Factors Influencing the Number of Lymph Nodes Harvested for Stage I-III Colorectal Cancer in Thai Patients
Abstract
Introduction: Lymph node (LN) status is the most important predictor of survival in non-metastatic colorectal cancer (CRC). Recent guidelines recommend that a minimum of 12 nodes be examined for accurate staging. Three major classes of factors may influence the number of IN examined, including surgeon, pathologist and tumor/host factors.
Objectives: To identify factors influencing the number of LN harvested for stage I-III CRC in Thai patients and to review the adequacy of LN harvested by one surgeon.
Patients and Methods: A retrospective study of stage I-II CRC patients who underwent curative-intent resection by one surgeon was performed. Patients who underwent subtotal or total colectomy and patients who had preoperative chemoradiation were excluded. Variability in the quality of surgical technique was reduced by including patients who had operations performed by one surgeon only.
Results: From January 2001 to February 2008, 278 patients including 135 (49%) males and 143 (51%) females were eligible for analysis. The mean age was 62.3 years (SD, 11.8 years). There were 157 colon cancers (56.5%) and 121 rectal cancers (43.5%). The mean number of LN harvested was 17.3 nodes (18.7 nodes for colon cancer and 15.4 nodes for rectal cancer) with a median of 15 nodes (colon cancer, 16 nodes; rectal cancer, 14 nodes). Overall, 41 patients (15%) had inadequate LN harvest (<12 nodes; colon cancer, 8%; rectal cancer, 24%). Multivariable analysis revealed that factors associated with inadequate LN harvest included older age (>70years), left-sided colon or rectal cancer and early T-stage.
Conclusions: Excluding surgeon and pathologist factors, the number of harvested LNs in Thai patients was affected by patient and tumor factors, including age, location of tumor and T-stage. The high proportion of adequate LN harvest in the present study was probably due to a high volume caseload and the uniformly good quality of surgery as performed by one surgeon.
References
1. Compton CC. Optimal pathologic staging: defining stage ll disease. Clin Cancer Res 2007:13(22 Suppl):6862s-70s.
2. Evans MD, Barton K, Rees A, et al. 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 2008;10:157-64.
3. Bilimoria KY, Stewart Ak, Palis BE, et al. Adequacy and importance of lymph node evaluation for colon cancer in elderly. J Am Coll Surg 2008;206:247-54.
4. Jestin P, Pahlman L, Glimelius B, et al. Cancer staging and survival in colon cancer is dependent on the quality of the pathologists' specimen examination. Eur J Cancer 2005;41: 2071-8.
5. Baxter NN, Virnig DJ, Rothenberger DA, et al, Lymph node evaluation in colorectal cancer patients: a population based study. J Natl Cancer Inst 2005;97:219-25.
6. Kobayashi H, Ueno H, Hashiguchi Y, et al, Distribution of lymph node metastasis is a prognostic index in patients with stage Ill colon cancer. Surgery 2006;139:516-22.
7. Schumacher P, Dineen S, Barnett C Jr, et al. The metastatic lymph node ratio predicts survival in colon cancer. Am J Surg 2007;194:827-32.
8. Bilchik AJ, DiNome M, Saha S, et al. Prospective multicenter trial of staging adequacy in colon cancer: preliminary results. Arch Surg 2006;141:527-34.
9. Sarli L, Bader G, lusco D et al. Number of lymph nodes examined and prognosis of TNM stage ll colorectal cancer. Eur J Cancer 2005;41:272-9.
10. Bilchik A. More (nodes) + more (analysis) = less (mortality): challenging the therapeutic equation for early-stage colon Ann Surg Oncol 2003;10:203-5.
11. WongJ, Bowles B, BuenoR, Shimizu D. Impact of the number of negative nodes on disease-free survival in colorectal cancer patients. Dis Colon Rectum 2002;45:1341-8.
12. Nelson H, Petrelli N, Carlin A, et al. Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Ins 2001:93:583-96.
13. Green FL, Page DL, Fleming ID, et al, editors. AJCC Cancer Staging Manual. 6th ed. New York: Springer Verlag, 2002.
14. Sobin LH, Wittekind Ch, editors. UICC TNM classification of malignant tumors. 5th ed. New York: John Wiley and Sons,1997,,
15. Dukes CE. The classification of cancer of the rectum. J Pathol Bacteriol 1932:35:323-32.
16. Chang GJ, Rodriguez-Bigas MA, Skibber JM, et al, Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 2007;99:433-41.
17. Goldstein NS, Weldon S, Coffey M, et al. Lymph node recovery from colorectal resection specimens removed from 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.
18. Wong JH, Severino R, Honnebier MB, et al. Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 1999:17:2896-900.
19. Morris EJ, Maughan NJ, Forman D, et al. Identifying stage IlI colorectal cancer patients: the influence of the patient, surgeon, and pathologist. J Clin Oncol 2007:25:2573-9.
20. Simunovic M, Baxter NN. Lymph node counts in colon cancer surgery; lessons for users of quality indicators. JAMA 2007;298:2194-5,
21. Swanson RS, Compton CC, Stewart AK, et al. The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 2003; 10; 65-71.
22. 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;21:2912-9.
23. Prandi M, Lionetto R, Bini A, et al. 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 2002:235:458-63.
24. Tepper JE, O'Connell MJ, Niedzwiecki D, et al. Impact of number of nodes retrieval on outcome in patients with rectal cancer. J Clin Oncol 2001, 19:157-63.
25. Joseph NE, Sigurdson ER, Hanlon AL, et al. Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol 2003;10:213-8.
26. Caplin S, Cerottini JP, Bosman FT, et al. For patients with Dukes B (TNM Stage II) colorectal carcinoma, examination of six or fewer lymph nodes is related to poor prognosis. Cancer 1998;83:666-72.
27. Wright FC, Law CH, Last L, et al. Lymph node retrieval and assessment in stage Il colorectal cancer: a population based study. Ann Surg Oncol 2003;10:903-9.
28. Cianchi F, Palomba A, Boldi V, et al. Lymph node recovery from colorectal tumor specimens: recommendation for a minimum number of lymph nodes to be examined. World J Surg 2002;26:384-9.
29. Chen SL, Bilchik AJ. More extensive nodal dissection improves survival for stages I to Ill of colon cancer: a population based study. Ann Surg 2006;244:602-10.
30. Pocard M, Panis Y, Malassagne B, et al. Assessing the effectiveness of mesorectal excision in rectal cancer: prognostic value of the number of lymph nodes found in resected specimens. Dis Colon Rectum 1998;41:839-45.
31. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 2001;345:638-46.
32. BurdyG, Panis Y, Alves A, et al. Identifying patients with T3-T4 node-negative colon cancer at high risk of recurrence. Dis Colon Rectum 2001:44:1682-18.
33. Ratto C, Sofo L, Ippoliti M, et al. Accurate lymph-node detection in colorectal specimens resected for cancer is of prognostic significance. Dis Colon Retum 1999:42:143-54.
34. Cserni G, Vinh-Hung V, Buzykowski T. Is there a minimum number of lymph nodes that should be histologically assessed for a reliable nodal staging of T3NOMO colorectal carcinomas? J Surg Oncol 2002;81:63-9.
35. Goldstein NS. Lymph node recoveries from 2,427 pT3 colorectal resection specimens spanning 45 years: recommendation for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol 2002;26:179-89.
36. Wong SL, Ji H, Hollenbeck BK, et al. Hospital lymph node examination rates and survival after resection for colon cancer. JAMA 2007:298:2149-54.
37. Bui L, Rempel E, Reeson D, et al. 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.
38. Johnson PM, Porter GA, Ricciardi R, et al. Increasing negative lymph node count is independently associated with improved long-term survival in stage IIB and IIC colon cancer. J Clin Oncol 2006;24:3570-5.
39. Chen SL, Bilchik AJ. Resecting lymph nodes in colon cancer: more than a staging operation? Ann Surg Oncol 2007:14:2175-6.
40. Morris EJ, Maughan NJ, Forman D, et al. Who to treat with adjuvant therapy in Dukes B/ stage ll colorectal cancer? The need for high quality pathology. Gut 2007:56:1419-25.
41. Ricciardi R, Baxter NN. Association versus causation versus quality improvement: setting benchmarks for lymph node evaluation in colon cancer. J Natl Cancer Inst 2007:99:414-5.
42. Hida J, Okuno K, Yasutomi M, et al, Number versus distribution in classifying regional lymph node metastases from colon cancer. J Am Coll Surg 2005;201:217-22.
43. Miller EA, Woosley J, Martin CF, et al. Hospital-to-hospital variation in lymph node detection after colorectal resection. Cancer 2004;101:1065-71.
44. Law CH, Wright FC, Rapanos T, et al. Impact of lymph node retrieval and pathological ultra-staging on the prognosis of Stage ll colon cancer. J Surg Oncol 2003;84:1 20 -6.
45. Sigurdson ER. Lymph node dissection: Is it diagnostic or therapeutic? J Clin Oncol 2003;21:965-7.
46. Gunderson LL, Sargent DJ, Tepper JE, et al. Impact of T and N stage and treatment on survival and relapse in adjuvant rectal cancer: a pooled analysis. J Clin Oncol 2004;22:1785-96
47. Greene FL, Stewart AK, Norton HJ, New tumor-node- metastasis staging strategy for node-positive (stage Ill) rectal cancer: an analysis. J Clin Oncol 2004;22:1778-84.
48. O'Connell JB, Maggard MA, Ko CY, Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. J Natl Cancer Inst 2004;96:1420-5.
49. Hernanz F, Revuelta S, Redondo C, et al. Colorectal adenocarcinoma: quality of the assessment of lymph node metastases. Dis Colon Rectum 1994:37:373-6.
50. Maurel J, Launoy G, Grosclaude P, et al. Lymph node harvest reporting in patients with carcinoma of the large bowel: a French population-based study. Cancer 1998;82:1482-6.
51. Kim J, Huynh R, Abraham I, et al. Number of lymph nodes examined and its impact on colorectal cancer staging. Am Surg 2006:72:902-5.
52. Compton CC, Fielding LP, Burgart LJ, et al, Prognostic factors in colorectal cancer: College of American Pathologists consensus statement 1999. Arch Pathol Lab Med 2000;1 24:979-94.
53. Compton CC, Greene FL. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 2004:54:295-308.
54. Otchy D, Hyman NH, Simmang C, et al. Practice parameters for colon cancer. Dis Colon Rectum 2004;47:1269-84.
55. Berberoglu U, Prognostic significance of total lymph node number in patients with T1-4NOMO colorectal cancer. Hepatogastroenterology 2004;51:1689-93.
56. Quirke P, Morris E. Reporting colorectal cancer. Histopathology 2007:50:103-22.
57. 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? Virchow Arch 2003;443:133-8.
58. Tsai HL Lu CY, Hsieh JS, et al. The prognostic significance of total lymph node harvest in patients with T2-4N0M0 colorectal cancer. J Gastrointest Surg 2007;11:660-5.
59. Greco P, Magro G. Staging in colorectal cancer: problems for pathologists. Histopathology 2007:51:553-5.
60. Fielding LP, Aresnault PA, Chapuis PH, et al. Working party report to the World Congress of Gastroenterology, Sydney 1990. J Gastroenterol Hepatol 1991;6:325-44.
61. Lemmens VE, Verheij CD, Janssen-Heijnen ML, et al. Mixed adherence to clinical practice guidelines for colorectal cancer in the Southern Netherlands in 2002. Eur J Surg Oncol 2006:32:168-73.
62. NICE Improving Outcomes in Colorectal Cancer. Manual Update, London: National Institute for Clinical Excellence, May 2004.
63. Derwinger K, Carlsson G, Gustavsson B. Stage migration in colorectal cancer related to improved Iymph node assessment. Eur J Surg Oncol 2007:33:849-53.
64. Wright FC, Law CH, Last LD, et al. Barriers to optimal assessment of lymph nodes in colorectal cancer specimens. Am J Clin Pathol 2004; 121:663-70
65. Compton CC, Updated protocol for the examination of specimens from patients with carcinomas of the colon and rectum, excluding carcinoid tumors, lymphomas, sarcomas, and tumors of the vermiform appendix: a basis for checklists. Cancer Committee. Arch Pathol Lab Med 2000;124:1016-25.
66. Rosen LS, Bilchik AJ, Beart RW Jr, et al. New approaches to assessing and treating early-stage colon and rectal cancer: summary statement from 2007 Santa Monica Conference. Clin Cancer Res 2007:13(22 Suppl):6853s-6s.
67. Benson AL, Schrag D, Somerfield MR, et al. American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage ll colon cancer. J Clin Oncol 2004:16:3408-19.
68. Johnson PM, Malatjalian D, Porter GA, Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study. J Gastrointest Surg 2002:6:883-90.
69. Bull AD, Biffin AHB, Mella J, et al. Colorectal cancer pathology reporting: A regional audit. J Clin Pathol 1997:50:138-42.
70. Pheby DF, Levine DF, Pitcher RW, Shepherd NA. Lymph node harvests directly influence the staging of colorectal cancer: evidence from a regional audit. J Clin Pathol 2004;57:43-7.
71. Thorn CC, Woodcock NP, Scott N, et al. What factors affect lymph node yield in surgery for rectal cancer? Colorectal Dis 2004;6:356-61.
72. Harmon JW, Tang DG, Gordon TA, et al. Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection. Ann Surg 1999;230:404-13.
73. Ko CY, Chang JT, Chaudhry s, et al. Are high-volume surgeons and hospitals the most important predictors of in hospital outcome for colon cancer resection? Surgery 2002;132:268-73.
74. Panageas ks, Schrag D, Riedel E, et al. The effect of clustering of outcomes on the association of procedure volume and surgical outcomes. Ann Intern Med 2003;139:658-65.
75. Meyerhardt JA, Tepper JE, Niedzwiecki D, et al, Impact of hospital procedure volume on surgical operation and long-term outcomes in high risk curatively resected rectal cancer: findings from the Intergroup 0114 Study. J Clin Oncol 2004;22:166-74.
76. Hodgson DC, Zhang W, Zaslavsky AM, et al. Relation of hospital volume to colostomy rates and survival for patients with rectal cancer. J Natl Cancer Inst 2003;95:708-16.
77. Schrag D, Cramer LD, Bach PB, et al. Influence of hospital procedure volume on outcomes following surgery for colon cancer. JAMA 2000;284:3028-35.
78. Schrag D, Panageas KS, Riedel E, et al. Surgeon volume compared to hospital volume as a predictor of outcome following primary colon cancer resection. J Surg Oncol 2003;83:68-78.
79. Rabeneck L, Davila JA, Thompson M, et al. Surgical volume and long-term survival following surgery for colorectal cancer in the Veterans Affairs Health-Care System. Am J Gastroenterol 2004:99:668-75.
80. Reinbach DH, McGregor JR, Murray GD, et al. Effect of the surgeon's specialty interest on the type of resection performed for colorectal cancer. Dis Colon Rectum 1994:37:1020-3.
81. Baxendall M, Lewis F, Guillou, et al. Disappearing lymph nodes: One explanation for the fall in number with increasing age. J Pathol 2005;208(Suppl 1):29A.
82. McArdle CS, McMillan DC, Hole DJ. Male gender adversely affects survival following surgery for colorectal cancer. Br J Surg 2003;90:711-5.
83. Nagtegaal ID, Quirke P, Colorectal tumour deposits in the mesorectum and pericolon; a critical review. Histopathology 2007:51:141-9,
84. Marr R, Birbeck K, Garvican J, et al. The modern abdominoperineal excision: the next challenge after total mesorectal excision. Ann Surg 2005;242:74-82.
85. Crucitti F, Doglietto GB, Belantone R, et al. Accurate specimen preparation and examination is mandatory to detect lymph nodes and avoid under staging in colorectal cancer. J Surg Oncol 1992;51:153-7.
86. Gorog D, Nagy P, Peter A, et al. Influence of obesity on lymph node recovery from rectal resection specimens. Pathol Oncol Res 2003;9:180-3.
87. Halm EA, Lee C, Chassin MR. Is volume related to outcome in health care? A systematic review and methodologic critique of the literature. Ann Intern Med 2002;137:511-20.
88. Smith AJ, Law CH, Khalifa MA, et al. Multimodal CME for surgeons and pathologists improves colon cancer staging. J Cancer Educ 2003;18:81-6.
89. Apaikulchorn S, Suwanthanma W, Euanorasetr C. Adequacy of Iymph node harvested by curative intent resection for colorectal cancer: Ramathibodi Experience. Thai J Surg 2007:28:51-6.
2. Evans MD, Barton K, Rees A, et al. 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 2008;10:157-64.
3. Bilimoria KY, Stewart Ak, Palis BE, et al. Adequacy and importance of lymph node evaluation for colon cancer in elderly. J Am Coll Surg 2008;206:247-54.
4. Jestin P, Pahlman L, Glimelius B, et al. Cancer staging and survival in colon cancer is dependent on the quality of the pathologists' specimen examination. Eur J Cancer 2005;41: 2071-8.
5. Baxter NN, Virnig DJ, Rothenberger DA, et al, Lymph node evaluation in colorectal cancer patients: a population based study. J Natl Cancer Inst 2005;97:219-25.
6. Kobayashi H, Ueno H, Hashiguchi Y, et al, Distribution of lymph node metastasis is a prognostic index in patients with stage Ill colon cancer. Surgery 2006;139:516-22.
7. Schumacher P, Dineen S, Barnett C Jr, et al. The metastatic lymph node ratio predicts survival in colon cancer. Am J Surg 2007;194:827-32.
8. Bilchik AJ, DiNome M, Saha S, et al. Prospective multicenter trial of staging adequacy in colon cancer: preliminary results. Arch Surg 2006;141:527-34.
9. Sarli L, Bader G, lusco D et al. Number of lymph nodes examined and prognosis of TNM stage ll colorectal cancer. Eur J Cancer 2005;41:272-9.
10. Bilchik A. More (nodes) + more (analysis) = less (mortality): challenging the therapeutic equation for early-stage colon Ann Surg Oncol 2003;10:203-5.
11. WongJ, Bowles B, BuenoR, Shimizu D. Impact of the number of negative nodes on disease-free survival in colorectal cancer patients. Dis Colon Rectum 2002;45:1341-8.
12. Nelson H, Petrelli N, Carlin A, et al. Guidelines 2000 for colon and rectal cancer surgery. J Natl Cancer Ins 2001:93:583-96.
13. Green FL, Page DL, Fleming ID, et al, editors. AJCC Cancer Staging Manual. 6th ed. New York: Springer Verlag, 2002.
14. Sobin LH, Wittekind Ch, editors. UICC TNM classification of malignant tumors. 5th ed. New York: John Wiley and Sons,1997,,
15. Dukes CE. The classification of cancer of the rectum. J Pathol Bacteriol 1932:35:323-32.
16. Chang GJ, Rodriguez-Bigas MA, Skibber JM, et al, Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 2007;99:433-41.
17. Goldstein NS, Weldon S, Coffey M, et al. Lymph node recovery from colorectal resection specimens removed from 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.
18. Wong JH, Severino R, Honnebier MB, et al. Number of nodes examined and staging accuracy in colorectal carcinoma. J Clin Oncol 1999:17:2896-900.
19. Morris EJ, Maughan NJ, Forman D, et al. Identifying stage IlI colorectal cancer patients: the influence of the patient, surgeon, and pathologist. J Clin Oncol 2007:25:2573-9.
20. Simunovic M, Baxter NN. Lymph node counts in colon cancer surgery; lessons for users of quality indicators. JAMA 2007;298:2194-5,
21. Swanson RS, Compton CC, Stewart AK, et al. The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 2003; 10; 65-71.
22. 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;21:2912-9.
23. Prandi M, Lionetto R, Bini A, et al. 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 2002:235:458-63.
24. Tepper JE, O'Connell MJ, Niedzwiecki D, et al. Impact of number of nodes retrieval on outcome in patients with rectal cancer. J Clin Oncol 2001, 19:157-63.
25. Joseph NE, Sigurdson ER, Hanlon AL, et al. Accuracy of determining nodal negativity in colorectal cancer on the basis of the number of nodes retrieved on resection. Ann Surg Oncol 2003;10:213-8.
26. Caplin S, Cerottini JP, Bosman FT, et al. For patients with Dukes B (TNM Stage II) colorectal carcinoma, examination of six or fewer lymph nodes is related to poor prognosis. Cancer 1998;83:666-72.
27. Wright FC, Law CH, Last L, et al. Lymph node retrieval and assessment in stage Il colorectal cancer: a population based study. Ann Surg Oncol 2003;10:903-9.
28. Cianchi F, Palomba A, Boldi V, et al. Lymph node recovery from colorectal tumor specimens: recommendation for a minimum number of lymph nodes to be examined. World J Surg 2002;26:384-9.
29. Chen SL, Bilchik AJ. More extensive nodal dissection improves survival for stages I to Ill of colon cancer: a population based study. Ann Surg 2006;244:602-10.
30. Pocard M, Panis Y, Malassagne B, et al. Assessing the effectiveness of mesorectal excision in rectal cancer: prognostic value of the number of lymph nodes found in resected specimens. Dis Colon Rectum 1998;41:839-45.
31. Kapiteijn E, Marijnen CA, Nagtegaal ID, et al. Preoperative radiotherapy combined with total mesorectal excision for resectable rectal cancer. N Engl J Med 2001;345:638-46.
32. BurdyG, Panis Y, Alves A, et al. Identifying patients with T3-T4 node-negative colon cancer at high risk of recurrence. Dis Colon Rectum 2001:44:1682-18.
33. Ratto C, Sofo L, Ippoliti M, et al. Accurate lymph-node detection in colorectal specimens resected for cancer is of prognostic significance. Dis Colon Retum 1999:42:143-54.
34. Cserni G, Vinh-Hung V, Buzykowski T. Is there a minimum number of lymph nodes that should be histologically assessed for a reliable nodal staging of T3NOMO colorectal carcinomas? J Surg Oncol 2002;81:63-9.
35. Goldstein NS. Lymph node recoveries from 2,427 pT3 colorectal resection specimens spanning 45 years: recommendation for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol 2002;26:179-89.
36. Wong SL, Ji H, Hollenbeck BK, et al. Hospital lymph node examination rates and survival after resection for colon cancer. JAMA 2007:298:2149-54.
37. Bui L, Rempel E, Reeson D, et al. 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.
38. Johnson PM, Porter GA, Ricciardi R, et al. Increasing negative lymph node count is independently associated with improved long-term survival in stage IIB and IIC colon cancer. J Clin Oncol 2006;24:3570-5.
39. Chen SL, Bilchik AJ. Resecting lymph nodes in colon cancer: more than a staging operation? Ann Surg Oncol 2007:14:2175-6.
40. Morris EJ, Maughan NJ, Forman D, et al. Who to treat with adjuvant therapy in Dukes B/ stage ll colorectal cancer? The need for high quality pathology. Gut 2007:56:1419-25.
41. Ricciardi R, Baxter NN. Association versus causation versus quality improvement: setting benchmarks for lymph node evaluation in colon cancer. J Natl Cancer Inst 2007:99:414-5.
42. Hida J, Okuno K, Yasutomi M, et al, Number versus distribution in classifying regional lymph node metastases from colon cancer. J Am Coll Surg 2005;201:217-22.
43. Miller EA, Woosley J, Martin CF, et al. Hospital-to-hospital variation in lymph node detection after colorectal resection. Cancer 2004;101:1065-71.
44. Law CH, Wright FC, Rapanos T, et al. Impact of lymph node retrieval and pathological ultra-staging on the prognosis of Stage ll colon cancer. J Surg Oncol 2003;84:1 20 -6.
45. Sigurdson ER. Lymph node dissection: Is it diagnostic or therapeutic? J Clin Oncol 2003;21:965-7.
46. Gunderson LL, Sargent DJ, Tepper JE, et al. Impact of T and N stage and treatment on survival and relapse in adjuvant rectal cancer: a pooled analysis. J Clin Oncol 2004;22:1785-96
47. Greene FL, Stewart AK, Norton HJ, New tumor-node- metastasis staging strategy for node-positive (stage Ill) rectal cancer: an analysis. J Clin Oncol 2004;22:1778-84.
48. O'Connell JB, Maggard MA, Ko CY, Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. J Natl Cancer Inst 2004;96:1420-5.
49. Hernanz F, Revuelta S, Redondo C, et al. Colorectal adenocarcinoma: quality of the assessment of lymph node metastases. Dis Colon Rectum 1994:37:373-6.
50. Maurel J, Launoy G, Grosclaude P, et al. Lymph node harvest reporting in patients with carcinoma of the large bowel: a French population-based study. Cancer 1998;82:1482-6.
51. Kim J, Huynh R, Abraham I, et al. Number of lymph nodes examined and its impact on colorectal cancer staging. Am Surg 2006:72:902-5.
52. Compton CC, Fielding LP, Burgart LJ, et al, Prognostic factors in colorectal cancer: College of American Pathologists consensus statement 1999. Arch Pathol Lab Med 2000;1 24:979-94.
53. Compton CC, Greene FL. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 2004:54:295-308.
54. Otchy D, Hyman NH, Simmang C, et al. Practice parameters for colon cancer. Dis Colon Rectum 2004;47:1269-84.
55. Berberoglu U, Prognostic significance of total lymph node number in patients with T1-4NOMO colorectal cancer. Hepatogastroenterology 2004;51:1689-93.
56. Quirke P, Morris E. Reporting colorectal cancer. Histopathology 2007:50:103-22.
57. 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? Virchow Arch 2003;443:133-8.
58. Tsai HL Lu CY, Hsieh JS, et al. The prognostic significance of total lymph node harvest in patients with T2-4N0M0 colorectal cancer. J Gastrointest Surg 2007;11:660-5.
59. Greco P, Magro G. Staging in colorectal cancer: problems for pathologists. Histopathology 2007:51:553-5.
60. Fielding LP, Aresnault PA, Chapuis PH, et al. Working party report to the World Congress of Gastroenterology, Sydney 1990. J Gastroenterol Hepatol 1991;6:325-44.
61. Lemmens VE, Verheij CD, Janssen-Heijnen ML, et al. Mixed adherence to clinical practice guidelines for colorectal cancer in the Southern Netherlands in 2002. Eur J Surg Oncol 2006:32:168-73.
62. NICE Improving Outcomes in Colorectal Cancer. Manual Update, London: National Institute for Clinical Excellence, May 2004.
63. Derwinger K, Carlsson G, Gustavsson B. Stage migration in colorectal cancer related to improved Iymph node assessment. Eur J Surg Oncol 2007:33:849-53.
64. Wright FC, Law CH, Last LD, et al. Barriers to optimal assessment of lymph nodes in colorectal cancer specimens. Am J Clin Pathol 2004; 121:663-70
65. Compton CC, Updated protocol for the examination of specimens from patients with carcinomas of the colon and rectum, excluding carcinoid tumors, lymphomas, sarcomas, and tumors of the vermiform appendix: a basis for checklists. Cancer Committee. Arch Pathol Lab Med 2000;124:1016-25.
66. Rosen LS, Bilchik AJ, Beart RW Jr, et al. New approaches to assessing and treating early-stage colon and rectal cancer: summary statement from 2007 Santa Monica Conference. Clin Cancer Res 2007:13(22 Suppl):6853s-6s.
67. Benson AL, Schrag D, Somerfield MR, et al. American Society of Clinical Oncology recommendations on adjuvant chemotherapy for stage ll colon cancer. J Clin Oncol 2004:16:3408-19.
68. Johnson PM, Malatjalian D, Porter GA, Adequacy of nodal harvest in colorectal cancer: a consecutive cohort study. J Gastrointest Surg 2002:6:883-90.
69. Bull AD, Biffin AHB, Mella J, et al. Colorectal cancer pathology reporting: A regional audit. J Clin Pathol 1997:50:138-42.
70. Pheby DF, Levine DF, Pitcher RW, Shepherd NA. Lymph node harvests directly influence the staging of colorectal cancer: evidence from a regional audit. J Clin Pathol 2004;57:43-7.
71. Thorn CC, Woodcock NP, Scott N, et al. What factors affect lymph node yield in surgery for rectal cancer? Colorectal Dis 2004;6:356-61.
72. Harmon JW, Tang DG, Gordon TA, et al. Hospital volume can serve as a surrogate for surgeon volume for achieving excellent outcomes in colorectal resection. Ann Surg 1999;230:404-13.
73. Ko CY, Chang JT, Chaudhry s, et al. Are high-volume surgeons and hospitals the most important predictors of in hospital outcome for colon cancer resection? Surgery 2002;132:268-73.
74. Panageas ks, Schrag D, Riedel E, et al. The effect of clustering of outcomes on the association of procedure volume and surgical outcomes. Ann Intern Med 2003;139:658-65.
75. Meyerhardt JA, Tepper JE, Niedzwiecki D, et al, Impact of hospital procedure volume on surgical operation and long-term outcomes in high risk curatively resected rectal cancer: findings from the Intergroup 0114 Study. J Clin Oncol 2004;22:166-74.
76. Hodgson DC, Zhang W, Zaslavsky AM, et al. Relation of hospital volume to colostomy rates and survival for patients with rectal cancer. J Natl Cancer Inst 2003;95:708-16.
77. Schrag D, Cramer LD, Bach PB, et al. Influence of hospital procedure volume on outcomes following surgery for colon cancer. JAMA 2000;284:3028-35.
78. Schrag D, Panageas KS, Riedel E, et al. Surgeon volume compared to hospital volume as a predictor of outcome following primary colon cancer resection. J Surg Oncol 2003;83:68-78.
79. Rabeneck L, Davila JA, Thompson M, et al. Surgical volume and long-term survival following surgery for colorectal cancer in the Veterans Affairs Health-Care System. Am J Gastroenterol 2004:99:668-75.
80. Reinbach DH, McGregor JR, Murray GD, et al. Effect of the surgeon's specialty interest on the type of resection performed for colorectal cancer. Dis Colon Rectum 1994:37:1020-3.
81. Baxendall M, Lewis F, Guillou, et al. Disappearing lymph nodes: One explanation for the fall in number with increasing age. J Pathol 2005;208(Suppl 1):29A.
82. McArdle CS, McMillan DC, Hole DJ. Male gender adversely affects survival following surgery for colorectal cancer. Br J Surg 2003;90:711-5.
83. Nagtegaal ID, Quirke P, Colorectal tumour deposits in the mesorectum and pericolon; a critical review. Histopathology 2007:51:141-9,
84. Marr R, Birbeck K, Garvican J, et al. The modern abdominoperineal excision: the next challenge after total mesorectal excision. Ann Surg 2005;242:74-82.
85. Crucitti F, Doglietto GB, Belantone R, et al. Accurate specimen preparation and examination is mandatory to detect lymph nodes and avoid under staging in colorectal cancer. J Surg Oncol 1992;51:153-7.
86. Gorog D, Nagy P, Peter A, et al. Influence of obesity on lymph node recovery from rectal resection specimens. Pathol Oncol Res 2003;9:180-3.
87. Halm EA, Lee C, Chassin MR. Is volume related to outcome in health care? A systematic review and methodologic critique of the literature. Ann Intern Med 2002;137:511-20.
88. Smith AJ, Law CH, Khalifa MA, et al. Multimodal CME for surgeons and pathologists improves colon cancer staging. J Cancer Educ 2003;18:81-6.
89. Apaikulchorn S, Suwanthanma W, Euanorasetr C. Adequacy of Iymph node harvested by curative intent resection for colorectal cancer: Ramathibodi Experience. Thai J Surg 2007:28:51-6.
Downloads
Published
2008-07-31
How to Cite
1.
Euanorasetr C, Lertsithichai P. Factors Influencing the Number of Lymph Nodes Harvested for Stage I-III Colorectal Cancer in Thai Patients. Thai J Surg [Internet]. 2008 Jul. 31 [cited 2024 Dec. 23];29(3):81-92. Available from: https://he02.tci-thaijo.org/index.php/ThaiJSurg/article/view/241034
Issue
Section
Original Articles
License
Articles must be contributed solely to The Thai Journal of Surgery and when published become the property of the Royal College of Surgeons of Thailand. The Royal College of Surgeons of Thailand reserves copyright on all published materials and such materials may not be reproduced in any form without the written permission.
