Skip to main content
Top
Published in: Annals of Surgical Oncology 1/2008

01-01-2008 | Hepatic and Pancreatic Tumors

Impact of Total Lymph Node Count and Lymph Node Ratio on Staging and Survival after Pancreatectomy for Pancreatic Adenocarcinoma: A Large, Population-Based Analysis

Authors: Mark B. Slidell, MD, MPH, David C. Chang, MPH, MBA, John L. Cameron, MD, Christopher Wolfgang, MD, PhD, Joseph M. Herman, MD, MSc, Richard D. Schulick, MD, Michael A. Choti, MD, MBA, Timothy M. Pawlik, MD, MPH

Published in: Annals of Surgical Oncology | Issue 1/2008

Login to get access

Abstract

Background

Based on data from other malignancies, the number of lymph nodes evaluated and the ratio of metastatic to examined lymph nodes (LNR) may be important predictors of survival. LNR has never been investigated in a large population-based study of patients with pancreatic adenocarcinoma.

Methods

The Surveillance, Epidemiology, and End Results (SEER) database was used to identify 4005 patients who underwent resection for pancreatic adenocarcinoma from 1988 to 2003. The effect of total lymph node count and LNR on survival was examined using univariate and multivariate analyses.

Results

The median number of lymph nodes examined was seven; 390 (10.1%) patients had no lymph nodes examined. Of those patients who had at least one lymph node examined, 1507 (43.3%) had no lymph node metastases (N0) and 1971 (56.7%) had metastatic nodal disease (N1). Overall median survival was 13 months, and 5-year survival was 6.8%. N1 disease was associated with a worse 5-year survival compared with N0 disease (4.3 vs 11.3%, respectively, P < .001). Patients with N0 disease could be further stratified based on the number of lymph nodes evaluated (median survival: 1–11 nodes, 16 months vs 12 or more nodes, 23 months; P < .001). For N1 patients, LNR was one of the most powerful factors associated with survival (LNR > 0–0.2, 15 months; LNR > 0.2–0.4, 12 months; LNR > 0.4, 10 months) (P < .001).

Conclusions

Most patients have an inadequate number of lymph nodes evaluated following pancreatic surgery. N0 patients who have fewer than 12 lymph nodes examined may be understaged. In patients with N1 disease, LNR may better substratify patients with regard to prognosis.
Literature
1.
go back to reference Greene FL. TNM staging for malignancies of the digestive tract: (2003) changes and beyond. Semin Surg Oncol 2003; 21(1):23–9PubMedCrossRef Greene FL. TNM staging for malignancies of the digestive tract: (2003) changes and beyond. Semin Surg Oncol 2003; 21(1):23–9PubMedCrossRef
2.
go back to reference Han SS, Jang JY, Kim SW, et al. Analysis of long-term survivors after surgical resection for pancreatic cancer. Pancreas 2006; 32(3):271–5PubMedCrossRef Han SS, Jang JY, Kim SW, et al. Analysis of long-term survivors after surgical resection for pancreatic cancer. Pancreas 2006; 32(3):271–5PubMedCrossRef
3.
go back to reference Makary MA, Winter JM, Cameron JL, et al. Pancreaticoduodenectomy in the very elderly. J Gastrointest Surg 2006; 10(3):347–56PubMedCrossRef Makary MA, Winter JM, Cameron JL, et al. Pancreaticoduodenectomy in the very elderly. J Gastrointest Surg 2006; 10(3):347–56PubMedCrossRef
4.
go back to reference Kuhlmann KF, de Castro SM, Wesseling JG, et al. Surgical treatment of pancreatic adenocarcinoma; actual survival and prognostic factors in 343 patients. Eur J Cancer 2004; 40(4):549–58PubMedCrossRef Kuhlmann KF, de Castro SM, Wesseling JG, et al. Surgical treatment of pancreatic adenocarcinoma; actual survival and prognostic factors in 343 patients. Eur J Cancer 2004; 40(4):549–58PubMedCrossRef
5.
go back to reference Reber HA. Lymph node involvement as a prognostic factor in pancreatic cancer. Int J Pancreatol 1990; 7(1–3):125–7PubMed Reber HA. Lymph node involvement as a prognostic factor in pancreatic cancer. Int J Pancreatol 1990; 7(1–3):125–7PubMed
6.
go back to reference Breslin TM, Hess KR, Harbison DB, et al. Neoadjuvant chemoradiotherapy for adenocarcinoma of the pancreas: treatment variables and survival duration. Ann Surg Oncol 2001; 8(2):123–32PubMedCrossRef Breslin TM, Hess KR, Harbison DB, et al. Neoadjuvant chemoradiotherapy for adenocarcinoma of the pancreas: treatment variables and survival duration. Ann Surg Oncol 2001; 8(2):123–32PubMedCrossRef
7.
go back to reference Benassai G, Mastrorilli M, Mosella F, Mosella G. Significance of lymph node metastases in the surgical management of pancreatic head carcinoma. J Exp Clin Cancer Res 1999; 18(1):23–8PubMed Benassai G, Mastrorilli M, Mosella F, Mosella G. Significance of lymph node metastases in the surgical management of pancreatic head carcinoma. J Exp Clin Cancer Res 1999; 18(1):23–8PubMed
8.
go back to reference Gebhardt C, Meyer W, Reichel M, Wunsch PH. Prognostic factors in the operative treatment of ductal pancreatic carcinoma. Langenbecks Arch Surg 2000; 385(1):14–20PubMedCrossRef Gebhardt C, Meyer W, Reichel M, Wunsch PH. Prognostic factors in the operative treatment of ductal pancreatic carcinoma. Langenbecks Arch Surg 2000; 385(1):14–20PubMedCrossRef
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. Ann Surg 2003; 237(1):74–85PubMedCrossRef 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(1):74–85PubMedCrossRef
10.
go back to reference Sohn TA, Yeo CJ, Cameron JL, et al. Resected adenocarcinoma of the pancreas-616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000; 4(6):567–79PubMedCrossRef Sohn TA, Yeo CJ, Cameron JL, et al. Resected adenocarcinoma of the pancreas-616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000; 4(6):567–79PubMedCrossRef
11.
go back to reference Pawlik TM, Abdalla EK, Barnett CC, et al. Feasibility of a randomized trial of extended lymphadenectomy for pancreatic cancer. Arch Surg 2005; 140(6):584–9; discussion 589–91PubMedCrossRef Pawlik TM, Abdalla EK, Barnett CC, et al. Feasibility of a randomized trial of extended lymphadenectomy for pancreatic cancer. Arch Surg 2005; 140(6):584–9; discussion 589–91PubMedCrossRef
12.
go back to reference Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997; 226(3):248–7; discussion 257–60PubMedCrossRef Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997; 226(3):248–7; discussion 257–60PubMedCrossRef
13.
go back to reference Le Voyer TE, Sigurdson ER, Hanlon AL, et al. Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 2003; 21(15):2912–9PubMedCrossRef Le Voyer TE, Sigurdson ER, Hanlon AL, et al. Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 2003; 21(15):2912–9PubMedCrossRef
14.
go back to reference Tepper JE, O’Connell MJ, Niedzwiecki D, et al. Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 2001; 19(1):157–63PubMed Tepper JE, O’Connell MJ, Niedzwiecki D, et al. Impact of number of nodes retrieved on outcome in patients with rectal cancer. J Clin Oncol 2001; 19(1):157–63PubMed
15.
go back to reference Berger AC, Sigurdson ER, LeVoyer T, et al. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol 2005; 23(34):8706–12PubMedCrossRef Berger AC, Sigurdson ER, LeVoyer T, et al. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol 2005; 23(34):8706–12PubMedCrossRef
16.
go back to reference Inoue K, Nakane Y, Iiyama H, et al. The superiority of ratio-based lymph node staging in gastric carcinoma. Ann Surg Oncol 2002; 9(1):27–34PubMedCrossRef Inoue K, Nakane Y, Iiyama H, et al. The superiority of ratio-based lymph node staging in gastric carcinoma. Ann Surg Oncol 2002; 9(1):27–34PubMedCrossRef
17.
go back to reference Bando E, Yonemura Y, Taniguchi K, et al. Outcome of ratio of lymph node metastasis in gastric carcinoma. Ann Surg Oncol 2002; 9(8):775–84PubMedCrossRef Bando E, Yonemura Y, Taniguchi K, et al. Outcome of ratio of lymph node metastasis in gastric carcinoma. Ann Surg Oncol 2002; 9(8):775–84PubMedCrossRef
18.
go back to reference Ichikura T, Ogawa T, Chochi K, et al. Minimum number of lymph nodes that should be examined for the International Union Against Cancer/American Joint Committee on Cancer TNM classification of gastric carcinoma. World J Surg 2003; 27(3):330–3PubMedCrossRef Ichikura T, Ogawa T, Chochi K, et al. Minimum number of lymph nodes that should be examined for the International Union Against Cancer/American Joint Committee on Cancer TNM classification of gastric carcinoma. World J Surg 2003; 27(3):330–3PubMedCrossRef
19.
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. Am Surg 2004; 70(3):235–40; discussion 240PubMed Berger AC, Watson JC, Ross EA, Hoffman JP. The metastatic/examined lymph node ratio is an important prognostic factor after pancreaticoduodenectomy for pancreatic adenocarcinoma. Am Surg 2004; 70(3):235–40; discussion 240PubMed
20.
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; 33(3):240–5PubMedCrossRef 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(3):240–5PubMedCrossRef
21.
go back to reference Pawlik TM GA, Cameron JL, Winter JM, et al. Prognostic Relevance of Lymph Node Ratio Following Pancreaticoduodenectomy for Pancreatic Cancer. Surgery 2007; 141(5):610–8PubMedCrossRef Pawlik TM GA, Cameron JL, Winter JM, et al. Prognostic Relevance of Lymph Node Ratio Following Pancreaticoduodenectomy for Pancreatic Cancer. Surgery 2007; 141(5):610–8PubMedCrossRef
22.
go back to reference Hartel M, Wente MN, Di Sebastiano P, et al. The role of extended resection in pancreatic adenocarcinoma: is there good evidence-based justification? Pancreatology 2004; 4(6):561–6PubMedCrossRef Hartel M, Wente MN, Di Sebastiano P, et al. The role of extended resection in pancreatic adenocarcinoma: is there good evidence-based justification? Pancreatology 2004; 4(6):561–6PubMedCrossRef
23.
go back to reference Zippin C, Lum D, Hankey BF. Completeness of hospital cancer case reporting from the SEER Program of the National Cancer Institute. Cancer 1995; 76(11):2343–50PubMedCrossRef Zippin C, Lum D, Hankey BF. Completeness of hospital cancer case reporting from the SEER Program of the National Cancer Institute. Cancer 1995; 76(11):2343–50PubMedCrossRef
24.
go back to reference Stata Statistical Software: Release 9.2 (computer program). College Station, TX: StataCorp LP 2005 Stata Statistical Software: Release 9.2 (computer program). College Station, TX: StataCorp LP 2005
25.
go back to reference Smith DD, Schwarz RR, Schwarz RE. Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol 2005; 23(28):7114–24PubMedCrossRef Smith DD, Schwarz RR, Schwarz RE. Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol 2005; 23(28):7114–24PubMedCrossRef
26.
go back to reference Ludwig MS, Goodman M, Miller DL, Johnstone PA. Postoperative survival and the number of lymph nodes sampled during resection of node-negative non-small cell lung cancer. Chest 2005; 128(3):1545–50PubMedCrossRef Ludwig MS, Goodman M, Miller DL, Johnstone PA. Postoperative survival and the number of lymph nodes sampled during resection of node-negative non-small cell lung cancer. Chest 2005; 128(3):1545–50PubMedCrossRef
27.
go back to reference Liu KJ, Loewen M, Atten MJ, et al. The survival of stage III gastric cancer patients is affected by the number of lymph nodes removed. Surgery 2003; 134(4):639–44; discussion 644–6PubMedCrossRef Liu KJ, Loewen M, Atten MJ, et al. The survival of stage III gastric cancer patients is affected by the number of lymph nodes removed. Surgery 2003; 134(4):639–44; discussion 644–6PubMedCrossRef
28.
go back to reference Konety BR, Joslyn SA, O’Donnell MA. Extent of pelvic lymphadenectomy and its impact on outcome in patients diagnosed with bladder cancer: analysis of data from the Surveillance, Epidemiology and End Results Program data base. J Urol 2003; 169(3):946–50PubMedCrossRef Konety BR, Joslyn SA, O’Donnell MA. Extent of pelvic lymphadenectomy and its impact on outcome in patients diagnosed with bladder cancer: analysis of data from the Surveillance, Epidemiology and End Results Program data base. J Urol 2003; 169(3):946–50PubMedCrossRef
29.
go back to reference Agrama MT, Reiter D, Cunnane MF, et al. Nodal yield in neck dissection and the likelihood of metastases. Otolaryngol Head Neck Surg 2003; 128(2):185–90PubMedCrossRef Agrama MT, Reiter D, Cunnane MF, et al. Nodal yield in neck dissection and the likelihood of metastases. Otolaryngol Head Neck Surg 2003; 128(2):185–90PubMedCrossRef
30.
go back to reference Bouvier AM, Haas O, Piard F, et al. How many nodes must be examined to accurately stage gastric carcinomas? Results from a population based study. Cancer 2002; 94(11):2862–6PubMedCrossRef Bouvier AM, Haas O, Piard F, et al. How many nodes must be examined to accurately stage gastric carcinomas? Results from a population based study. Cancer 2002; 94(11):2862–6PubMedCrossRef
31.
go back to reference Wisnivesky JP, Henschke C, McGinn T, Iannuzzi MC. Prognosis of Stage II non-small cell lung cancer according to tumor and nodal status at diagnosis. Lung Cancer 2005; 49(2):181–6PubMedCrossRef Wisnivesky JP, Henschke C, McGinn T, Iannuzzi MC. Prognosis of Stage II non-small cell lung cancer according to tumor and nodal status at diagnosis. Lung Cancer 2005; 49(2):181–6PubMedCrossRef
32.
go back to reference Swanson RS, Compton CC, Stewart AK, Bland KI. The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 2003; 10(1):65–71PubMedCrossRef Swanson RS, Compton CC, Stewart AK, Bland KI. The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 2003; 10(1):65–71PubMedCrossRef
33.
go back to reference Schwarz RE, Smith DD. Extent of lymph node retrieval and pancreatic cancer survival: information from a large US population database. Ann Surg Oncol 2006; 13(9):1189–200PubMedCrossRef Schwarz RE, Smith DD. Extent of lymph node retrieval and pancreatic cancer survival: information from a large US population database. Ann Surg Oncol 2006; 13(9):1189–200PubMedCrossRef
34.
go back to reference Herr HW. Superiority of ratio based lymph node staging for bladder cancer. J Urol 2003; 169(3):943–5PubMedCrossRef Herr HW. Superiority of ratio based lymph node staging for bladder cancer. J Urol 2003; 169(3):943–5PubMedCrossRef
35.
go back to reference Thorn CC, Woodcock NP, Scott N, et al. What factors affect lymph node yield in surgery for rectal cancer? Colorectal Dis 2004; 6(5):356–61PubMedCrossRef Thorn CC, Woodcock NP, Scott N, et al. What factors affect lymph node yield in surgery for rectal cancer? Colorectal Dis 2004; 6(5):356–61PubMedCrossRef
Metadata
Title
Impact of Total Lymph Node Count and Lymph Node Ratio on Staging and Survival after Pancreatectomy for Pancreatic Adenocarcinoma: A Large, Population-Based Analysis
Authors
Mark B. Slidell, MD, MPH
David C. Chang, MPH, MBA
John L. Cameron, MD
Christopher Wolfgang, MD, PhD
Joseph M. Herman, MD, MSc
Richard D. Schulick, MD
Michael A. Choti, MD, MBA
Timothy M. Pawlik, MD, MPH
Publication date
01-01-2008
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 1/2008
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-007-9587-1

Other articles of this Issue 1/2008

Annals of Surgical Oncology 1/2008 Go to the issue