JL, Lillemoe KD, Campbell KA, Sauter PK, Coleman J, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma—part 3: update on 5-year survival. Journal of Gastrointestinal Surgery. 2005 Dec;9(9):1191–204; discussion 1204–6. Riall TS, Cameron JL, Lillemoe KD, Campbell KA, Sauter PK, Coleman J, et al. Pancreaticoduodenectomy with or without distal gastrectomy and extended retroperitoneal lymphadenectomy for periampullary adenocarcinoma—part 3: update on 5-year survival. Journal of Gastrointestinal Surgery. 2005 Dec;9(9):1191–204; discussion 1204–6.
37.
go back to reference Pedrazzoli S, DiCarlo V, Dionigi R, Mosca F, Pederzoli P, Pasquali C, 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. Annals of surgery. 1998 Oct;228(4):508–17. Pedrazzoli S, DiCarlo V, Dionigi R, Mosca F, Pederzoli P, Pasquali C, 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. Annals of surgery. 1998 Oct;228(4):508–17.
38.
go back to reference Bhatti I, Peacock O, Awan AK, Semeraro D, Larvin M, Hall RI. Lymph node ratio versus number of affected lymph nodes as predictors of survival for resected pancreatic adenocarcinoma. World Journal of Surgery. 2010 Apr;34(4):768–75. Bhatti I, Peacock O, Awan AK, Semeraro D, Larvin M, Hall RI. Lymph node ratio versus number of affected lymph nodes as predictors of survival for resected pancreatic adenocarcinoma. World Journal of Surgery. 2010 Apr;34(4):768–75.
Metadata
Title
N0/N1, PNL, or LNR? The Effect of Lymph Node Number on Accurate Survival Prediction in Pancreatic Ductal Adenocarcinoma
Authors
Nakul P. Valsangkar
Devon M. Bush
James S. Michaelson
Cristina R. Ferrone
Jennifer A. Wargo
Keith D. Lillemoe
Carlos Fernández-del Castillo
Andrew L. Warshaw
Sarah P. Thayer
Publication date
01-02-2013
Publisher
Springer-Verlag
Published in
Journal of Gastrointestinal Surgery / Issue 2/2013
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-012-1974-7

Other articles of this Issue 2/2013

Journal of Gastrointestinal Surgery 2/2013 Go to the issue