International Journal of Colorectal Disease

, Volume 25, Issue 11, pp 1333–1341 | Cite as

Pathological examination of 12 regional lymph nodes and long-term survival in stages I–III colon cancer patients: an analysis of 2,056 consecutive patients in two branches of same institution

  • Hong Hwa Chen
  • Dilip Chakravarty K
  • Jeng-Yi Wang
  • Chung-Rong Changchien
  • Reiping TangEmail author
Original Article



Pathologic examination of at least 12 lymph nodes (LNs) is widely accepted as a standard for colon cancer surgery. We sought to address its association with patient source, other clinicopathological factors, and survival by comparing information from two branches in a large single institution.


Patients with stages I–III adenocarcinoma of the colon between 1998 and 2003 were identified from the Chang Gung Colorectal Tumor Registry in two branches (Linkou and Kaohsiung branches) of same institution. We used multivariate analysis to adjust for variables with P < 0.1 in univariate analyses.


A minimum of 12 examined nodes were observed in 80% of patients in Linkou branch versus 25% in Kaohsiung branch (P < 0.0001). Younger age, right hemicolectomy, larger tumor, higher tumor stage, higher caseload of surgeons, and patients at Linkou branch with an odds ratio (OR) as high as 23 (95% CI, 17–31) were independently associated with a higher frequency of ≥12 examined nodes. Patients with examined node number of <12 had a greater risk of recurrence within stages II and III (stage II: adjusted OR 1.88, 95% CI 1.27–2.79; stage III: adjusted OR 1.58, 95% CI 1.15–2.17) but not within stage I (OR 0.73, 95% CI 0.23–2.24).


The results confirm that factors influencing nodal harvest are multifactorial and the examined LN number of 12 or more is associated with an increased long-term survival in stages II–III colon cancer. It is possible to adequately sample and examine a sufficient number of nodes in the majority of colon cancer specimens by standardized conventional methods.


Colon cancer Survival Outcome Lymph node harvest TNM 

Supplementary material

384_2010_1020_MOESM1_ESM.doc (62 kb)
Table S1 (DOC 62 kb)
384_2010_1020_MOESM2_ESM.doc (46 kb)
Table S2 (DOC 45 kb)
384_2010_1020_Fig3_ESM.jpg (33 kb)
Fig. S1

(JPEG 33 kb)

384_2010_1020_MOESM3_ESM.tif (134 kb)
High resolution image. (TIFF 134 kb)


  1. 1.
    Cancer registry annual report (2008) Taiwan, R.O.C., Taipei. Department of Health, the Executive Yuan, R.O.CGoogle Scholar
  2. 2.
    Nelson H, Petrelli N, Carlin A et al (2001) Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Inst 93:583–596CrossRefPubMedGoogle Scholar
  3. 3.
    Jemal A, Siegel R, Ward E et al (2008) Cancer statistics 2008. CA Cancer J Clin 58:71–96CrossRefPubMedGoogle Scholar
  4. 4.
    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 21:2912–2919CrossRefPubMedGoogle Scholar
  5. 5.
    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 99:433–441CrossRefPubMedGoogle Scholar
  6. 6.
    Fielding LP, Arsenault PA, Chapuis PH et al (1991) Clinicopathological staging for colorectal cancer. An international documentation systems and international comprehensive anatomical terminology. J Gastroenterol Hepatol 6:325–344CrossRefPubMedGoogle Scholar
  7. 7.
    Gonen M, Schran D, Weiser MR (2009) Nodal staging score: a tool to assess adequate staging of node-negative colon cancer. J Clin Oncol 27:6166–6171CrossRefPubMedGoogle Scholar
  8. 8.
    Wong JH, Severino R, Honnebier MB et al (1999) Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 17:2896–2900PubMedGoogle Scholar
  9. 9.
    Mammen JM, James LE, Molloy M et al (2007) The relationship of lymph node dissection and colon cancer survival in the Veterans Affairs Central Cancer Registry. Am J Surg 194:349–354CrossRefPubMedGoogle Scholar
  10. 10.
    Johnson PM, Malatjalian D, Porter GA (2002) Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study. J Gastrointest Surg 6:883–888CrossRefPubMedGoogle Scholar
  11. 11.
    Caplin S, Cerottini JP, Bosman FT et al (1998) For patients with Dukes’ B (TNM stage II) colorectal carcinoma, examination of six or fewer lymph nodes is related to poor prognosis. Cancer 83:666–672CrossRefPubMedGoogle Scholar
  12. 12.
    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 10:65–71CrossRefPubMedGoogle Scholar
  13. 13.
    Vather R, Sammour T, Kahokehr A, Connolly AB, Hill AG (2009) Lymph node evaluation and long-term survival in stage II and stage III colon cancer: a national study. Ann Surg Oncol 16:585–593CrossRefPubMedGoogle Scholar
  14. 14.
    Goldstein NS (2002) Lymph node recoveries from 2, 427 pT3 colorectal resection specimens spanning 45 years: recommendations for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol 26:179–189CrossRefPubMedGoogle Scholar
  15. 15.
    Compton CC, Greene FL (2004) The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 54:295–308CrossRefPubMedGoogle Scholar
  16. 16.
    National Comprehensive Cancer Network (NCCN); Available at Accessed June 26, 2009
  17. 17.
    Sobin HL, Greene FL (2001) TNM classification: clarification of number of regional lymph node for pN0. Cancer 92:452CrossRefPubMedGoogle Scholar
  18. 18.
    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 124:979–994PubMedGoogle Scholar
  19. 19.
    Wong SL, Ji H, Hollenbeck BK et al (2007) Hospital lymph node examination rates and survival after resection for colon cancer. JAMA 298:2149–2154CrossRefPubMedGoogle Scholar
  20. 20.
    Jestin P, Pahlman L, Glimelius B, Gunnarsson U (2005) Cancer staging and survival in colon cancer is dependent on the quality of the pathologists’ specimen examination. Eur J Cancer 41:2071–2078CrossRefPubMedGoogle Scholar
  21. 21.
    Bilimoria KY, Stewart AK, Palis BE et al (2008) Adequacy and importance of lymph node evaluation for colon cancer in the elderly. J Am Coll Surg 206:247–254CrossRefPubMedGoogle Scholar
  22. 22.
    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 41:272–279CrossRefPubMedGoogle Scholar
  23. 23.
    Prandi M, Lionetto R, Bini A et al (2002) Prognostic evaluation of stage B colon cancer patients is improved by an adequate lymphadenectomy: results of a secondary analysis of a large scale adjuvant trial. Ann Surg 235:458–463CrossRefPubMedGoogle Scholar
  24. 24.
    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 10:213–218CrossRefPubMedGoogle Scholar
  25. 25.
    Jessup JM, Gunderson LL, Greene FL et al (2009) Colon and rectum. In: Edge SB, Byrd DR, Compton CC et al (eds) AJCC cancer staging manual, 7th edn. Springer, New York, pp 143–164Google Scholar
  26. 26.
    Baxter NN, Virnig DJ, Rothenberger DA, Morris AM, Jessurun J, Virnig BA (2005) Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst 97:219–225CrossRefPubMedGoogle Scholar
  27. 27.
    Kelder W, Inberg B, Schaapveld M et al (2009) Impact of the number of histologically examined lymph nodes on prognosis in colon cancer: a population-based study in the Netherlands. Dis Colon Rectum 52:260–267PubMedGoogle Scholar
  28. 28.
    Evans MD, Barton K, Rees A et al (2008) The impact of surgeon and pathologist on lymph node retrieval in colorectal cancer and its impact on survival for patients with Dukes’ stage B disease. Colorectal Dis 10:157–164PubMedGoogle Scholar
  29. 29.
    Feinstein AR, Sosin DM, Wells CK (1985) The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 312:1604–1608CrossRefPubMedGoogle Scholar
  30. 30.
    Pagès F, Berger A, Camus M et al (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353:2654–2666CrossRefPubMedGoogle Scholar
  31. 31.
    Eveno C, Nemeth J, Soliman H et al (2010) Association between a high number of isolated lymph nodes in T1 to T4 N0M0 colorectal cancer and the microsatellite instability phenotype. Arch Surg 145:12–17CrossRefPubMedGoogle Scholar
  32. 32.
    Sankila R, Aaltonen LA, Järvinen HJ, Mecklin JP (1996) Better survival rates in patients with MLH1-associated hereditary colorectal cancer. Gastroenterology 110:682–687CrossRefPubMedGoogle Scholar
  33. 33.
    Jass JR (2000) Pathology of hereditary nonpolyposis colorectal cancer. Ann NY Acad Sci 910:62–74CrossRefPubMedGoogle Scholar
  34. 34.
    Wright FC, Gagliardi AR, Law CH et al (2008) A randomized controlled trial to improve lymph node assessment in stage II colon cancer. Arch Surg 143:1050–1055CrossRefPubMedGoogle Scholar
  35. 35.
    Bembenek AE, Rosenberg R, Wagler E et al (2007) Sentinel lymph node biopsy in colon cancer: a prospective multicenter trial. Ann Surg 245:858–863CrossRefPubMedGoogle Scholar
  36. 36.
    Nordgård O, Oltedal S, Kørner H et al (2009) Quantitative RT-PCR detection of tumor cells in sentinel lymph nodes isolated from colon cancer patients with an ex vivo approach. Ann Surg 249:602–607CrossRefPubMedGoogle Scholar
  37. 37.
    Stojadinovic A, Nissan A, Protic M et al (2007) Prospective randomized study comparing sentinel lymph node evaluation with standard pathologic evaluation for the staging of colon carcinoma: results from the United States Military Cancer Institute Clinical Trials Group Study GI-01. Ann Surg 245:846–857CrossRefPubMedGoogle Scholar
  38. 38.
    Bertagnolli M, Miedema B, Redston M et al (2004) Sentinel node staging of resectable colon cancer: results of a multicenter study. Ann Surg 240:624–628PubMedGoogle Scholar
  39. 39.
    Lim SJ, Feig BW, Wang H et al (2008) Sentinel lymph node evaluation does not improve staging accuracy in colon cancer. Ann Surg Oncol 15:46–51CrossRefPubMedGoogle Scholar
  40. 40.
    Redston M, Compton CC, Miedema BW et al (2006) Analysis of micrometastatic disease in sentinel lymph nodes from resectable colon cancer: results of Cancer and Leukemia Group B Trial 80001. J Clin Oncol 24878–24883Google Scholar
  41. 41.
    Berger AC, Sigurdson ER, LeVoyer T et al (2005) Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol 23:8706–8712CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Hong Hwa Chen
    • 1
    • 3
  • Dilip Chakravarty K
    • 2
  • Jeng-Yi Wang
    • 2
    • 3
  • Chung-Rong Changchien
    • 2
    • 3
  • Reiping Tang
    • 2
    • 4
    • 5
    Email author
  1. 1.Section of Colon and Rectal Surgery, Department of SurgeryChang Gung Memorial HospitalKaohsiungTaiwan
  2. 2.Section of Colon and Rectal Surgery, Department of SurgeryChang Gung Memorial HospitalLinkouTaiwan
  3. 3.College of MedicineChang Gung UniversityTaoyuanTaiwan
  4. 4.School of Traditional Chinese MedicineChang Gung UniversityTaoyuanTaiwan
  5. 5.Section of Colon and Rectal Surgery, Department of SurgeryChang Gung Memorial HospitalTaipeiRepublic of China

Personalised recommendations