Abstract
Background
The prognostic value of nodal status in colorectal cancer (CRC) patients may be influenced by the total number of lymph nodes (LNs) harvested. This study evaluates the impact of LN ratio (LNR) on CRC patients’ outcome.
Methods
A total of 612 stage III CRC patients who underwent curative-intent surgery between 2004 and 2008 were enrolled. The measured end point was postoperative disease-free survival (DFS) and overall survival (OS).
Results
The metastatic LN numbers were significantly higher in patients with more than 12 LN harvested (4.6 ± 5.81 vs. 2.7 ± 1.97, P < 0.001). The mean LNR was 22.9 ± 20 % (range = 2–100 %, median = 16.7 %). As the cutoff value of LNR was set above 17 %, the impact of the LNR on 5-year DFS became statistically significant. In univariate analysis, the 5-year DFS and OS for patients with high-LNR tumors was 54.4 and 57.3 %, respectively, significantly lower than those for patients with low-LNR tumors (72.8 and 76.4 %; P < 0.001). In multivariate analysis, the independent factors affecting the 5-year DFS and OS were tumor depth, carcinoembryonic antigen level, and LNR.
Conclusion
The LNR, set at the median value or 17 %, could be an independent prognostic factor for stage III CRC patients.
Similar content being viewed by others
References
Compton CC, Fielding LP, Burgart LJ et al (2000) Prognostic factors in colorectal cancer. College of American Pathologists Consensus Statement 1999. Arch Pathol Lab Med 124:979–994. doi:10.1043/0003-9985(2000)124<0979:pficc>2.0.co;2
Edge SB, Byrd DR, Compton CC et al (2010) AJCC cancer staging manual, 7th edn. Springer, New York
Sobin LH, Gospodarowicz MK, Wittekind C (2009) TNM Classification of Malignant Tumours, 7th edn. Wiley–Blackwell, New York
Joseph NE, Sigurdson ER, Hanlon AL et al (2003) Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol 10:213–218
Baxter NN, Virnig DJ, Rothenberger DA et al (2005) Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst 97:219–225. doi:10.1093/jnci/dji020
Chang GJ, Rodriguez-Bigas MA, Skibber JM et al (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99:433–441. doi:10.1093/jnci/djk092
Le Voyer TE, Sigurdson ER, Hanlon AL et al (2003) Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 21:2912–2919. doi:10.1200/jco.2003.05.062
Xing Y, Badgwell BD, Ross MI et al (2009) Lymph node ratio predicts disease-specific survival in melanoma patients. Cancer 115:2505–2513. doi:10.1002/cncr.24290
Woodward WA, Vinh-Hung V, Ueno NT et al (2006) Prognostic value of nodal ratios in node-positive breast cancer. J Clin Oncol 24:2910–2916. doi:10.1200/jco.2005.03.1526
Inoue K, Nakane Y, Iiyama H et al (2002) The superiority of ratio-based lymph node staging in gastric carcinoma. Ann Surg Oncol 9:27–34
Berger AC, Sigurdson ER, Le Voyer T et al (2005) Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol 23:8706–8712. doi:10.1200/jco.2005.02.8852
Lee HY, Choi HJ, Park KJ et al (2007) Prognostic significance of metastatic lymph node ratio in node-positive colon carcinoma. Ann Surg Oncol 14:1712–1717. doi:10.1245/s10434-006-9322-3
National Comprehensive Cancer Network v3 (2010) Colon cancer clinical practice guidelines in oncology. http://www.nccn.org. Accessed Jan 2012
Baxter NN, Ricciardi R, Simunovic M, Urbach DR, Virnig BA (2010) An evaluation of the relationship between lymph node number and staging in pT3 colon cancer using population-based data. Dis Colon Rectum 53:65–70. doi:10.1007/DCR.0b013e3181c70425
Sjo OH, Merok MA, Svindland A, Nesbakken A (2012) Prognostic impact of lymph node harvest and lymph node ratio in patients with colon cancer. Dis Colon Rectum 55:307–315. doi:10.1097/DCR.0b013e3182423f62
Storli K, Søndenaa K, Furnes B, Leh S, Nesvik I, Bru T, Gudlaugsson E, Bukholm I, Norheim-Andersen S, Eide G (2011) Improved lymph node harvest from resected colon cancer specimens did not cause upstaging from TNM stage II to III. World J Surg 35:2796–2803. doi:10.1007/s00268-011-1248-7
Swanson RS, Compton CC, Stewart AK et al (2003) The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 10:65–71
Goldstein NS, Sanford W, Coffey M et al (1996) 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 106:209–216
Sarli L, Bader G, Iusco D et al (2005) Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer. Eur J Cancer 41:272–279. doi:10.1016/j.ejca.2004.10.010
Bando E, Yonemura Y, Taniguchi K et al (2002) Outcome of ratio of lymph node metastasis in gastric carcinoma. Ann Surg Oncol 9:775–784
Morris EJA, Maughan NJ, Forman D et al (2007) Identifying stage III colorectal cancer patients: the influence of the patient, surgeon, and pathologist. J Clin Oncol 25:2573–2579. doi:10.1200/JCO.2007.11.0445
Gonen M, Schrag D, Weiser MR (2009) Nodal staging score: a tool to assess adequate staging of node-negative colon cancer. J Clin Oncol 27:6166–6171. doi:10.1200/jco.2009.23.7958
Leibl S, Tsybrovskyy O, Denk H (2003) How many lymph nodes are necessary to stage early and advanced adenocarcinoma of the sigmoid colon and upper rectum? Virchows Arch 443:133–138. doi:10.1007/s00428-003-0858-3
Rodriguez Santiago JM, Munoz E, Marti M et al (2005) Metastatic lymph node ratio as a prognostic factor in gastric cancer. Eur J Surg Oncol 31:59–66. doi:10.1016/j.ejso.2004.09.013
van der Wal BC, Butzelaar RM, van der Meij S et al (2002) Axillary lymph node ratio and total number of removed lymph nodes: predictors of survival in stage I and II breast cancer. Eur J Surg Oncol 28:481–489
Berger AC, Watson JC, Ross EA et al (2004) The metastatic/examined lymph node ratio is an important prognostic factor after pancreaticoduodenectomy for pancreatic adenocarcinoma. Am Surg 70:235–240; discussion 240
Peng J, Xu Y, Guan Z et al (2008) Prognostic significance of the metastatic lymph node ratio in node-positive rectal cancer. Ann Surg Oncol 15:3118–3123. doi:10.1245/s10434-008-0123-8
Wang J, Hassett JM, Dayton MT et al (2008) Lymph node ratio: role in the staging of node-positive colon cancer. Ann Surg Oncol 15:1600–1608. doi:10.1245/s10434-007-9716-x
Moug SJ, Saldanha JD, McGregor JR et al (2009) Positive lymph node retrieval ratio optimises patient staging in colorectal cancer. Br J Cancer 100:1530–1533. doi:10.1038/sj.bjc.6605049
Vaccaro CA, Im V, Rossi GL et al (2009) Lymph node ratio as prognosis factor for colon cancer treated by colorectal surgeons. Dis Colon Rectum 52:1244–1250. doi:10.1007/DCR.0b013e3181a65f0b
Schumacher P, Dineen S, Barnett C Jr et al (2007) The metastatic lymph node ratio predicts survival in colon cancer. Am J Surg 194:827–831; discussion 831–832. doi:10.1016/j.amjsurg.2007.08.030
Rosenberg R, Friederichs J, Schuster T et al (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3,026 patients over a 25-year time period. Ann Surg 248:968–978. doi:10.1097/SLA.0b013e318190eddc
Peschaud F, Benoist S, Julie C et al (2008) The ratio of metastatic to examined lymph nodes is a powerful independent prognostic factor in rectal cancer. Ann Surg 248:1067–1073. doi:10.1097/SLA.0b013e31818842ec
Gao P, Song YX, Wang ZN et al (2012) Integrated ratio of metastatic to examined lymph nodes and number of metastatic lymph nodes into the AJCC staging system for colon cancer. PLoS ONE 7:e35021. doi:10.1371/journal.pone.0035021
Rosenberg R, Engel J, Bruns C et al (2010) The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients. Ann Surg 251:1070–1078. doi:10.1097/SLA.0b013e3181d7789d
Redston M (2001) Carcinogenesis in the GI tract: from morphology to genetics and back again. Mod Pathol 14:236–245. doi:10.1038/modpathol.3880292
Distler P, Holt PR (1997) Are right- and left-sided colon neoplasms distinct tumors? Dig Dis 15:302–311
Thibodeau SN, Bren G, Schaid D (1993) Microsatellite instability in cancer of the proximal colon. Science 260:816–819
Author information
Authors and Affiliations
Corresponding author
Additional information
Yen-Jung Lu and Pei-Ching Lin contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lu, YJ., Lin, PC., Lin, CC. et al. The Impact of the Lymph Node Ratio is Greater than Traditional Lymph Node Status in Stage III Colorectal Cancer Patients. World J Surg 37, 1927–1933 (2013). https://doi.org/10.1007/s00268-013-2051-4
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00268-013-2051-4