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Published in: BMC Surgery 1/2016

Open Access 01-12-2016 | Research article

Factors affecting number of lymph nodes harvested and the impact of examining a minimum of 12 lymph nodes in stage I-III colorectal cancer patients: a retrospective single institution cohort study of 1167 consecutive patients

Authors: Hsiang-Lin Tsai, Ching-Wen Huang, Yung-Sung Yeh, Cheng-Jen Ma, Chao-Wen Chen, Chien-Yu Lu, Ming-Yii Huang, I-Ping Yang, Jaw-Yuan Wang

Published in: BMC Surgery | Issue 1/2016

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Abstract

Background

To identify factors affecting the harvest of lymph nodes (LNs) and to investigate the association between examining a minimum of 12 LNs and clinical outcomes in stage I-III colorectal cancer (CRC) patients.

Methods

The clinicopathologic features and the number of examined LNs for 1167 stage I-III CRC patients were analyzed to identify factors affecting the number of LNs harvested and the correlations between clinical outcomes and high harvests (≧12 LNs) and low harvests (<12 LNs).

Results

A multivariate analysis showed that age (P = 0.007), tumor size (P = 0.030), and higher T stage (P = 0.001) were independent factors affecting the examinations of LNs in colon cancer and that tumor size (P = 0.015) was the only independent factor in rectal cancer. Patients with low harvests had poorer overall survival with stage II and stage III CRC (stage II: P < 0.0001; III: P = 0.001) and poorer disease-free survival for stages I-III (stage I: P = 0.023; II: P < 0.0001; III: P = 0.001).

Conclusions

The factors influencing nodal harvest are multifactorial, and an adequate number of examined LNs (≧12) is associated with a survival benefit. Removal of at least 12 LNs will determine the lymph node status reliably.
Literature
1.
go back to reference Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.CrossRefPubMed Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.CrossRefPubMed
2.
go back to reference Compton CC, Green FI. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin. 2004;54:295–308.CrossRefPubMed Compton CC, Green FI. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin. 2004;54:295–308.CrossRefPubMed
3.
go back to reference Compton CC, Fielding LP, Burgart LJ, Conley B, Cooper HS, Hamilton SR, et al. Prognostic factors in colorectal cancer. College of American Pathologists Consensus Statement 1999. Arch Pathol Lab Med. 2000;124:979–94.PubMed Compton CC, Fielding LP, Burgart LJ, Conley B, Cooper HS, Hamilton SR, et al. Prognostic factors in colorectal cancer. College of American Pathologists Consensus Statement 1999. Arch Pathol Lab Med. 2000;124:979–94.PubMed
5.
go back to reference Goldstein NS, Sanford W, Coffey M, Layfield LJ. Lymph node recovery from colorectal resection specimens removed for adenocarcinoma. Trends over time and a recommendation for a minimum number of lymph nodes to be recovered. Am J Clin Pathol. 1996;106:209–16.CrossRefPubMed Goldstein NS, Sanford W, Coffey M, Layfield LJ. Lymph node recovery from colorectal resection specimens removed for adenocarcinoma. Trends over time and a recommendation for a minimum number of lymph nodes to be recovered. Am J Clin Pathol. 1996;106:209–16.CrossRefPubMed
6.
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;10:65–71.CrossRefPubMed 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;10:65–71.CrossRefPubMed
7.
go back to reference Johnson PM, Porter GA, Ricciardi R, Baxter NN. Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol. 2006;24:3570–5.CrossRefPubMed Johnson PM, Porter GA, Ricciardi R, Baxter NN. Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol. 2006;24:3570–5.CrossRefPubMed
8.
go back to reference Tsai HL, Yeh YS, Yu FJ, Lu CY, Chen CF, Chen CW, et al. Predicting factors of postoperative relapse in T2-4N0M0 colorectal cancer patients via harvesting a minimum of 12 lymph nodes. Int J Colorectal Dis. 2009;24:177–83.CrossRefPubMed Tsai HL, Yeh YS, Yu FJ, Lu CY, Chen CF, Chen CW, et al. Predicting factors of postoperative relapse in T2-4N0M0 colorectal cancer patients via harvesting a minimum of 12 lymph nodes. Int J Colorectal Dis. 2009;24:177–83.CrossRefPubMed
9.
go back to reference Sarli L, Bader G, Iusco D, Salvemini C, Mauro DD, Mazzeo A, et al. Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer. Eur J Cancer. 2005;41:272–9.CrossRefPubMed Sarli L, Bader G, Iusco D, Salvemini C, Mauro DD, Mazzeo A, et al. Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer. Eur J Cancer. 2005;41:272–9.CrossRefPubMed
10.
go back to reference Tsai HL, Yang IP, Lin CH, Chai CY, Huang YH, Chen CF, et al. Predictive value of vascular endothelial growth factor overexpression in early relapse of colorectal cancer patients after curative resection. Int J Colorectal Dis. 2013;28:415–24.CrossRefPubMed Tsai HL, Yang IP, Lin CH, Chai CY, Huang YH, Chen CF, et al. Predictive value of vascular endothelial growth factor overexpression in early relapse of colorectal cancer patients after curative resection. Int J Colorectal Dis. 2013;28:415–24.CrossRefPubMed
11.
go back to reference Hogan NM, Winter DC. A nodal positivity constant: new perspectives in lymph node evaluation and colorectal cancer. World J Surg. 2013;37:878–82.CrossRefPubMed Hogan NM, Winter DC. A nodal positivity constant: new perspectives in lymph node evaluation and colorectal cancer. World J Surg. 2013;37:878–82.CrossRefPubMed
12.
go back to reference Hida J, Okuno K, Yasutomi M, Yoshifuji T, Matsuzaki T, Uchida T, et al. Number versus distribution in classifying regional lymph node metastases from colon cancer. J Am Coll Surg. 2005;201:217–22.CrossRefPubMed Hida J, Okuno K, Yasutomi M, Yoshifuji T, Matsuzaki T, Uchida T, et al. Number versus distribution in classifying regional lymph node metastases from colon cancer. J Am Coll Surg. 2005;201:217–22.CrossRefPubMed
13.
go back to reference Tsai HL, Lu CH, Hsieh JS, Wu DC, Jan CM, Chai CY, et al. The prognostic significance of total lymph node harvest in patients with T2-4N0M0 colorectal cancer. J Gastrointest Surg. 2007;11:660–5.CrossRefPubMed Tsai HL, Lu CH, Hsieh JS, Wu DC, Jan CM, Chai CY, et al. The prognostic significance of total lymph node harvest in patients with T2-4N0M0 colorectal cancer. J Gastrointest Surg. 2007;11:660–5.CrossRefPubMed
14.
go back to reference Rosenberg R, Engel J, Bruns C, Heitland W, Hermes N, Jauch KW, et al. The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients. Ann Surg. 2010;251:1070–8.CrossRefPubMed Rosenberg R, Engel J, Bruns C, Heitland W, Hermes N, Jauch KW, et al. The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients. Ann Surg. 2010;251:1070–8.CrossRefPubMed
15.
go back to reference Kotake K, Honjo S, Sugihara K, Hashiguchi Y, Kato T, Kodaira S, et al. Number of lymph nodes retrieval is an important determinant of survival of patients with stage II and stage III colorectal cancer. Jpn J Clin Oncol. 2012;42:29–35.CrossRefPubMed Kotake K, Honjo S, Sugihara K, Hashiguchi Y, Kato T, Kodaira S, et al. Number of lymph nodes retrieval is an important determinant of survival of patients with stage II and stage III colorectal cancer. Jpn J Clin Oncol. 2012;42:29–35.CrossRefPubMed
16.
go back to reference Sjo OH, Merok MA, Svindland A, Nesbakken A. Prognostic impact of lymph node harvest and lymph node ratio in patients with colon cancer. Dis Colon Rectum. 2012;55:307–15.CrossRefPubMed Sjo OH, Merok MA, Svindland A, Nesbakken A. Prognostic impact of lymph node harvest and lymph node ratio in patients with colon cancer. Dis Colon Rectum. 2012;55:307–15.CrossRefPubMed
17.
go back to reference Chen SL, Bilchik AJ. More extensive nodal dissection improves survival for stage I to III of colon cancer: a population-based study. Ann Surg. 2006;244:602–10.PubMedPubMedCentral Chen SL, Bilchik AJ. More extensive nodal dissection improves survival for stage I to III of colon cancer: a population-based study. Ann Surg. 2006;244:602–10.PubMedPubMedCentral
18.
go back to reference Bui L, Rempel E, Reeson D, Simunovic M. Lymph node counts, rates of positive lymph nodes, and patient survival for colon cancer surgery in Ontario, Canada: A population-based study. J Surg Oncol. 2006;93:439–45.CrossRefPubMed Bui L, Rempel E, Reeson D, Simunovic M. Lymph node counts, rates of positive lymph nodes, and patient survival for colon cancer surgery in Ontario, Canada: A population-based study. J Surg Oncol. 2006;93:439–45.CrossRefPubMed
19.
go back to reference Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst. 2007;99:433–41.CrossRefPubMed Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst. 2007;99:433–41.CrossRefPubMed
20.
go back to reference Baxter NN, Virnig DJ, Rothenberger DA, Morris AM, Jessurun J, Virnig BA. Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst. 2005;97:219–25.CrossRefPubMed Baxter NN, Virnig DJ, Rothenberger DA, Morris AM, Jessurun J, Virnig BA. Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst. 2005;97:219–25.CrossRefPubMed
21.
go back to reference Gonsalves WI, Kanuri S, Tashi T, Aldoss I, Sama A, AI-Howaidi I, et al. Clinicopathologic factors associated with lymph node retrieval in resectable colon cancer: A veteran’s affairs central cancer registry (VACCR) database analysis. J Surg Oncol. 2011;104:667–71.CrossRefPubMed Gonsalves WI, Kanuri S, Tashi T, Aldoss I, Sama A, AI-Howaidi I, et al. Clinicopathologic factors associated with lymph node retrieval in resectable colon cancer: A veteran’s affairs central cancer registry (VACCR) database analysis. J Surg Oncol. 2011;104:667–71.CrossRefPubMed
22.
go back to reference Leibl S, Tsybrovskyy O, Denk H. How many lymph nodes are necessary to stage early and advanced adenocarcinoma of the sigmoid colon and upper rectum? Virchows Arch. 2003;443:133–8.CrossRefPubMed Leibl S, Tsybrovskyy O, Denk H. How many lymph nodes are necessary to stage early and advanced adenocarcinoma of the sigmoid colon and upper rectum? Virchows Arch. 2003;443:133–8.CrossRefPubMed
23.
go back to reference Tekkis P, Smith JJ, Heriot AG, Darzi AW, Thompson MR, Stamatakis JD, et al. A national study on lymph node retrieval in resectional surgery for colorectal cancer. Dis Colon Rectum. 2006;49:1673–83.CrossRefPubMed Tekkis P, Smith JJ, Heriot AG, Darzi AW, Thompson MR, Stamatakis JD, et al. A national study on lymph node retrieval in resectional surgery for colorectal cancer. Dis Colon Rectum. 2006;49:1673–83.CrossRefPubMed
24.
go back to reference Chen HH, Chakravarty KD, Wang JY, Changchien CR, Tang R. Pathological examination of 12 regional lymph nodes and long-term survival in stage I-III colon cancer patients: an analysis of 2,056 consecutive patients in two branches of same institution. Int J Colorectal Dis. 2010;25:1333–41.CrossRefPubMed Chen HH, Chakravarty KD, Wang JY, Changchien CR, Tang R. Pathological examination of 12 regional lymph nodes and long-term survival in stage I-III colon cancer patients: an analysis of 2,056 consecutive patients in two branches of same institution. Int J Colorectal Dis. 2010;25:1333–41.CrossRefPubMed
25.
go back to reference Kelder W, Inberg B, Schaapveld M, Karrenbeld A, Grond J, Wiggers T, et al. Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum. 2009;52:260–7.CrossRefPubMed Kelder W, Inberg B, Schaapveld M, Karrenbeld A, Grond J, Wiggers T, et al. Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum. 2009;52:260–7.CrossRefPubMed
26.
go back to reference Bilimoria KY, Stewart AK, Palis BE, Bentrem DJ, Talamoti MS, Ko CY. Adequacy and importance of lymph node evaluation for colon cancer in the elderly. J Am Coll Surg. 2008;206:247–54.CrossRefPubMed Bilimoria KY, Stewart AK, Palis BE, Bentrem DJ, Talamoti MS, Ko CY. Adequacy and importance of lymph node evaluation for colon cancer in the elderly. J Am Coll Surg. 2008;206:247–54.CrossRefPubMed
27.
go back to reference Vather R, Sammour T, Kahokehr A, Connolly AB, Hill AG. Lymph node evaluation and long-term survival in stage II and stage III colon cancer: a national study. Ann Surg Oncol. 2009;16:585–93.CrossRefPubMed Vather R, Sammour T, Kahokehr A, Connolly AB, Hill AG. Lymph node evaluation and long-term survival in stage II and stage III colon cancer: a national study. Ann Surg Oncol. 2009;16:585–93.CrossRefPubMed
28.
go back to reference Le Voyer TE, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ, 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;21:2912–9.CrossRefPubMed Le Voyer TE, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ, 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;21:2912–9.CrossRefPubMed
29.
go back to reference Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med. 1985;312:1604–8.CrossRefPubMed Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med. 1985;312:1604–8.CrossRefPubMed
30.
go back to reference Eveno C, Nemeth J, Soliman H, Praz F, de The H, Valleur P, et al. Association between a high number of isolated lymph nodes in T1 to T4N0M0 colorectal cancer and the microsatellite instability phenotype. Arch Surg. 2010;145:12–7.PubMed Eveno C, Nemeth J, Soliman H, Praz F, de The H, Valleur P, et al. Association between a high number of isolated lymph nodes in T1 to T4N0M0 colorectal cancer and the microsatellite instability phenotype. Arch Surg. 2010;145:12–7.PubMed
Metadata
Title
Factors affecting number of lymph nodes harvested and the impact of examining a minimum of 12 lymph nodes in stage I-III colorectal cancer patients: a retrospective single institution cohort study of 1167 consecutive patients
Authors
Hsiang-Lin Tsai
Ching-Wen Huang
Yung-Sung Yeh
Cheng-Jen Ma
Chao-Wen Chen
Chien-Yu Lu
Ming-Yii Huang
I-Ping Yang
Jaw-Yuan Wang
Publication date
01-12-2016
Publisher
BioMed Central
Published in
BMC Surgery / Issue 1/2016
Electronic ISSN: 1471-2482
DOI
https://doi.org/10.1186/s12893-016-0132-7

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