TNM staging system of colorectal carcinoma: Surgical pathology of the seventh edition

Diagnostic Histopathology

Volumn 17, Issue 6, 2011, Pages 243-262

  Puppa, Giacomo ^a  

^a 'G Fracastoro' City Hospital   (Italy)

Author keywords

Colorectal cancer; Staging; TNM

Indexed keywords

ANTINEOPLASTIC AGENT; APC PROTEIN; B RAF KINASE; K RAS PROTEIN; PROTEIN P53;

ARTICLE; CANCER CHEMOTHERAPY; CANCER CLASSIFICATION; CANCER GRADING; CANCER GROWTH; CANCER INVASION; CANCER LOCALIZATION; CANCER RADIOTHERAPY; CANCER STAGING; CANCER SURVIVAL; CANCER TISSUE; COLORECTAL CARCINOMA; DISEASE SEVERITY; DISTANT METASTASIS; GENE MUTATION; HISTOPATHOLOGY; HUMAN; LYMPH NODE METASTASIS; LYMPHATIC SYSTEM; LYMPHOCYTIC INFILTRATION; PATHOLOGIST; RECTUM CANCER; SURGICAL ANATOMY; TISSUE STRUCTURE; VEIN;

EID: 79958170918     PISSN: 17562317     EISSN: 18767621     Source Type: Journal    
DOI: 10.1016/j.mpdhp.2011.03.006     Document Type: Article

References (231)

1. Ferlay J., Shin H.R., Bray F., Forman D., Mathers C., Parkin D.M. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 2010, 127:2893-2917.
2. Dukes C.E. The classification of cancer of the rectum. J Pathol Bacteriol 1932, 35:323-332.
3. Jass J.R., Morson B.C. Reporting colorectal cancer. J Clin Pathol 1987, 40:1016-1023.
4. Jass J.R., Ajioka Y., Allen J.P., et al. Assessment of invasive growth pattern and lymphocytic infiltration in colorectal cancer. Histopathology 1996, 28:543-548.
5. Sobin L.H., Compton C.C. TNM seventh edition: what's new, what's changed: communication from the International Union against Cancer and the American Joint Committee on Cancer. Cancer 2010, 116:5336-5339.
6. Compton C.C., Greene F.L. The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 2004, 54:295-308.
7. Gospodarowicz M.K., Miller D., Groome P.A., Greene F.L., Logan P.A., Sobin L.H. The process for continuous improvement of the TNM classification. Cancer 2004, 100:1-5.
8. Gunderson L.L., Jessup J.M., Sargent D.J., Greene F.L., Stewart A. Revised tumor and node categorization for rectal cancer based on surveillance, epidemiology, and end results and rectal pooled analysis outcomes. J Clin Oncol 2010, 28:256-263.
9. Gunderson L.L., Jessup J.M., Sargent D.J., Greene F.L., Stewart A.K. Revised TN categorization for colon cancer based on national survival outcomes data. J Clin Oncol 2010, 28:264-271.
10. Greene F.L., Sobin L.H. The staging of cancer: a retrospective and prospective appraisal. CA Cancer J Clin 2008, 58:180-190.
11. Edge S.B., Compton C.C. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 2010, 17:1471-1474.
12. Hassan C., Zullo A., Risio M., Rossini F.P., Morini S. Histologic risk factors and clinical outcome in colorectal malignant polyp: a pooled-data analysis. Dis Colon Rectum 2005, 48:1588-1596.
13. Ueno H., Mochizuki H., Hashiguchi Y., et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology 2004, 127:385-394.
14. Morson B.C. Histological criteria for local excision. Br J Surg 1985, 72(suppl):S53-S54.
15. Williams B., Saunders B.P. The rationale for current practice in the management of malignant colonic polyps. Endoscopy 1993, 25:469-474.
16. Cooper H.S., Deppisch L.M., Kahn E.I., et al. Pathology of the malignant colorectal polyp. Hum Pathol 1998, 29:15-26.
17. Haggitt R.C., Glotzbach R.E., Soffer E.E., Wruble L.D. Prognostic factors in colorectal carcinomas arising in adenomas: implications for lesions removed by endoscopic polypectomy. Gastroenterology 1985, 89:328-336.
18. Kikuchi R., Takano M., Takagi K., et al. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 1995, 38:1286-1295.
19. Merkel S., Mansmann U., Siassi M., Papadopoulos T., Hohenberger W., Hermanek P. The prognostic inhomogeneity in pT3 rectal carcinomas. Int J Colorectal Dis 2001, 16:298-304.
20. Bori R., Sejben I., Svebis M., et al. Heterogeneity of pT3 colorectal carcinomas according to the depth of invasion. Pathol Oncol Res 2009, 15:527-532.
21. Wittekind C., Henson D.E., Hutter R.V., Sobin L.H. TNM supplement. A commentary on uniform use 2003, John Wiley & Sons, Hoboken, New Jersey. 3rd edn.
22. Wittekind C., Henson D.E., Hutter R.V., Sobin L.H. TNM supplement. A commentary on uniform use 2001, Wiley-Liss, New York. 2nd edn.
23. Miyoshi M., Ueno H., Hashiguchi Y., Mochizuki H., Talbot I.C. Extent of mesorectal tumor invasion as a prognostic factor after curative surgery for T3 rectal cancer patients. Ann Surg 2006, 243:492-498.
24. Cianchi F., Messerini L., Comin C.E., et al. Pathologic determinants of survival after resection of T3N0 (Stage IIA) colorectal cancer: proposal for a new prognostic model. Dis Colon Rectum 2007, 50:1332-1341.
25. Compton C.C. Key issues in reporting common cancer specimens: problems in pathologic staging of colon cancer. Arch Pathol Lab Med 2006, 130:318-324.
26. Compton C., Fenoglio-Preiser C.M., Pettigrew N., Fielding L.P. American Joint Committee on Cancer prognostic factors consensus conference: colorectal working group. Cancer 2000, 88:1739-1757.
27. Compton C.C. For the members of the Cancer Committee, College of American Pathologists. Colon and rectum January 2005, Updated, College of American Pathologists, accessed 30 Sep 2005. http://www.cap.org/apps/docs/cancer_protocols/2005/colonrectum05_ckw.pdf.
28. TNM classification of malignant tumors 2002, Wiley-Liss, New York. 6th edn. L.H. Sobin, C. Wittekind (Eds.).
29. Shepherd N.A., Baxter K.J., Love S.B. The prognostic importance of peritoneal involvement in colonic cancer: a prospective evaluation. Gastroenterology 1997, 112:1096-1102.
30. Keshava A., Chapuis P.H., Chan C., Lin B.P., Bokey E.L., Dent O.F. 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, 9:609-618.
31. Izbicki J.R., Hosch S.B., Knoefel W.T., Passlick B., Bloechle C., Broelsch C.E. Extended resections are beneficial for patients with locally advanced colorectal cancer. Dis Colon Rectum 1995, 38:1251-1256.
32. Oh S.Y., Kim Y.B., Paek O.J., Suh K.W. Contiguous invasion per se does not affect prognosis in colon cancer. J Surg Oncol 2009, 99:71-74.
33. Croner R.S., Merkel S., Papadopoulos T., Schellerer V., Hohenberger W., Goehl J. Multivisceral resection for colon carcinoma. Dis Colon Rectum 2009, 52:1381-1386.
34. Washington K., Berlin J., Branton P., et al. Protocol for the examination of specimens from patients with primary carcinomas of the colon and rectum July 2008, College of American Pathologists, accessed 5 Sep 2008. http://www.cap.org/apps/docs/committees/cancer/cancer_protocols/2008/colonrectum08_pw.pdf.
35. Washington M.K., Berlin J., Branton P.A., et al. Protocol for the examination of specimens from patients with primary carcinomas of the colon and rectum. Arch Pathol Lab Med 2008, 132:1182-1193.
36. TNM classification of malignant tumors 2009, Wiley-Blackwell, New York. 7th edn. L.H. Sobin, M.K. Gospodarowicz, C. Wittekind (Eds.).
37. Ludeman L., Shepherd N.A. Serosal involvement in gastrointestinal cancer: its assessment and significance. Histopathology 2005, 47:123-131.
38. Stewart C., Hillery S., Havlat M. Serosal involvement in colorectal carcinoma. Histopathology 2006, 49:435-437.
39. Compton C.C. Colorectal carcinoma: diagnostic, prognostic, and molecular features. Mod Pathol 2003, 16:376-388.
40. Kojima M., Nakajima K., Ishii G., Saito N., Ochiai A. Peritoneal elastic laminal invasion of colorectal cancer: the diagnostic utility and clinicopathologic relationship. Am J Surg Pathol 2010, 34:1351-1360.
41. Puppa G., Shepherd N.A., Sheahan K., Stewart C.J. Peritoneal elastic lamina invasion in colorectal cancer: the answer to a controversial area of pathology?. Am J Surg Pathol 2011, 35:465-468.
42. 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, 92:2754-2759.
43. Greene F.L., Stewart A.K., Norton H.J. A new TNM staging strategy for node-positive (stage III) colon cancer: an analysis of 50,042 patients. Ann Surg 2002, 236:416-421.
44. Lagarde S.M., Ten Kate F.J., de Boer D.J., Busch O.R., Obertop H., van Lanschot J.J. Extracapsular lymph node involvement in node-positive patients with adenocarcinoma of the distal esophagus or gastroesophageal junction. Am J Surg Pathol 2006, 30:171-176.
45. 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, 137:511-517.
46. 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, 44:1838-1844.
47. 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, 20:843-855.
48. Messerini L., Cianchi F., Cortesini C., Comin C.E. Incidence and prognostic significance of occult tumor cells in lymph nodes from patients with stage IIA colorectal carcinoma. Hum Pathol 2006, 37:1259-1267.
49. Verrill C., Carr N.J., Wilkinson-Smith E., Seel E.H. Histopathological assessment of lymph nodes in colorectal carcinoma: does triple levelling detect significantly more metastases?. J Clin Pathol 2004, 57:1165-1167.
50. TNM classification of malignant tumors 1987, Springer-Verlag, New York. 4th edn. P. Hermanek, L.H. Sobin (Eds.).
51. TNM classification of malignant tumors 1997, Wiley-Liss, New York. 5th edn. L.H. Sobin, C. Wittekind (Eds.).
52. Dukes C.E., Bussey H.J. The spread of rectal cancer and its effect on prognosis. Br J Cancer 1958, 12:309-320.
53. 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, 183:611-615.
54. Kim J.C., Lee K.H., Yu C.S., et al. The clinicopathological significance of inferior mesenteric lymph node metastasis in colorectal cancer. Eur J Surg Oncol 2004, 30:271-279.
55. Newland R.C., Dent O.F., Lyttle M.N., Chapuis P.H., Bokey E.L. Pathologic determinants of survival associated with colorectal cancer with lymph node metastases. A multivariate analysis of 579 patients. Cancer 1994, 73:2076-2082.
56. Ueno H., Mochizuki H., Hashiguchi Y., Hase K. Prognostic determinants of patients with lateral nodal involvement by rectal cancer. Ann Surg 2001, 234:190-197.
57. Vaccaro C.A., Bonadeo F.A., Benati M.L., et al. Colorectal cancer staging: reappraisal of N/PN classification. Dis Colon Rectum 2004, 47:66-69.
58. Hermanek P., Guggenmoos-Holzmann I., Gall F.P. Prognostic factors in rectal carcinoma. A contribution to the further development of tumor classification. Dis Colon Rectum 1989, 32:593-599.
59. Bruch H.P., Schwandner O., Schiedeck T.H., Roblick U.J. Actual standards and controversies on operative technique and lymph-node dissection in colorectal cancer. Langenbecks Arch Surg 1999, 384:167-175.
60. Steup W.H., Moriya Y., van de Velde C.J. Patterns of lymphatic spread in rectal cancer. A topographical analysis on lymph node metastases. Eur J Cancer 2002, 38:911-918.
61. 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, 92:756-763.
62. 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, 93:609-615.
63. West N.P., Hohenberger W., Weber K., Perrakis A., Finan P.J., Quirke P. Complete mesocolic excision with central vascular ligation produces an oncologically superior specimen compared with standard surgery for carcinoma of the colon. J Clin Oncol 2010, 28:272-278.
64. General rules for clinical and pathological studies on cancer of the colon, rectum and anus. Part I. Clinical classification. Japanese Research Society for Cancer of the Colon and Rectum. Jpn J Surg 1983, 13:557-573.
65. Jass J.R., O'Brien J., Riddell R.H., Snover D.C. Recommendations for the reporting of surgically resected specimens of colorectal carcinoma: Association of Directors of Anatomic and Surgical Pathology. Am J Clin Pathol 2008, 129:13-23.
66. Goldstein N.S., Sanford W., Coffey M., Layfield L.J. 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, 106:209-216.
67. Tsai H.L., Lu C.Y., Hsieh J.S., et al. The prognostic significance of total lymph node harvest in patients with T2-4N0M0 colorectal cancer. J Gastrointest Surg 2007, 11:660-665.
68. Goldstein N.S. 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, 26:179-189.
69. Tekkis P.P., Smith J.J., Heriot A.G., Darzi A.W., Thompson M.R., Stamatakis J.D. A national study on lymph node retrieval in resectional surgery for colorectal cancer. Dis Colon Rectum 2006, 49:1673-1683.
70. National Quality Forum endorses consensus standards for diagnosis and treatment of breast and colorectal cancer 2007, accessed 20 Feb 2009. http://www.qualityforum.org/PressReleases.aspx.
71. Murphy J., Pocard M., Jass J.R., O'Sullivan G.C., Lee G., Talbot I.C. Number and size of lymph nodes recovered from dukes B rectal cancers: correlation with prognosis and histologic antitumor immune response. Dis Colon Rectum 2007, 50:1526-1534.
72. 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, 41:272-279.
73. Johnson P.M., Porter G.A., Ricciardi R., Baxter N.N. Increasing negative lymph node count is independently associated with improved long-term survival in stage IIIB and IIIC colon cancer. J Clin Oncol 2006, 24:3570-3575.
74. Chang G.J., Rodriguez-Bigas M.A., Skibber J.M., Moyer V.A. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 2007, 99:433-441.
75. Ogino S., Nosho K., Irahara N., et al. Negative lymph node count is associated with survival of colorectal cancer patients, independent of tumoral molecular alterations and lymphocytic reaction. Am J Gastroenterol 2010, 105:420-433.
76. Morris E.J., Maughan N.J., Forman D., Quirke P. Identifying stage III colorectal cancer patients: the influence of the patient, surgeon, and pathologist. J Clin Oncol 2007, 25:2573-2579.
77. Chou J.F., Row D., Gonen M., Liu Y.H., Schrag D., Weiser M.R. Clinical and pathologic factors that predict lymph node yield from surgical specimens in colorectal cancer: a population-based study. Cancer 2010, 116:2560-2570.
78. Eveno C., Nemeth J., Soliman H., et al. Association between a high number of isolated lymph nodes in T1 to T4 N0M0 colorectal cancer and the microsatellite instability phenotype. Arch Surg 2010, 145:12-17.
79. Miller E.A., Woosley J., Martin C.F., Sandler R.S. Hospital-to-hospital variation in lymph node detection after colorectal resection. Cancer 2004, 101:1065-1071.
80. Larson D.W., Marcello P.W., Larach S.W., 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, 248:746-750.
81. Truong C., Wong J.H., Lum S.S., Morgan J.W., Roy-Chowdhury S. The impact of hospital volume on the number of nodes retrieved and outcome in colorectal cancer. Am Surg 2008, 74:944-947.
82. Rieger N.A., Barnett F.S., Moore J.W., et al. Quality of pathology reporting impacts on lymph node yield in colon cancer. J Clin Oncol 2007, 25:463-464.
83. Brown H.G., Luckasevic T.M., Medich D.S., Celebrezze J.P., Jones S.M. Efficacy of manual dissection of lymph nodes in colon cancer resections. Mod Pathol 2004, 17:402-406.
84. Hernanz F., Garcia-Somacarrera E., Fernandez F. The assessment of lymph nodes missed in mesenteric tissue after standard dissection of colorectal cancer specimens. Colorectal Dis 2010, 12:e57-e60.
85. Markl B., Kerwel T.G., Wagner T., Anthuber M., Arnholdt H.M. Methylene blue injection into the rectal artery as a simple method to improve lymph node harvest in rectal cancer. Mod Pathol 2007, 20:797-801.
86. Parkash V., Bifulco C., Feinn R., Concato J., Jain D. To count and how to count, that is the question: interobserver and intraobserver variability among pathologists in lymph node counting. Am J Clin Pathol 2010, 134:42-49.
87. Berger A.C., Sigurdson E.R., LeVoyer T., et al. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol 2005, 23:8706-8712.
88. Lee H.Y., Choi H.J., Park K.J., et al. Prognostic significance of metastatic lymph node ratio in node-positive colon carcinoma. Ann Surg Oncol 2007, 14:1712-1717.
89. Frederique P., Stephane B., Catherine J., et al. The ratio of metastatic to examined lymph nodes is a powerful independent prognostic factor in rectal cancer. Ann Surg 2008, 248:1067-1073.
90. 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, 15:3118-3123.
91. 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, 248:968-978.
92. Rosenberg R., Engel J., Bruns C., et al. The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients. Ann Surg 2010, 251:1070-1078.
93. Derwinger K., Carlsson G., Ekman T. Defining stage III disease in colorectal cancer-aspects on treatment and evaluation of survival. J Surg Oncol 2010, 102:424-427.
94. Poston G., Adam R., Vauthey J.N. Downstaging or Downsizing: time for a new staging system in advanced colorectal cancer?. J Clin Oncol 2006, 24:2702-2706.
95. 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, 12:6961-6965.
96. Poston G.J., Figueras J., Giuliante F., et al. Urgent need for a new staging system in advanced colorectal cancer. J Clin Oncol 2008, 26:4828-4833.
97. Greene F.L., Brierley J., O'Sullivan B., Sobin L.H., Wittekind C. On the use and abuse of X in the TNM classification. Cancer 2005, 103:647-649.
98. Brent A., Talbot R., Coyne J., Nash G. Should indeterminate lung lesions reported on staging CT scans influence the management of patients with colorectal cancer?. Colorectal Dis 2007, 9:816-818.
99. Lim G.H., Koh D.C., Cheong W.K., Wong K.S., Tsang C.B. Natural history of small, " indeterminate" hepatic lesions in patients with colorectal cancer. Dis Colon Rectum 2009, 52:1487-1491.
100. Christoffersen M.W., Bulut O., Jess P. The diagnostic value of indeterminate lung lesions on staging chest computed tomographies in patients with colorectal cancer. Dan Med Bull 2010, 57. A4093.
101. Liebig C., Ayala G., Wilks J., et al. Perineural invasion is an independent predictor of outcome in colorectal cancer. J Clin Oncol 2009, 27:5131-5137.
102. Poeschl E.M., Pollheimer M.J., Kornprat P., et al. Perineural invasion: correlation with aggressive phenotype and independent prognostic variable in both colon and rectum cancer. J Clin Oncol 2010, 28:e358-e360.
103. Wittekind C., Compton C.C., Greene F.L., Sobin L.H. TNM residual tumor classification revisited. Cancer 2002, 94:2511-2516.
104. Wittekind C., Compton C., Quirke P., et al. A uniform residual tumor (R) classification: integration of the R classification and the circumferential margin status. Cancer 2009, 115:3483-3488.
105. Colon and Rectum. AJCC cancer staging handbook 2010, 173-206. Springer, New York, NY. 7th edn. S.B. Edge, D.R. Byrd, C.C. Compton, A.G. Fritz, F.L. Greene, A.E. Trotti (Eds.).
106. Colon and Rectum. AJCC cancer staging manual 2010, 143-164. Springer, New York, NY. 7th edn. S.B. Edge, D.R. Byrd, C.C. Compton, A.G. Fritz, F.L. Greene, A.E. Trotti (Eds.).
107. Puppa G., Bortolasi L., Colombari R., Sheahan K. Residual tumor (R) classification in colorectal cancer: reduced, expanded, or not uniform?. Arch Pathol Lab Med 2011, 135:288.
108. Compton C.C., Sobin L.H. In reply. Arch Pathol Lab Med 2011, 135:289.
109. Merkel S., Wein A., Gunther K., Papadopoulos T., Hohenberger W., Hermanek P. High-risk groups of patients with Stage II colon carcinoma. Cancer 2001, 92:1435-1443.
110. Turner R.R., Li C., Compton C.C. Newer pathologic assessment techniques for colorectal carcinoma. Clin Cancer Res 2007, 13:6871s-6876s.
111. Compton C.C. Optimal pathologic staging: defining stage II disease. Clin Cancer Res 2007, 13:6862s-6870s.
112. Quah H.M., Chou J.F., Gonen M., et al. Identification of patients with high-risk stage II colon cancer for adjuvant therapy. Dis Colon Rectum 2008, 51:503-507.
113. Zlobec I., Lugli A. Prognostic and predictive factors in colorectal cancer. J Clin Pathol 2008, 61:561-569.
114. Epithelial neoplasia of the intestines. Tumors of the intestines. third series ed 2003, Armed Forces Institute of Pathology. J. Rosai, L.H. Sobin (Eds.).
115. Ueno H., Hashiguchi Y., Kajiwara Y., et al. Proposed objective criteria for " grade 3" in early invasive colorectal cancer. Am J Clin Pathol 2010, 134:312-322.
116. Ueno H., Mochizuki H., Hashiguchi Y., et al. Histological grading of colorectal cancer: a simple and objective method. Ann Surg 2008, 247:811-818.
117. Washington M.K., Berlin J., Branton P., et al. Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med 2009, 133:1539-1551.
118. Haupt B., Ro J.Y., Schwartz M.R., Shen S.S. Colorectal adenocarcinoma with micropapillary pattern and its association with lymph node metastasis. Mod Pathol 2007, 20:729-733.
119. Kim M.J., Hong S.M., Jang S.J., et al. Invasive colorectal micropapillary carcinoma: an aggressive variant of adenocarcinoma. Hum Pathol 2006, 37:809-815.
120. Xu F., Xu J., Lou Z., et al. Micropapillary component in colorectal carcinoma is associated with lymph node metastasis in T1 and T2 Stages and decreased survival time in TNM stages I and II. Am J Surg Pathol 2009, 33:1287-1292.
121. WHO classification of tumours of the digestive system 2010, World Health Organization. F.T. Bosman, F. Carneiro, R.H. Hruban (Eds.).
122. Ueno H., Murphy J., Jass J.R., Mochizuki H., Talbot I.C. Tumour 'budding' as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 2002, 40:127-132.
123. Wang L.M., Kevans D., Mulcahy H., et al. Tumor budding is a strong and reproducible prognostic marker in T3N0 colorectal cancer. Am J Surg Pathol 2009, 33:134-141.
124. Wang H.S., Liang W.Y., Lin T.C., et al. Curative resection of T1 colorectal carcinoma: risk of lymph node metastasis and long-term prognosis. Dis Colon Rectum 2005, 48:1182-1192.
125. Ueno H., Price A.B., Wilkinson K.H., Jass J.R., Mochizuki H., Talbot I.C. A new prognostic staging system for rectal cancer. Ann Surg 2004, 240:832-839.
126. Prall F., Nizze H., Barten M. Tumour budding as prognostic factor in stage I/II colorectal carcinoma. Histopathology 2005, 47:17-24.
127. 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, 45:628-634.
128. Okuyama T., Oya M., Ishikawa H. Budding as a useful prognostic marker in pT3 well- or moderately-differentiated rectal adenocarcinoma. J Surg Oncol 2003, 83:42-47.
129. Okuyama T., Nakamura T., Yamaguchi M. Budding is useful to select high-risk patients in stage II well-differentiated or moderately differentiated colon adenocarcinoma. Dis Colon Rectum 2003, 46:1400-1406.
130. Hase K., Shatney C., Johnson D., Trollope M., Vierra M. Prognostic value of tumor " budding" in patients with colorectal cancer. Dis Colon Rectum 1993, 36:627-635.
131. Choi H.J., Park K.J., Shin J.S., Roh M.S., Kwon H.C., Lee H.S. Tumor budding as a prognostic marker in stage-III rectal carcinoma. Int J Colorectal Dis 2007, 22:863-868.
132. Nakamura T., Mitomi H., Kanazawa H., Ohkura Y., Watanabe M. Tumor budding as an index to identify high-risk patients with stage II colon cancer. Dis Colon Rectum 2008, 51:568-572.
133. Kazama S., Watanabe T., Ajioka Y., Kanazawa T., Nagawa H. Tumour budding at the deepest invasive margin correlates with lymph node metastasis in submucosal colorectal cancer detected by anticytokeratin antibody CAM5.2. Br J Cancer 2006, 94:293-298.
134. Ogawa T., Yoshida T., Tsuruta T., et al. Tumor budding is predictive of lymphatic involvement and lymph node metastases in submucosal invasive colorectal adenocarcinomas and in non-polypoid compared with polypoid growths. Scand J Gastroenterol 2009, 44:605-614.
135. Zlobec I., Lugli A. Invasive front of colorectal cancer: dynamic interface of pro-/anti-tumor factors. World J Gastroenterol 2009, 15:5898-5906.
136. Zlobec I., Baker K., Minoo P., Hayashi S., Terracciano L., Lugli A. Tumor border configuration added to TNM staging better stratifies stage II colorectal cancer patients into prognostic subgroups. Cancer 2009, 115:4021-4029.
137. Ogino S., Nosho K., Irahara N., et al. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 2009, 15:6412-6420.
138. Jass J.R., Atkin W.S., Cuzick J., et al. The grading of rectal cancer: historical perspectives and a multivariate analysis of 447 cases. Histopathology 1986, 10:437-459.
139. Harrison J.C., Dean P.J., el-Zeky F., Vander Z.R. From Dukes through Jass: pathological prognostic indicators in rectal cancer. Hum Pathol 1994, 25:498-505.
140. Sternberg A., Amar M., Alfici R., Groisman G. Conclusions from a study of venous invasion in stage IV colorectal adenocarcinoma. J Clin Pathol 2002, 55:17-21.
141. Talbot I.C., Ritchie S., Leighton M., Hughes A.O., Bussey H.J., Morson B.C. The clinical significance of invasion of veins by rectal cancer. Br J Surg 1980, 67:439-442.
142. Washington M.K. Colorectal carcinoma: selected issues in pathologic examination and staging and determination of prognostic factors. Arch Pathol Lab Med 2008, 132:1600-1607.
143. Nascimbeni R., Burgart L.J., Nivatvongs S., Larson D.R. Risk of lymph node metastasis in T1 carcinoma of the colon and rectum. Dis Colon Rectum 2002, 45:200-206.
144. Greene F.L. Current TNM staging of colorectal cancer. Lancet Oncol 2007, 8:572-573.
145. Sobin L.H. TNM, sixth edition: new developments in general concepts and rules. Semin Surg Oncol 2003, 21:19-22.
146. Koukourakis M.I., Giatromanolaki A., Sivridis E., Gatter K.C., Harris A.L. For Tumour and Angiogenesis Research Group. Inclusion of vasculature-related variables in the dukes staging system of colon cancer. Clin Cancer Res 2005, 11:8653-8660.
147. Sternberg A., Sibirsky O., Cohen D., Blumenson L.E., Petrelli N.J. Validation of a new classification system for curatively resected colorectal adenocarcinoma. Cancer 1999, 86:782-792.
148. Sternberg A., Sibirsky O., Cohen D., Blumenson L.E., Rodriguez-Bigas M.A., Petrelli N.J. New approach to the substaging of node-positive colorectal adenocarcinoma. Ann Surg Oncol 1999, 6:161-165.
149. Kingston E.F., Goulding H., Bateman A.C. Vascular invasion is underrecognized in colorectal cancer using conventional hematoxylin and eosin staining. Dis Colon Rectum 2007, 50:1867-1872.
150. Littleford S.E., Baird A., Rotimi O., Verbeke C.S., Scott N. Interobserver variation in the reporting of local peritoneal involvement and extramural venous invasion in colonic cancer. Histopathology 2009, 55:407-413.
151. Vass D.G., Ainsworth R., Anderson J.H., Murray D., Foulis A.K. The value of an elastic tissue stain in detecting venous invasion in colorectal cancer. J Clin Pathol 2004, 57:769-772.
152. 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, 59:207-210.
153. Abdulkader M., Abdulla K., Rakha E., Kaye P. Routine elastic staining assists detection of vascular invasion in colorectal cancer. Histopathology 2006, 49:487-492.
154. Inoue T., Mori M., Shimono R., Kuwano H., Sugimachi K. Vascular invasion of colorectal carcinoma readily visible with certain stains. Dis Colon Rectum 1992, 35:34-39.
155. Howlett C.J., Tweedie E.J., Driman D.K. Use of an elastic stain to show venous invasion in colorectal carcinoma: a simple technique for detection of an important prognostic factor. J Clin Pathol 2009, 62:1021-1025.
156. Sejben I., Bori R., Cserni G. Venous invasion demonstrated by orcein staining of colorectal carcinoma specimens is associated with the development of distant metastasis. J Clin Pathol 2010, 63:575-578.
157. Liang P., Nakada I., Hong J.W., et al. Prognostic significance of immunohistochemically detected blood and lymphatic vessel invasion in colorectal carcinoma: its impact on prognosis. Ann Surg Oncol 2007, 14:470-477.
158. Sato T., Ueno H., Mochizuki H., et al. Objective criteria for the grading of venous invasion in colorectal cancer. Am J Surg Pathol 2010, 34:454-462.
159. Talbot I.C., Ritchie S., Leighton M., Hughes A.O., Bussey H.J., Morson B.C. Invasion of veins by carcinoma of rectum: method of detection, histological features and significance. Histopathology 1981, 5:141-163.
160. Blenkinsopp W.K., Stewart-Brown S., Blesovsky L., Kearney G., Fielding L.P. Histopathology reporting in large bowel cancer. J Clin Pathol 1981, 34:509-513.
161. Puppa G., Caneva A., Colombari R. Venous invasion detection in colorectal cancer: which approach, which technique?. J Clin Pathol 2009, 62:102-103.
162. 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, 27:1227-1230.
163. 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, 45:744-749.
164. Nagtegaal I.D., Quirke P. Colorectal tumour deposits in the mesorectum and pericolon; a critical review. Histopathology 2007, 51:141-149.
165. Ueno H., Mochizuki H. Clinical significance of extrabowel skipped cancer infiltration in rectal cancer. Surg Today 1997, 27:617-622.
166. Goldstein N.S., Turner J.R. 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, 88:2228-2238.
167. Wunsch K., Muller J., Jahnig H., Herrmann R.A., Arnholdt H.M., Markl B. Shape is not associated with the origin of pericolonic tumor deposits. Am J Clin Pathol 2010, 133:388-394.
168. Tateishi S., Arima S., Futami K., et al. A clinicopathological investigation of " tumor nodules" in colorectal cancer. Surg Today 2005, 35:377-384.
169. Ratto C., Ricci R., Rossi C., Morelli U., Vecchio F.M., Doglietto G.B. Mesorectal microfoci adversely affect the prognosis of patients with rectal cancer. Dis Colon Rectum 2002, 45:733-742.
170. Stiles T.E., Dean P., Harrison J. Nature and significance of nodular metastases of colonic carcinoma in pericolonic fat [abstract]. Mod Pathol 1995, 8:69A.
171. Lo D.S., Pollett A., Siu L.L., Gallinger S., Burkes R.L. Prognostic significance of mesenteric tumor nodules in patients with stage III colorectal cancer. Cancer 2008, 112:50-54.
172. 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, 127:287-294.
173. 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, 22:410-415.
174. Puppa G. Enhanced pathologic analysis for pericolonic tumor deposits: is it worth it?. Am J Clin Pathol 2010, 134:1019-1021.
175. Belt E.J., van Stijn M.F., Bril H., et al. Lymph node negative colorectal cancers with isolated tumor deposits should be classified and treated as stage III. Ann Surg Oncol 2010, 17:3203-3211.
176. Pramateftakis M.G., Kanellos D., Vrakas G., et al. Progress in rectal cancer staging and treatment. Tech Coloproctol 2010, 14(Suppl 1):S29-S31.
177. Minoo P., Zlobec I., Peterson M., Terracciano L., Lugli A. Characterization of rectal, proximal and distal colon cancers based on clinicopathological, molecular and protein profiles. Int J Oncol 2010, 37:707-718.
178. Bilimoria K.Y., Palis B., Stewart A.K., et al. Impact of tumor location on nodal evaluation for colon cancer. Dis Colon Rectum 2008, 51:154-161.
179. Meguid R.A., Slidell M.B., Wolfgang C.L., Chang D.C., Ahuja N. Is there a difference in survival between right- versus left-sided colon cancers?. Ann Surg Oncol 2008, 15:2388-2394.
180. Frattini M., Balestra D., Suardi S., et al. Different genetic features associated with colon and rectal carcinogenesis. Clin Cancer Res 2004, 10:4015-4021.
181. Li F.Y., Lai M.D. Colorectal cancer, one entity or three. J Zhejiang Univ Sci B 2009, 10:219-229.
182. Suttie S.A., Shaikh I., Mullen R., Amin A.I., Daniel T., Yalamarthi S. Outcome of right and left sided colonic and rectal cancer following surgical resection. Colorectal Dis 2010, doi:10.1111/j.1463-1318.2010.02356.x.
183. Roh M.S., Colangelo L.H., O'Connell M.J., et al. Preoperative multimodality therapy improves disease-free survival in patients with carcinoma of the rectum: NSABP R-03. J Clin Oncol 2009, 27:5124-5130.
184. Ayala D.N., Russo S.M., Blackstock A.W. Multidisciplinary treatment of resectable rectal cancer. Expert Rev Gastroenterol Hepatol 2009, 3:383-394.
185. Nagtegaal I.D., Marijnen C.A., Kranenbarg E.K., van de Velde C.J., van Krieken J.H. 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, 26:350-357.
186. Nagtegaal I.D., Quirke P. What is the role for the circumferential margin in the modern treatment of rectal cancer?. J Clin Oncol 2008, 26:303-312.
187. Quirke P., Durdey P., Dixon M.F., Williams N.S. Local recurrence of rectal adenocarcinoma due to inadequate surgical resection. Histopathological study of lateral tumour spread and surgical excision. Lancet 1986, 2:996-999.
188. Wibe A., Rendedal P.R., Svensson E., et al. Prognostic significance of the circumferential resection margin following total mesorectal excision for rectal cancer. Br J Surg 2002, 89:327-334.
189. Gosens M.J., Klaassen R.A., 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, 13:6617-6623.
190. Nagtegaal I.D., van de Velde C.J., van der Worp E., Kapiteijn E., Quirke P., van Krieken J.H. Macroscopic evaluation of rectal cancer resection specimen: clinical significance of the pathologist in quality control. J Clin Oncol 2002, 20:1729-1734.
191. 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, 18:335-341.
192. Garcia-Granero E., Faiz O., Munoz E., et al. Macroscopic assessment of mesorectal excision in rectal cancer: a useful tool for improving quality control in a multidisciplinary team. Cancer 2009, 115:3400-3411.
193. Quirke P., Morris E. Reporting colorectal cancer. Histopathology 2007, 50:103-112.
194. 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]. Journal of Clinical Oncology 2006, 24(suppl):3528.
195. Ryan R., Gibbons D., Hyland J.M., et al. Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology 2005, 47:141-146.
196. Mandard A.M., Dalibard F., Mandard J.C., et al. Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma. Clinicopathologic correlations. Cancer 1994, 73:2680-2686.
197. Dworak O., Keilholz L., Hoffmann A. Pathological features of rectal cancer after preoperative radiochemotherapy. Int J Colorectal Dis 1997, 12:19-23.
198. Nagtegaal I.D., Gosens M.J., Marijnen C.A., Rutten H.J., van de Velde C.J., van Krieken J.H. Combinations of tumor and treatment parameters are more discriminative for prognosis than the present TNM system in rectal cancer. J Clin Oncol 2007, 25:1647-1650.
199. Roy P., Serra S., Chetty R. Interobserver variability in grading of response to neoadjuvant chemoradiotherapy in rectal adenocarcinomas using five grading Systems [abstract]. Mod Pathol 2010, 23:165A.
200. Bouzourene H., Bosman F.T., 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, 94:1121-1130.
201. 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, 10:563-568.
202. Rodel C., Martus P., Papadoupolos T., et al. Prognostic significance of tumor regression after preoperative chemoradiotherapy for rectal cancer. J Clin Oncol 2005, 23:8688-8696.
203. 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, 21:645-651.
204. Quah H.M., Chou J.F., Gonen M., et al. Pathologic stage is most prognostic of disease-free survival in locally advanced rectal cancer patients after preoperative chemoradiation. Cancer 2008, 113:57-64.
205. Rullier A., Laurent C., Capdepont M., Vendrely V., Bioulac-Sage P., Rullier E. Impact of tumor response on survival after radiochemotherapy in locally advanced rectal carcinoma. Am J Surg Pathol 2010, 34:562-568.
206. Pucciarelli S., Toppan P., Friso M.L., 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, 47:1798-1807.
207. Caricato M., Ausania F., De D.E., et al. Tumor regression in mesorectal lymphnodes after neoadjuvant chemoradiation for rectal cancer. Eur J Surg Oncol 2007, 33:724-728.
208. 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, 18:299-304.
209. Blazer D.G., Kishi Y., Maru D.M., et al. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol 2008, 26:5344-5351.
210. Gervaz P., Rubbia-Brandt L., Andres A., et al. Neoadjuvant chemotherapy in patients with stage IV colorectal cancer: a comparison of histological response in liver metastases, primary tumors, and regional lymph nodes. Ann Surg Oncol 2010, 17:2714-2719.
211. Wichmann M.W., Muller C., Meyer G., et al. Effect of preoperative radiochemotherapy on lymph node retrieval after resection of rectal cancer. Arch Surg 2002, 137:206-210.
212. Marks J.H., Valsdottir E.B., Rather A.A., Nweze I.C., Newman D.A., Chernick M.R. Fewer than 12 lymph nodes can be expected in a surgical specimen after high-dose chemoradiation therapy for rectal cancer. Dis Colon Rectum 2010, 53:1023-1029.
213. 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, 26:2106-2111.
214. Jass J.R. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 2007, 50:113-130.
215. 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, 21:1071-1087.
216. Nannini M., Pantaleo M.A., Maleddu A., Astolfi A., Formica S., Biasco G. Gene expression profiling in colorectal cancer using microarray technologies: results and perspectives. Cancer Treat Rev 2009, 35:201-209.
217. Garman K.S., Acharya C.R., 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, 105:19432-19437.
218. Uen Y.H., Lin S.R., Wu D.C., et al. Prognostic significance of multiple molecular markers for patients with stage II colorectal cancer undergoing curative resection. Ann Surg 2007, 246:1040-1046.
219. Ogino S., Nosho K., Kirkner G.J., et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 2009, 58:90-96.
220. 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, 13:5082-5088.
221. Zlobec I., Minoo P., Baumhoer D., et al. Multimarker phenotype predicts adverse survival in patients with lymph node-negative colorectal cancer. Cancer 2008, 112:495-502.
222. Zlobec I., Baker K., Terracciano L.M., Lugli A. RHAMM, p21 combined phenotype identifies microsatellite instability-high colorectal cancers with a highly adverse prognosis. Clin Cancer Res 2008, 14:3798-3806.
223. Nibbe R.K., Koyuturk M., Chance M.R. An integrative-omics approach to identify functional sub-networks in human colorectal cancer. PLoS Comput Biol 2010, 6. e1000639.
224. Normanno N., Tejpar S., Morgillo F., De L.A., Van C.E., Ciardiello F. Implications for KRAS status and EGFR-targeted therapies in metastatic CRC. Nat Rev Clin Oncol 2009, 6:519-527.
225. Siena S., Sartore-Bianchi A., Di N.F., Balfour J., Bardelli A. Biomarkers predicting clinical outcome of epidermal growth factor receptor-targeted therapy in metastatic colorectal cancer. J Natl Cancer Inst 2009, 101:1308-1324.
226. De R.W., Claes B., Bernasconi D., et al. Effects of KRAS, BRAF, NRAS, and PIK3CA mutations on the efficacy of cetuximab plus chemotherapy in chemotherapy-refractory metastatic colorectal cancer: a retrospective consortium analysis. Lancet Oncol 2010, 11:753-762.
227. Vilar E., Gruber S.B. Microsatellite instability in colorectal cancer - the stable evidence. Nat Rev Clin Oncol 2010, 7:153-162.
228. Shia J., Klimstra D.S., Nafa K., et al. Value of immunohistochemical detection of DNA mismatch repair proteins in predicting germline mutation in hereditary colorectal neoplasms. Am J Surg Pathol 2005, 29:96-104.
229. Overbeek L.I., Ligtenberg M.J., Willems R.W., et al. Interpretation of immunohistochemistry for mismatch repair proteins is only reliable in a specialized setting. Am J Surg Pathol 2008, 32:1246-1251.
230. Walther A., Houlston R., Tomlinson I. Association between chromosomal instability and prognosis in colorectal cancer: a meta-analysis. Gut 2008, 57:941-950.
231. Zlobec I., Baker K., Minoo P., Jass J.R., Terracciano L., Lugli A. Node-negative 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, 14:143-148.