World Journal of Surgery

, Volume 39, Issue 12, pp 3008–3015 | Cite as

Prognostic Impact of Distribution of Lymph Node Metastases in Stage III Colon Cancer

  • Toshiya Nagasaki
  • Takashi AkiyoshiEmail author
  • Yoshiya Fujimoto
  • Tsuyoshi Konishi
  • Satoshi Nagayama
  • Yosuke Fukunaga
  • Masami Arai
  • Masashi Ueno
Original Scientific Report



Complete mesocolic excision (CME) with central vascular ligation (CVL) is a well-known concept in colon cancer surgery. However, data on the oncological benefits of CVL are scarce. The objective of this study was to evaluate the prognostic significance of the distribution of lymph node metastases (LND) in patients with stage III colon cancer who underwent CME with CVL.


In total, 446 consecutive patients who underwent curative resection for stage III colon cancer from 2005 to 2011 were analyzed. Patients were classified as having LND1 (metastases in pericolic nodes), LND2 (metastases in intermediate nodes), or LND3 (metastases in main nodes). Survival outcomes were compared among the three groups.


LND1, LND2, and LND3 were identified in 299 (67.0 %), 122 (27.4 %), and 25 (5.6 %) patients, respectively. The 5-year overall survival and relapse-free survival (RFS) of all patients were 86.7 and 76.2 %, respectively. The 5-year RFS of patients with LND1, LND2, and LND3 were 82.8, 65.4, and 52.0 %, respectively (p < 0.0001). Multivariate analysis showed that LND2 was an independent prognostic factor for RFS (p = 0.0185), although the significance of LND3 was marginal (p = 0.0621). Among patients with pN1, the 5-year RFS of patients with LND1 and LND2+3 were significantly different (84.4 vs. 71.5 %, respectively, p = 0.0102), and similar tendency was found between patients with pN2-LND1 and pN2-LND2+3 (72.6 vs. 53.1 %, p = 0.0428).


The high 5-year survival rates of patients with stage III colon cancer, even those with LND2 and LND3, would justify CVL as the standard procedure for advanced colon cancer.


Lymph Node Metastasis Colon Cancer Lynch Syndrome Complete Mesocolic Excision Advanced Colon Cancer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Author contributions

TN and TA contributed to the conception and design of this study. All the authors acquired, analyzed, and interpreted the data. All the authors contributed to drafting the article and to its critical revision. All the authors read and approved the final version.

Compliance with ethical standards

Conflict of interest

All the authors have no conflict of interest or financial ties to disclose in association with this study.


  1. 1.
    Hashiguchi Y, Hase K, Ueno H et al (2010) Prognostic significance of the number of lymph nodes examined in colon cancer surgery: clinical application beyond simple measurement. Ann Surg 251:872–881CrossRefPubMedGoogle Scholar
  2. 2.
    Newland RC, Dent OF, Lyttle MN et al (1994) Pathologic determinants of survival associated with colorectal cancer with lymph node metastases. A multivariate analysis of 579 patients. Cancer 73:2076–2082CrossRefPubMedGoogle Scholar
  3. 3.
    Edge SB, Compton CC (2010) The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 17:1471–1474CrossRefPubMedGoogle Scholar
  4. 4.
    Kobayashi H, Ueno H, Hashiguchi Y et al (2006) Distribution of lymph node metastasis is a prognostic index in patients with stage III colon cancer. Surgery 139:516–522CrossRefPubMedGoogle Scholar
  5. 5.
    Kim CH, Huh JW, Kim HR et al (2014) Prognostic comparison between number and distribution of lymph node metastases in patients with right-sided colon cancer. Ann Surg Oncol 21:1361–1368CrossRefPubMedGoogle Scholar
  6. 6.
    Huh JW, Kim YJ, Kim HR (2012) Distribution of lymph node metastases is an independent predictor of survival for sigmoid colon and rectal cancer. Ann Surg 255:70–78CrossRefPubMedGoogle Scholar
  7. 7.
    Hida J, Okuno K, Yasutomi M et al (2005) Number versus distribution in classifying regional lymph node metastases from colon cancer. J Am Coll Surg 201:217–222CrossRefPubMedGoogle Scholar
  8. 8.
    Yeo K, Kim HH, Kim D et al (2014) A distribution weighted prognostic scoring model for node status in advanced rectal cancer. Cancer Res Treat 46:41–47PubMedCentralCrossRefPubMedGoogle Scholar
  9. 9.
    Hohenberger W, Weber K, Matzel K et al (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation–technical notes and outcome. Colorectal Dis 11:354–364CrossRefPubMedGoogle Scholar
  10. 10.
    West NP, Hohenberger W, Weber K et al (2010) Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol 28:272–278CrossRefPubMedGoogle Scholar
  11. 11.
    West NP, Morris EJA, Rotimi O et al (2008) Pathology grading of colon cancer surgical resection and its association with survival: a retrospective observational study. Lancet Oncol 9:857–865CrossRefPubMedGoogle Scholar
  12. 12.
    Akiyoshi T, Kuroyanagi H, Fujimoto Y et al (2010) Short-term outcomes of laparoscopic colectomy for transverse colon cancer. J Gastrointest Surg 14:818–823CrossRefPubMedGoogle Scholar
  13. 13.
    Akiyoshi T, Kuroyanagi H, Ueno M et al (2011) Learning curve for standardized laparoscopic surgery for colorectal cancer under supervision: a single-center experience. Surg Endosc 25:1409–1414CrossRefPubMedGoogle Scholar
  14. 14.
    Akiyoshi T, Kuroyanagi H, Oya M et al (2010) Factors affecting difficulty of laparoscopic surgery for left-sided colon cancer. Surg Endosc 24:2749–2754CrossRefPubMedGoogle Scholar
  15. 15.
    Fujimoto Y, Akiyoshi T, Kuroyanagi H et al (2010) Safety and feasibility of laparoscopic intersphincteric resection for very low rectal cancer. J Gastrointest Surg 14:645–650CrossRefPubMedGoogle Scholar
  16. 16.
    Japanese Society for cancer of the Colon and Rectum (2009) Japanese classification of colorectal carcinoma, 2nd edn. Kanehara & Co, TokyoGoogle Scholar
  17. 17.
    Weber K, Merkel S, Perrakis A et al (2013) Is there a disadvantage to radical lymph node dissection in colon cancer? Int J Colorectal Dis 28:217–226CrossRefPubMedGoogle Scholar
  18. 18.
    Cho MS, Baek SJ, Hur H et al (2014) Modified complete mesocolic excision with central vascular ligation for the treatment of right-sided colon cancer: long-term outcomes and prognostic factors. Ann Surg 00:1–8Google Scholar
  19. 19.
    Kobayashi H, Enomoto M, Higuchi T et al (2011) Clinical significance of lymph node ratio and location of nodal involvement in patients with right colon cancer. Dig Surg 28:190–197CrossRefPubMedGoogle Scholar
  20. 20.
    Kanemitsu Y, Komori K, Kimura K et al (2013) D3 lymph node dissection in right hemicolectomy with a no-touch isolation technique in patients with colon cancer. Dis Colon Rectum 56:815–824CrossRefPubMedGoogle Scholar
  21. 21.
    Kang J, Hur H, Min BS et al (2011) Prognostic impact of inferior mesenteric artery lymph node metastasis in colorectal cancer. Ann Surg Oncol 18:704–710CrossRefPubMedGoogle Scholar
  22. 22.
    Nagasue Y, Akiyoshi T, Ueno M et al (2013) Laparoscopic versus open multivisceral resection for primary colorectal cancer: comparison of perioperative outcomes. J Gastrointest Surg 17:1299–1305CrossRefPubMedGoogle Scholar
  23. 23.
    Nagasaki T, Akiyoshi T, Ueno M et al (2014) Laparoscopic salvage surgery for locally recurrent rectal cancer. J Gastrointest Surg 18:1319–1326CrossRefPubMedGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2015

Authors and Affiliations

  • Toshiya Nagasaki
    • 1
  • Takashi Akiyoshi
    • 1
    Email author
  • Yoshiya Fujimoto
    • 1
  • Tsuyoshi Konishi
    • 1
  • Satoshi Nagayama
    • 1
  • Yosuke Fukunaga
    • 1
  • Masami Arai
    • 2
  • Masashi Ueno
    • 1
  1. 1.Gastroenterological Center, Department of Gastroenterological Surgery, Cancer Institute HospitalJapanese Foundation for Cancer ResearchTokyoJapan
  2. 2.Department of Clinical Genetic Oncology, Cancer Institute HospitalJapanese Foundation for Cancer ResearchTokyoJapan

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