TNM staging system of colorectal carcinoma: A critical appraisal of challenging issues

Archives of Pathology and Laboratory Medicine

Volumn 134, Issue 6, 2010, Pages 837-852

  Puppa, Giacomo ^a,b   Sonzogni, Angelica ^c   Colombari, Romano ^a   Pelosi, Giuseppe ^c,d  

^a G Fracastoro Hospital   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

^c EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT;

ARTICLE; CANCER STAGING; COLORECTAL TUMOR; HUMAN; METHODOLOGY; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PERITONEUM; TREATMENT OUTCOME; VASCULARIZATION;

ANTINEOPLASTIC AGENTS; COLORECTAL NEOPLASMS; HUMANS; NEOPLASM STAGING; NEOVASCULARIZATION, PATHOLOGIC; PERITONEUM; TREATMENT OUTCOME;

EID: 77953228914     PISSN: 00039985     EISSN: 15432165     Source Type: Journal    
DOI: None     Document Type: Article

References (188)

1. Dukes CE. The classification of cancer of the rectum. J Pathol Bacteriol. 1932;35: 323-332.
2. Kirklin JV, Dockerty MB, Waugh JM. The role of the peritoneal reflection in the prognosis of carcinoma of the rectum and sigmoid colon. Surg Gynecol Obstet. 1949;88(3):326-331.
3. Astler VB, Coller FA. The prognostic significance of direct extension of carcinoma of the colon and rectum. Ann Surg. 1954;139(6):846-852.
4. Dukes CE, Bussey HJ. The spread of rectal cancer and its effect on prognosis. Br J Cancer. 1958;12(3):309-320.
5. Jass JR, Morson BC. Reporting colorectal cancer. J Clin Pathol. 1987;40(9):1016-1023.
6. Haslam AC, Pearson JM, Bisset DL, Michie HR, Hobbiss JH. A Dukes/Jass combination-is it more discriminating? Colorectal Dis. 2006;8(5):418-422.
7. Sobin LH, Wittekind C, eds. TNM Classification of Malignant Tumors. 6th ed. New York, NY: Wiley-Liss; 2002.
8. Compton CC, Greene FL. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin. 2004;54(6):295-308.
9. Gospodarowicz MK, Miller D, Groome PA, Greene FL, Logan PA, Sobin LH. The process for continuous improvement of the TNM classification. Cancer. 2004;100(1):1-5.
10. Sobin LH, Wittekind C, eds. TNM Classification of Malignant Tumors. 5th ed. New York, NY: Wiley-Liss; 1997.
11. Hermanek P, Sobin LH, eds. TNM Classification of Malignant Tumors. 4th ed. New York, NY: Springer-Verlag; 1987.
12. Compton CC. Colorectal carcinoma: diagnostic, prognostic, and molecular features. Mod Pathol. 2003;16(4):376-388.
13. Turner RR, Li C, Compton CC. Newer pathologic assessment techniques for colorectal carcinoma. Clin Cancer Res. 2007;13(22 pt 2):6871s-6876s.
14. Zlobec I, Lugli A. Prognostic and predictive factors in colorectal cancer. J Clin Pathol. 2008;61(5):561-569.
15. Greene FL, Sobin LH. The staging of cancer: a retrospective and prospective appraisal. CA Cancer J Clin. 2008;58(3):180-190.
16. Hermanek P, Sobin LH, Wittekind C. How to improve the present TNM staging system. Cancer. 1999;86(11):2189-2191.
17. Compton CC. Optimal pathologic staging: defining stage II disease. Clin Cancer Res. 2007;13(22, pt 2):6862s-6870s.
18. Quah HM, Chou JF, Gonen M, et al. Identification of patients with highrisk stage II colon cancer for adjuvant therapy. Dis Colon Rectum. 2008;51(5):503-507.
19. Merkel S, Wein A, Gunther K, Papadopoulos T, Hohenberger W, Hermanek P. High-risk groups of patients with stage II colon carcinoma. Cancer. 2001;92(6):1435-1443.
20. Jeong SY, Chessin DB, Schrag D, Riedel E, Wong WD, Guillem JG. Re: Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. J Natl Cancer Inst. 2005;97(22):1705-1706.
21. 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(19):1420-1425.
22. Rosai J, Sobin LH, eds. Epithelial neoplasia of the intestines. In: Tumors of the Intestines. Washington, DC: Armed Forces Institute of Pathology; 2003. Atlas of Tumor Pathology; 3rd series.
23. Ueno H, Mochizuki H, Hashiguchi Y, et al. Histological grading of colorectal cancer: a simple and objective method. Ann Surg. 2008;247(5):811-818.
24. Jass JR, O'Brien J, Riddell RH, Snover DC. Recommendations for the reporting of surgically resected specimens of colorectal carcinoma: Association of Directors of Anatomic and Surgical Pathology. Am J Clin Pathol. 2008;129(1):13-23.
25. Wang LM, Kevans D, Mulcahy H, et al. Tumor budding is a strong and reproducible prognostic marker in T3N0 colorectal cancer. Am J Surg Pathol. 2009;33(1):134-141.
26. Wang HS, Liang WY, Lin TC, et al. Curative resection of T1 colorectal carcinoma: risk of lymph node metastasis and long-term prognosis. Dis Colon Rectum. 2005;48(6):1182-1192.
27. Ueno H, Price AB, Wilkinson KH, Jass JR, Mochizuki H, Talbot IC. A new prognostic staging system for rectal cancer. Ann Surg. 2004;240(5):832-839.
28. Prall F, Nizze H, Barten M. Tumour budding as prognostic factor in stage I/II colorectal carcinoma. Histopathology. 2005;47(1):17-24.
29. Okuyama T, Oya M, Ishikawa H. Budding as a risk factor for lymph node metastasis in pT1 or pT2 well-differentiated colorectal adenocarcinoma. Dis Colon Rectum. 2002;45(5):628-634.
30. Okuyama T, Oya M, Ishikawa H. Budding as a useful prognostic marker in pT3 well-or moderately-differentiated rectal adenocarcinoma. J Surg Oncol. 2003;83(1):42-47.
31. Okuyama T, Nakamura T, Yamaguchi M. Budding is useful to select highrisk patients in stage II well-differentiated or moderately differentiated colon adenocarcinoma. Dis Colon Rectum. 2003;46(10):1400-1406.
32. Hase K, Shatney C, Johnson D, Trollope M, Vierra M. Prognostic value of tumor "budding" in patients with colorectal cancer. Dis Colon Rectum. 1993;36(7):627-635.
33. Choi HJ, Park KJ, Shin JS, Roh MS, Kwon HC, Lee HS. Tumor budding as a prognostic marker in stage-III rectal carcinoma. Int J Colorectal Dis. 2007;22(8):863-868.
34. Washington MK. Colorectal carcinoma: selected issues in pathologic examination and staging and determination of prognostic factors. Arch Pathol Lab Med. 2008;132(10):1600-1607.
35. Jass JR, Atkin WS, Cuzick J, et al. The grading of rectal cancer: historical perspectives and a multivariate analysis of 447 cases. Histopathology. 1986;10(5):437-459.
36. Jass JR, Ajioka Y, Allen JP, et al. Assessment of invasive growth pattern and lymphocytic infiltration in colorectal cancer. Histopathology. 1996;28(6):543-548.
37. Merkel S, Mansmann U, Siassi M, Papadopoulos T, Hohenberger W, Hermanek P. The prognostic inhomogeneity in pT3 rectal carcinomas. Int J Colorectal Dis. 2001;16(5):298-304.
38. Bori R, Sejben I, Svébis M, et al. Heterogeneity of pT3 colorectal carcinomas according to the depth of invasion [published online ahead of print January 27, 2009]. Pathol Oncol Res. doi:10.1007/s12253-009-9149-x.
39. Wittekind C, Henson DE, Hutter RV, Sobin LH. TNM Supplement: A Commentary on Uniform Use. 3rd ed. Hoboken, New Jersey: John Wiley & Sons; 2003.
40. Wittekind C, Henson DE, Hutter RV, Sobin LH. TNM Supplement: A Commentary on Uniform Use. 2nd ed. New York, NY: Wiley-Liss; 2001.
41. Miyoshi M, Ueno H, Hashiguchi Y, Mochizuki H, Talbot IC. Extent of mesorectal tumor invasion as a prognostic factor after curative surgery for T3 rectal cancer patients. Ann Surg. 2006;243(4):492-498.
42. Cianchi F, Messerini L, Comin CE, et al. Pathologic determinants of survival after resection of T3N0 (stage IIA) colorectal cancer: proposal for a new prognostic model. Dis Colon Rectum. 2007;50(9):1332-1341.
43. Compton CC. Key issues in reporting common cancer specimens: problems in pathologic staging of colon cancer. Arch Pathol Lab Med. 2006;130(3):318-324.
44. Coverlizza S, Risio M, Ferrari A, Fenoglio-Preiser CM, Rossini FP. Colorectal adenomas containing invasive carcinoma: pathologic assessment of lymph node metastatic potential. Cancer. 1989;64(9):1937-1947.
45. Hassan C, Zullo A, Risio M, Rossini FP, Morini S. Histologic risk factors and clinical outcome in colorectal malignant polyp: a pooled-data analysis. Dis Colon Rectum. 2005;48(8):1588-1596.
46. Terry MB, Neugut AI, Bostick RM, Potter JD, Haile RW, Fenoglio-Preiser CM. Reliability in the classification of advanced colorectal adenomas. Cancer Epidemiol Biomarkers Prev. 2002;11(7):660-663.
47. Treanor D, Quirke P. Pathology of colorectal cancer. Clin Oncol (R Coll Radiol). 2007;19(10):769-776.
48. Hassan C, Laghi A, Zullo A, Iafrate F, Morini S. Q&A on diagnosis, screening and follow-up of colorectal neoplasia. Dig Liver Dis. 2008;40(2):85-96.
49. Ueno H, Mochizuki H, Hashiguchi Y, et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology. 2004;127(2):385-394.
50. Morson BC. Histological criteria for local excision. Br J Surg. 1985;72(suppl):S53-S54.
51. Williams B, Saunders BP. The rationale for current practice in the management of malignant colonic polyps. Endoscopy. 1993;25(7):469-474.
52. Cooper HS, Deppisch LM, Kahn EI, et al. Pathology of the malignant colorectal polyp. Hum Pathol. 1998;29(1):15-26.
53. Compton C, Fenoglio-Preiser CM, Pettigrew N, Fielding LP. American Joint Committee on Cancer Prognostic Factors Consensus Conference: Colorectal Working Group. Cancer. 2000;88(7):1739-1757.
54. Haggitt RC, Glotzbach RE, Soffer EE, Wruble LD. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology. 1985;89(2):328-336.
55. Kikuchi R, Takano M, Takagi K, et al. Management of early invasive colorectal cancer: risk of recurrence and clinical guidelines. Dis Colon Rectum. 1995;38(12):1286-1295.
56. Shia J, Klimstra DS. Intramucosal poorly differentiated colorectal carcinoma: can it be managed conservatively? Am J Surg Pathol. 2008;32(10):1586-1588.
57. Viale G, Sonzogni A, Pruneri G, et al. Histopathologic examination of axillary sentinel lymph nodes in breast carcinoma patients. J Surg Oncol. 2004;85(3):123-128.
58. Sternberg A, Amar M, Alfici R, Groisman G. Conclusions from a study of venous invasion in stage IV colorectal adenocarcinoma. J Clin Pathol. 2002;55(1):17-21.
59. Talbot IC, Ritchie S, Leighton M, Hughes AO, Bussey HJ, Morson BC. The clinical significance of invasion of veins by rectal cancer. Br J Surg. 1980;67: 439-442.
60. Nascimbeni R, Burgart LJ, Nivatvongs S, Larson DR. Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum. 2002;45(2):200-206.
61. Greene FL. Current TNM staging of colorectal cancer. Lancet Oncol. 2007;8(7):572-573.
62. Sobin LH. TNM, sixth edition: new developments in general concepts and rules. Semin Surg Oncol. 2003;21(1):19-22.
63. Koukourakis MI, Giatromanolaki A, Sivridis E, Gatter KC, Harris AL, for Tumour and Angiogenesis Research Group. Inclusion of vasculature-related variables in the Dukes staging system of colon cancer. Clin Cancer Res. 2005;11(24):8653-8660.
64. Sternberg A, Sibirsky O, Cohen D, Blumenson LE, Petrelli NJ. Validation of a new classification system for curatively resected colorectal adenocarcinoma. Cancer. 1999;86(5):782-792.
65. Sternberg A, Sibirsky O, Cohen D, Blumenson LE, Rodriguez-Bigas MA, Petrelli NJ. New approach to the substaging of node-positive colorectal adenocarcinoma. Ann Surg Oncol. 1999;6(2):161-165. (Pubitemid 29114279)
66. Minsky BD, Cohen AM. Blood vessel invasion in colorectal cancer-an alternative to TNM staging? Ann Surg Oncol. 1999;6(2):129-130.
67. Minsky B, Mies C. The clinical significance of vascular invasion in colorectal cancer. Dis Colon Rectum. 1989;32(9):794-803.
68. Talbot IC, Ritchie S, Leighton M, Hughes AO, Bussey HJ, Morson BC. Invasion of veins by carcinoma of rectum: method of detection, histological features and significance. Histopathology. 1981;5(2):141-163.
69. Kingston EF, Goulding H, Bateman AC. Vascular invasion is underrecognized in colorectal cancer using conventional hematoxylin and eosin staining. Dis Colon Rectum. 2007;50(11):1867-1872.
70. Vass DG, Ainsworth R, Anderson JH, Murray D, Foulis AK. The value of an elastic tissue stain in detecting venous invasion in colorectal cancer. J Clin Pathol. 2004;57(7):769-772.
71. Sternberg A, Mizrahi A, Amar M, Groisman G. Detection of venous invasion in surgical specimens of colorectal carcinoma: the efficacy of various types of tissue blocks. J Clin Pathol. 2006;59(2):207-210.
72. Abdulkader M, Abdulla K, Rakha E, Kaye P. Routine elastic staining assists detection of vascular invasion in colorectal cancer. Histopathology. 2006;49(5):487-492.
73. Inoue T, Mori M, Shimono R, Kuwano H, Sugimachi K. Vascular invasion of colorectal carcinoma readily visible with certain stains. Dis Colon Rectum. 1992;35(1):34-39.
74. Liang P, Nakada I, Hong JW, et al. Prognostic significance of immunohistochemically detected blood and lymphatic vessel invasion in colorectal carcinoma: its impact on prognosis. Ann Surg Oncol. 2007;14(2):470-477.
75. Blenkinsopp WK, Stewart-Brown S, Blesovsky L, Kearney G, Fielding LP. Histopathology reporting in large bowel cancer. J Clin Pathol. 1981;34(5):509-513.
76. Dirschmid K, Lang A, Mathis G, Haid A, Hansen M. Incidence of extramural venous invasion in colorectal carcinoma: findings with a new technique. Hum Pathol. 1996;27(11):1227-1230.
77. Ono C, Yoshinaga K, Enomoto M, Sugihara K. Discontinuous rectal cancer spread in the mesorectum and the optimal distal clearance margin in situ. Dis Colon Rectum. 2002;45(6):744-749.
78. Puppa G, Maisonneuve P, Sonzogni A, et al. Pathological assessment of pericolonic tumor deposits in advanced colonic carcinoma: relevance to prognosis and tumor staging. Mod Pathol. 2007;20(8):843-855.
79. Nagtegaal ID, Quirke P. Colorectal tumour deposits in the mesorectum and pericolon: a critical review. Histopathology. 2007;51(2):141-149.
80. Ueno H, Mochizuki H. Clinical significance of extrabowel skipped cancer infiltration in rectal cancer. Surg Today. 1997;27(7):617-622. (Pubitemid 27456043)
81. Goldstein NS, Turner JR. Pericolonic tumor deposits in patients with T3N+MO colon adenocarcinomas: markers of reduced disease free survival and intra-abdominal metastases and their implications for TNM classification. Cancer. 2000;88(10):2228-2238.
82. Tateishi S, Arima S, Futami K, et al. A clinicopathological investigation of "tumor nodules" in colorectal cancer. Surg Today. 2005;35(5):377-384.
83. Ratto C, Ricci R, Rossi C, Morelli U, Vecchio FM, Doglietto GB. Mesorectal microfoci adversely affect the prognosis of patients with rectal cancer. Dis Colon Rectum. 2002;45(6):733-742.
84. Stiles TE, Dean P, Harrison J. Nature and significance of nodular metastases of colonic carcinoma in pericolonic fat [abstract]. Mod Pathol. 1995;8: 69A.
85. Lo DS, Pollett A, Siu LL, Gallinger S, Burkes RL. Prognostic significance of mesenteric tumor nodules in patients with stage III colorectal cancer. Cancer. 2008;112(1):50-54.
86. Ueno H, Mochizuki H, Hashiguchi Y, et al. Extramural cancer deposits without nodal structure in colorectal cancer: optimal categorization for prognostic staging. Am J Clin Pathol. 2007;127(2):287-294.
87. Puppa G, Ueno H, Kayahara M, et al. Tumor deposits are encountered in advanced colorectal cancer and other adenocarcinomas: an expanded classification with implications for colorectal cancer staging system including a unifying concept of in-transit metastases. Mod Pathol. 2009;22(3):410-415.
88. Compton CC, for the Members of the Cancer Committee, College of American Pathologists. Colon and rectum. College of American Pathologists Web site. http://www.cap.org/apps/docs/cancer-protocols/2005/colonrectum05-ckw.pdf. Updated January 2005. Accessed September 30, 2005.
89. Shepherd NA, Baxter KJ, Love SB. The prognostic importance of peritoneal involvement in colonic cancer: a prospective evaluation. Gastroenterology. 1997;112(4):1096-1102.
90. Keshava A, Chapuis PH, Chan C, Lin BP, Bokey EL, Dent OF. The significance of involvement of a free serosal surface for recurrence and survival following resection of clinicopathological stage B and C rectal cancer. Colorectal Dis. 2007;9(7):609-618.
91. Izbicki JR, Hosch SB, Knoefel WT, Passlick B, Bloechle C, Broelsch CE. Extended resections are beneficial for patients with locally advanced colorectal cancer. Dis Colon Rectum. 1995;38(12):1251-1256.
92. Oh SY, Kim YB, Paek OJ, Suh KW. Contiguous invasion per se does not affect prognosis in colon cancer. J Surg Oncol. 2009;99(1):71-74.
93. Washington K, Berlin J, Branton P, et al. Protocol for the examination of specimens from patients with primary carcinomas of the colon and rectum. College of American Pathologists Web Site. Published July 2008. http://www.cap.org/apps/docs/committees/cancer/cancer-protocols/2008/ colonrectum08-pw.pdf. Accessed September 5, 2008.
94. Washington MK, Berlin J, Branton PA, et al. Protocol for the examination of specimens from patients with primary carcinomas of the colon and rectum. Arch Pathol Lab Med. 2008;132(7):1182-1193.
95. Ludeman L, Shepherd NA. Serosal involvement in gastrointestinal cancer: its assessment and significance. Histopathology. 2005;47(2):123-131.
96. Stewart C, Hillery S, Havlat M. Serosal involvement in colorectal carcinoma. Histopathology. 2006;49(4):435-437.
97. Merkel S, Mansmann U, Papadopoulos T, Wittekind C, Hohenberger W, Hermanek P. The prognostic inhomogeneity of colorectal carcinomas Stage III: a proposal for subdivision of Stage III. Cancer. 2001;92(11):2754-2759.
98. Greene FL, Stewart AK, Norton HJ. A new TNM staging strategy for nodepositive (stage III) colon cancer: an analysis of 50, 042 patients. Ann Surg. 2002;236(4):416-421.
99. Dhar DK, Yoshimura H, Kinukawa N, et al. Metastatic lymph node size and colorectal cancer prognosis. J Am Coll Surg. 2005;200(1):20-28.
100. Wong JH, Steinemann S, Tom P, Morita S, Tauchi-Nishi P. Volume of lymphatic metastases does not independently influence prognosis in colorectal cancer. J Clin Oncol. 2002;20(6):1506-1511.
101. Lagarde SM, Ten Kate FJ, de Boer DJ, Busch OR, Obertop H, van Lanschot JJ. Extracapsular lymph node involvement in node-positive patients with adenocarcinoma of the distal esophagus or gastroesophageal junction. Am J Surg Pathol. 2006;30(2):171-176.
102. Nakamura K, Ozaki N, Yamada T, et al. Evaluation of prognostic significance in extracapsular spread of lymph node metastasis in patients with gastric cancer. Surgery. 2005;137(5):511-517.
103. Komuta K, Okudaira S, Haraguchi M, Furui J, Kanematsu T. Identification of extracapsular invasion of the metastatic lymph nodes as a useful prognostic sign in patients with resectable colorectal cancer. Dis Colon Rectum. 2001;44(12):1838-1844.
104. Ueno H, Mochizuki H, Hashiguchi Y, Hase K. Prognostic determinants of patients with lateral nodal involvement by rectal cancer. Ann Surg. 2001;234(2):190-197.
105. Shida H, Ban K, Matsumoto M, et al. Prognostic significance of location of lymph node metastases in colorectal cancer. Dis Colon Rectum. 1992;35(11):1046-1050.
106. Newland RC, Dent OF, Lyttle MN, Chapuis PH, Bokey EL. Pathologic determinants of survival associated with colorectal cancer with lymph node metastases: a multivariate analysis of 579 patients. Cancer. 1994;73(8):2076-2082.
107. Hida J, Yasutomi M, Fujimoto K, et al. Comparison between the Japanese general rules and the TNM system in the regional lymph node classification of carcinoma of the colon. J Am Coll Surg. 1996;183(6):611-615.
108. Kim JC, Lee KH, Yu CS, et al. The clinicopathological significance of inferior mesenteric lymph node metastasis in colorectal cancer. Eur J Surg Oncol. 2004;30(3):271-279.
109. Vaccaro CA, Bonadeo FA, Benati ML, et al. Colorectal cancer staging: reappraisal of N/PN classification. Dis Colon Rectum. 2004;47(1):66-69.
110. Hermanek P, Guggenmoos-Holzmann I, Gall FP. Prognostic factors in rectal carcinoma: a contribution to the further development of tumor classification. Dis Colon Rectum. 1989;32(7):593-599.
111. Bruch HP, Schwandner O, Schiedeck TH, Roblick UJ. Actual standards and controversies on operative technique and lymph-node dissection in colorectal cancer. Langenbecks Arch Surg. 1999;384(2):167-175.
112. Steup WH, Moriya Y, van de Velde CJ. Patterns of lymphatic spread in rectal cancer: a topographical analysis on lymph node metastases. Eur J Cancer. 2002;38(7):911-918.
113. Ueno M, Oya M, Azekura K, Yamaguchi T, Muto T. Incidence and prognostic significance of lateral lymph node metastasis in patients with advanced low rectal cancer. Br J Surg. 2005;92(6):756-763.
114. Kanemitsu Y, Hirai T, Komori K, Kato T. Survival benefit of high ligation of the inferior mesenteric artery in sigmoid colon or rectal cancer surgery. Br J Surg. 2006;93(5):609-615.
115. Japanese Research Society for Cancer of the Colon and Rectum. General rules for clinical and pathological studies on cancer of the colon, rectum and anus, part I: clinical classification. Jpn J Surg. 1983;13(6):557-573.
116. Greene FL, Stewart AK, Norton HJ. New tumor-node-metastasis staging strategy for node-positive (stage III) rectal cancer: an analysis. J Clin Oncol. 2004;22(10):1778-1784.
117. Messerini L, Cianchi F, Cortesini C, Comin CE. Incidence and prognostic significance of occult tumor cells in lymph nodes from patients with stage IIA colorectal carcinoma. Hum Pathol. 2006;37(10):1259-1267.
118. Verrill C, Carr NJ, Wilkinson-Smith E, Seel EH. Histopathological assessment of lymph nodes in colorectal carcinoma: does triple levelling detect significantly more metastases? J Clin Pathol. 2004;57(11):1165-1167.
119. 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(2):209-216.
120. 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(5):660-665.
121. Goldstein NS. Lymph node recoveries from 2427 pT3 colorectal resection specimens spanning 45 years: recommendations for a minimum number of recovered lymph nodes based on predictive probabilities. Am J Surg Pathol. 2002;26(2):179-189.
122. Tekkis PP, Smith JJ, Heriot AG, Darzi AW, Thompson MR, Stamatakis JD. A national study on lymph node retrieval in resectional surgery for colorectal cancer. Dis Colon Rectum. 2006;49(11):1673-1683.
123. National Quality Forum endorses consensus standards for diagnosis and treatment of breast and colorectal cancer. http://www.qualityforum.org/Press- Releases.aspx. Published 2007. Accessed February 20, 2009.
124. Murphy J, Pocard M, Jass JR, O'Sullivan GC, Lee G, Talbot IC. Number and size of lymph nodes recovered from dukes B rectal cancers: correlation with prognosis and histologic antitumor immune response. Dis Colon Rectum. 2007;50(10):1526-1534.
125. Sarli L, Bader G, Iusco D, et al. Number of lymph nodes examined and prognosis of TNM stage II colorectal cancer. Eur J Cancer. 2005;41(2):272-279.
126. 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(22):3570-3575.
127. 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(6):433-441.
128. Morris EJ, Maughan NJ, Forman D, Quirke P. Identifying stage III colorectal cancer patients: the influence of the patient, surgeon, and pathologist. J Clin Oncol. 2007;25(18):2573-2579.
129. Miller EA, Woosley J, Martin CF, Sandler RS. Hospital-to-hospital variation in lymph node detection after colorectal resection. Cancer. 2004;101(5):1065-1071.
130. Larson DW, Marcello PW, Larach SW, et al. Surgeon volume does not predict outcomes in the setting of technical credentialing: results from a randomized trial in colon cancer. Ann Surg. 2008;248(5):746-750.
131. Truong C, Wong JH, Lum SS, Morgan JW, Roy-Chowdhury S. The impact of hospital volume on the number of nodes retrieved and outcome in colorectal cancer. Am Surg. 2008;74(10):944-947.
132. Rieger NA, Barnett FS, Moore JW, et al. Quality of pathology reporting impacts on lymph node yield in colon cancer. J Clin Oncol. 2007;25(4):463-464.
133. Brown HG, Luckasevic TM, Medich DS, Celebrezze JP, Jones SM. Efficacy of manual dissection of lymph nodes in colon cancer resections. Mod Pathol. 2004;17(4):402-406.
134. Markl B, Kerwel TG, Wagner T, Anthuber M, Arnholdt HM. Methylene blue injection into the rectal artery as a simple method to improve lymph node harvest in rectal cancer. Mod Pathol. 2007;20(7):797-801.
135. Berger AC, Sigurdson ER, LeVoyer T, et al. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol. 2005;23(34):8706-8712.
136. Lee HY, Choi HJ, Park KJ, et al. Prognostic significance of metastatic lymph node ratio in node-positive colon carcinoma. Ann Surg Oncol. 2007;14(5):1712-1717.
137. Peschaud F, Benoist S, Julié C, et al. The ratio of metastatic to examined lymph nodes is a powerful independent prognostic factor in rectal cancer. Ann Surg. 2008;248(6):1067-1073.
138. Peng J, Xu Y, Guan Z, et al. Prognostic significance of the metastatic lymph node ratio in node-positive rectal cancer. Ann Surg Oncol. 2008;15(11):3118-3123.
139. Rosenberg R, Friederichs J, Schuster T, et al. Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3026 patients over a 25-year time period. Ann Surg. 2008;248(6):968-978.
140. Puppa G, Maisonneuve P, Sonzogni A, et al. Independent prognostic value of fascin immunoreactivity in stage III-IV colonic adenocarcinoma. Br J Cancer. 2007;96(7):1118-1126.
141. Poston G, Adam R, Vauthey JN. Downstaging or downsizing: time for a new staging system in advanced colorectal cancer? J Clin Oncol. 2006;24(18):2702- 2706.
142. Nagashima I, Takada T, Nagawa H, Muto T, Okinaga K. Proposal of a new and simple staging system of colorectal liver metastasis. World J Gastroenterol. 2006;12(43):6961-6965.
143. Poston GJ, Figueras J, Giuliante F, et al. Urgent need for a new staging system in advanced colorectal cancer. J Clin Oncol. 2008;26(29):4828-4833.
144. de Haas RJ, Wicherts DA, Flores E, Azoulay D, Castaing D, Adam R. R1 resection by necessity for colorectal liver metastases: is it still a contraindication to surgery? Ann Surg. 2008;248(4):626-637.
145. Nagtegaal ID, Gosens MJ, Marijnen CA, Rutten HJ, van de Velde CJ, van Krieken JH. Combinations of tumor and treatment parameters are more discriminative for prognosis than the present TNM system in rectal cancer. J Clin Oncol. 2007;25(13):1647-1650.
146. Quirke P, Morris E. Reporting colorectal cancer. Histopathology. 2007;50(1):103-112.
147. Rutten H, Sebag-Montefiore R, Glynne-Jones R, et al. Capecitabine, oxaliplatin, radiotherapy, and excision (CORE) in patients with MRI-defined locally advanced rectal adenocarcinoma: results of an international multicenter phase II study [abstract]. J Clin Oncol. 2006;24(suppl):3528.
148. Ryan R, Gibbons D, Hyland JM, et al. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology. 2005;47(2):141-146.
149. Mandard AM, Dalibard F, Mandard JC, et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma: clinicopathologic correlations. Cancer. 1994;73(11):2680-2686.
150. Dworak O, Keilholz L, Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy. Int J Colorectal Dis. 1997;12(1):19-23.
151. Bouzourene H, Bosman FT, Seelentag W, Matter M, Coucke P. Importance of tumor regression assessment in predicting the outcome in patients with locally advanced rectal carcinoma who are treated with preoperative radiotherapy. Cancer. 2002;94(4):1121-1130.
152. Suarez J, Vera R, Balen E, et al. Pathologic response assessed by Mandard grade is a better prognostic factor than down staging for disease-free survival after preoperative radiochemotherapy for advanced rectal cancer. Colorectal Dis. 2008;10(6):563-568.
153. Rodel C, Martus P, Papadoupolos T, et al. Prognostic significance of tumor regression after preoperative chemoradiotherapy for rectal cancer. J Clin Oncol. 2005;23(34):8688-8696.
154. Losi L, Luppi G, Gavioli M, et al. Prognostic value of Dworak grade of regression (GR) in patients with rectal carcinoma treated with preoperative radiochemotherapy. Int J Colorectal Dis. 2006;21(7):645-651.
155. Quah HM, Chou JF, Gonen M, et al. Pathologic stage is most prognostic of disease-free survival in locally advanced rectal cancer patients after preoperative chemoradiation. Cancer. 2008;113(1):57-64.
156. Pucciarelli S, Toppan P, Friso ML, et al. Complete pathologic response following preoperative chemoradiation therapy for middle to lower rectal cancer is not a prognostic factor for a better outcome. Dis Colon Rectum. 2004;47(11):1798-1807.
157. Gosens MJ, Klaassen RA, Tan-Go I, et al. Circumferential margin involvement is the crucial prognostic factor after multimodality treatment in patients with locally advanced rectal carcinoma. Clin Cancer Res. 2007;13(22, pt 1):6617-6623.
158. Leibold T, Shia J, Ruo L, et al. Prognostic implications of the distribution of lymph node metastases in rectal cancer after neoadjuvant chemoradiotherapy. J Clin Oncol. 2008;26(13):2106-2111.
159. Wichmann MW, Muller C, Meyer G, et al. Effect of preoperative radiochemotherapy on lymph node retrieval after resection of rectal cancer. Arch Surg. 2002;137(2):206-210. (Pubitemid 34142139)
160. Greene FL, Brierley J, O'Sullivan B, Sobin LH, Wittekind C. On the use and abuse of X in the TNM classification. Cancer. 2005;103(3):647-649.
161. Rubbia-Brandt L, Giostra E, Brezault C, et al. Importance of histological tumor response assessment in predicting the outcome in patients with colorectal liver metastases treated with neo-adjuvant chemotherapy followed by liver surgery. Ann Oncol. 2007;18(2):299-304.
162. Blazer DG III, Kishi Y, Maru DM, et al. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol. 2008;26(33):5344-5351.
163. Wittekind C, Compton CC, Greene FL, Sobin LH. TNM residual tumor classification revisited. Cancer. 2002;94(9):2511-2516.
164. Nagtegaal ID, Marijnen CA, Kranenbarg EK, van de Velde CJ, van Krieken JH. Circumferential margin involvement is still an important predictor of local recurrence in rectal carcinoma: not one millimeter but two millimeters is the limit. Am J Surg Pathol. 2002;26(3):350-357.
165. Nagtegaal ID, Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer? J Clin Oncol. 2008;26(2):303-312.
166. Quirke P, Durdey P, Dixon MF, Williams NS. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection: histopathological study of lateral tumour spread and surgical excision. Lancet. 1986;2(8514):996-999.
167. Wibe A, Rendedal PR, Svensson E, et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer. Br J Surg. 2002;89(3):327-334.
168. Hermanek P, Hermanek P, Hohenberger W, Klimpfinger M, Kockerling F, Papadopoulos T. The pathological assessment of mesorectal excision: implications for further treatment and quality management. Int J Colorectal Dis. 2003;18(4):335-341.
169. Nagtegaal ID, van de Velde CJ, van der Worp E, Kapiteijn E, Quirke P, van Krieken JH. Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol. 2002;20(7):1729-1734.
170. Scott N, Jamali A, Verbeke C, Ambrose NS, Botterill ID, Jayne DG. Retroperitoneal margin involvement by adenocarcinoma of the caecum and ascending colon: what does it mean? Colorectal Dis. 2008;10(3):289-293.
171. Bateman AC, Carr NJ, Warren BF. The retroperitoneal surface in distal caecal and proximal ascending colon carcinoma: the Cinderella surgical margin? J Clin Pathol. 2005;58(4):426-428.
172. Tejpar S. The multidisciplinary management of gastrointestinal cancer: the use of molecular markers in the diagnosis and treatment of colorectal cancer. Best Pract Res Clin Gastroenterol. 2007;21(6):1071-1087.
173. NCCN updates guidelines for colorectal cancer. National Comprehensive Cancer Network Web Site. http://www.nccn.org/about/news/newsinfo.asp?NewsID5194. Published November 3, 2008. Accessed February 2, 2009.
174. Popat S, Hubner R, Houlston RS. Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol. 2005;23(3):609-618.
175. Lanza G, Gafa R, Santini A, Maestri I, Guerzoni L, Cavazzini L.
176. Funaioli C, Pinto C, Mutri V, Di FF, Ceccarelli C, Martoni AA. Does biomolecular characterization of stage II/III colorectal cancer have any prognostic value? Clin Colorectal Cancer. 2006;6(1):38-45.
177. Bendardaf R, Lamlum H, Ristamaki R, Korkeila E, Syrjanen K, Pyrhonen S. Mismatch repair status is a predictive factor of tumour response to 5-fluorouracil and irinotecan chemotherapy in patients with advanced colorectal cancer. Tumour Biol. 2007;28(4):212-220.
178. Jover R, Zapater P, Castells A, et al. The efficacy of adjuvant chemotherapy with 5-fluorouracil in colorectal cancer depends on the mismatch repair status. Eur J Cancer. 2008;45(3):365-373.
179. Jass JR. Molecular heterogeneity of colorectal cancer: implications for cancer control. Surg Oncol. 2007;16(suppl 1):S7-S9.
180. Nannini M, Pantaleo MA, Maleddu A, Astolfi A, Formica S, Biasco G. Gene expression profiling in colorectal cancer using microarray technologies: results and perspectives. Cancer Treat Rev. 2009;35(3):201-209.
181. Garman KS, Acharya CR, Edelman E, et al. A genomic approach to colon cancer risk stratification yields biologic insights into therapeutic opportunities. Proc Natl Acad Sci U S A. 2008;105(49):19432-19437.
182. Uen YH, Lin SR, Wu DC, et al. Prognostic significance of multiple molecular markers for patients with stage II colorectal cancer undergoing curative resection. Ann Surg. 2007;246(6):1040-1046.
183. Ogino S, Nosho K, Kirkner GJ, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut. 2009;58(1):90-96.
184. Xu F, Wang F, Di M, et al. Classification based on the combination of molecular and pathologic predictors is superior to molecular classification on prognosis in colorectal carcinoma. Clin Cancer Res. 2007;13(17):5082-5088.
185. Zlobec I, Minoo P, Baumhoer D, et al. Multimarker phenotype predicts adverse survival in patients with lymph node-negative colorectal cancer. Cancer. 2008;112(3):495-502.
186. Zlobec I, Baker K, Terracciano LM, Lugli A. RHAMM, p21 combined phenotype identifies microsatellite instability-high colorectal cancers with a highly adverse prognosis. Clin Cancer Res. 2008;14(12):3798-3806.
187. Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology. 2007;50(1):113-130.
188. Zlobec I, Baker K, Minoo P, Jass JR, Terracciano L, Lugli A. Nodenegative colorectal cancer at high risk of distant metastasis identified by combined analysis of lymph node status, vascular invasion, and Raf-1 kinase inhibitor protein expression. Clin Cancer Res. 2008;14(1):143-148.