Patologické hodnocení vzorků kolorektálního karcinomu: pokročilé a časné léze
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Annika Resch; Nora I. Schneider; Cord Langner
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Institute of Pathology, Medical University of Graz, Graz, Austria
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Čes.-slov. Patol., 51, 2015, No. 1, p. 12-22
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Reviews Article
U pacientů s lokálně omezeným kolorektálním karcinomem je metodou volby resekce, v některých případech však mohou být časné nádory řešeny také endoskopickým zákrokem bez nutnosti operace. U pokročilých kolorektálních karcinomů hraje při klinickém rozhodování o optimální léčbě zásadní roli přesné určení stadia včetně histopatologického posouzení lymfatických uzlin. Počet odstraněných lymfatických uzlin závisí na rozsahu a kompletnosti chirurgického zákroku, pečlivosti patologa při vyšetření uzlin, ale také na demografických parametrech pacienta, lokalizaci nádoru a jeho biologických vlastnostech. Současná doporučení udávají, že při histopatologickém vyšetření by mělo být standardně nalezeno alespoň 12 uzlin. U nemocných s nádory bez uzlinových metastáz může pro posouzení rizika recidivy sloužit celá řada histologických parametrů - kromě histologické typizace, zhodnocení invaze krevních a lymfatických cév také identifikace bujení nádoru na periferii (tumor budding), nekrózy a kvantifikace protinádorové zánětlivé odpovědi, která byla v několika studiích ověřena jako příznivý prognostický faktor. V případě karcinomu rekta hraje významnou roli postižení radiálního (cirkumferentního) resekčního okraje a rozsah chirurgického odstranění mezorekta. Časný (či povrchový) kolorektální karcinom je definován jako invazivní adenokarcinom postihující, avšak nepřesahující submukózu. Při vyšetření je třeba věnovat pozornost celé řadě znaků, jejichž přítomnost ukazuje na nutnost radikálního chirurgického řešení. Vedle posouzení kompletnosti excize je vyžadováno vyhodnocení parametrů predikujících přítomnost uzlinových metastáz, jako jsou hloubka invaze submukózy, grade a přítomnost dalších rizikových faktorů, jako angioinvaze či tumor budding. Kombinace těchto parametrů umožní stratifikovat nemocné do skupin s nízkým a vysokým rizikem.
Klíčová slova:
kolorektální karcinom – časný kolorektální karcinom – uzlinová metastáza – histopatologické parametry – rizikové faktory – prognóza
Sources
1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014; 64(1): 9-29.
2. Compton CC. Optimal pathologic staging: defining stage II disease. Clin Cancer Re. 2007; 13(22 Pt 2): 6862-6870.
3. Beaton C, Twine CP, Williams GL, Radcliffe AG. Systematic review and meta-analysis of histopathological factors influencing the risk of lymph node metastasis in early colorectal cancer. Colorectal Dis 2013; 15(7): 788-797.
4. Bosch SL, Teerenstra S, de Wilt JH, Cunningham C, Nagtegaal ID. Predicting lymph node metastasis in pT1 colorectal cancer: a systematic review of risk factors providing rationale for therapy decisions. Endoscopy 2013; 45(10): 827-834.
5. 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.
6. Benson AB 3rd, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Engstrom PF, et al. Localized colon cancer, version 3.2013: featured updates to the NCCN Guidelines. J Natl Compr Canc Net. 2013; 11(5): 519-528.
7. Nagtegaal ID, Tot T, Jayne DG, McShane P, Nihlberg A, Marshall HC, et al. Lymph nodes, tumor deposits, and TNM: are we getting better? J Clin Oncol 2011; 29(18): 2487-2492.
8. Resch A, Langner C. Lymph node staging in colorectal cancer: old controversies and recent advances. World J Gastroenterol 2013; 19(46): 8515-8526.
9. McDonald JR, Renehan AG, O’Dwyer ST, Haboubi NY. Lymph node harvest in colon and rectal cancer: Current considerations. World J Gastrointest Surg 2012; 4(1): 9-19.
10. Williams GT, Quirke P, Shepherd NA. The royal college of pathologists. Standards and datasets for reporting cancers. Dataset for colorectal cancer, 2nd edition, 2007 (http://www.rcpath.org/publications-media/publications/datasets/colorectal-cancer.htm).
11. Jass JR, O’Brien J, Riddell RH, Snover DC. Association of Directors of Anatomic and Surgical Pathology. 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.
12. Washington MK, Berlin J, Branton P, Burgart LJ, Carter DK, Fitzgibbons PL, et al. Members of the Cancer Committee, College of American Pathologists. Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med 2009; 133(10): 1539-1551.
13. Benson AB 3rd, Arnoletti JP, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, et al. Colon Cancer. J Natl Compr Canc Net. 2011; 9(11): 1238-1290.
14. Benson AB 3rd, Bekaii-Saab T, Chan E, Chen YJ, Choti MA, Cooper HS, Rectal cancer. J Natl Compr Canc Netw 2012; 10(12): 1528-1564.
15. Fielding LP, Arsenault PA, Chapuis PH, Dent O, Gathright B, Hardcastle JD, et al. Clinicopathological staging for colorectal cancer: an International Documentation System (IDS) and an International Comprehensive Anatomical Terminology (ICAT). J Gastroenterol Hepatol 1991; 6(4): 325-344.
16. Baxter NN, Virnig DJ, Rothenberger DA, Morris AM, Jessurun J, Virnig BA. Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst 2005; 97(3): 219-225.
17. Bilimoria KY, Palis B, Stewart AK, Bentrem DJ, Freel AC, Sigurdson ER, et al. Impact of tumor location on nodal evaluation for colon cancer. Dis Colon Rectum 2008; 51(2): 154-161.
18. Gehoff A, Basten O, Sprenger T, Conradi LC, Bismarck C, Bandorski D, et al. Optimal lymph node harvest in rectal cancer (UICC stages II and III) after preoperative 5-FU-based radiochemotherapy. Acetone compression is a new and highly efficient method. Am J Surg Pathol 2012; 36(2): 202-213.
19. Baxter NN. Is lymph node count an ideal quality indicator for cancer care? J Surg Oncol 2009; 99(4): 265-268.
20. Märkl B, Rössle J, Arnholdt HM, et al. The clinical significance of lymph node size in colon cancer. Mod Pathol 2012; 25(10): 1413-1422.
21. Märkl 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.
22. Märkl B, Schaller T, Krammer I, Cacchi C, Arnholdt HM, Schenkirsch G, et al. Methylene blue-assisted lymph node dissection technique is not associated with an increased detection of lymph node metastases in colorectal cancer. Mod Pathol 2013; 26(9): 1246-1254.
23. Berger AC, Sigurdson ER, LeVoyer T, Hanlon A, Mayer RJ, Macdonald JS, et al. Colon cancer survival is associated with decreasing ratio of metastatic to examined lymph nodes. J Clin Oncol 2005; 23(34): 8706-8712.
24. Sjo OH, Merok MA, Svindland A, Nesbakken A. Prognostic impact of lymph node harvest and lymph node ratio in patients with colon cancer. Dis Colon Rectum 2012; 55(3): 307-315.
25. Medani M, Kelly N, Samaha G, Duff G, Healy V, Mulcahy E, et al. An appraisal of lymph node ratio in colon and rectal cancer: not one size fits all. Int J Colorectal Dis 2013; 28(10): 1377-1384.
26. Chen SL, Steele SR, Eberhardt J, Zhu K, Bilchik A, Stojadinovic A. Lymph node ratio as a quality and prognostic indicator in stage III colon cancer. Ann Surg 2011; 253(1): 82-87.
27. Kang J, Hur H, Min BS, Lee KY, Kim NK. Prognostic impact of the lymph node ratio in rectal cancer patients who underwent preoperative chemoradiation. J Surg Oncol 2011; 104(1): 53-58.
28. Bembenek AE, Rosenberg R, Wagler E, Gretschel S, Sendler A, Siewert JR, et al. Sentinel lymph node biopsy in colon cancer: a prospective multicenter trial. Ann Surg 2007; 245(6): 858-863.
29. van der Zaag ES, Kooij N, van de Vijver MJ, Bemelman WA, Peters HM, Buskens CJ. Diagnosing occult tumour cells and their predictive value in sentinel nodes of histologically negative patients with colorectal cancer. Eur J Surg Oncol 2010; 36(4): 350-357.
30. Märkl B, Arnholdt HM, Jähnig H, Spatz H, Anthuber M, Oruzio DV, et al. A new concept for the role of ex vivo sentinel lymph nodes in node-negative colorectal cancer. Ann Surg Oncol 2010; 17(10): 2647-2655.
31. van der Zaag ES, Bouma WH, Tanis PJ, Ubbink DT, Bemelman WA, Buskens CJ. Systematic review of sentinel lymph node mapping procedure in colorectal cancer. Ann Surg Oncol 2012; 19(11): 3449-3459.
32. Hamilton SR, Bosman FT, Boffetta P, Ilyas M, Morreau, Nakamura SI, et al. Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, Theise ND, eds. WHO classification of tumours of the digestive system. 4th edition. Lyon France: IARC Press; 2010: 134–146.
33. Langner C, Harbaum L, Pollheimer MJ, Kornprat P, Lindtner RA, Schlemmer A, et al. Mucinous differentiation in colorectal cancer--indicator of poor prognosis? Histopathology 2012; 60(7): 1060-1072.
34. Verhulst J, Ferdinande L, Demetter P, Ceelen W. Mucinous subtype as prognostic factor in colorectal cancer: a systematic review and meta-analysis. J Clin Pathol 2012; 65(5): 381-388.
35. Gao P, Song YX, Xu YY, Sun Z, Sun JX, Xu HM, et al. Does the prognosis of colorectal mucinous carcinoma depend upon the primary tumour site? Results from two independent databases. Histopathology 2013; 63(5): 603-615.
36. 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(3): 707-718.
37. Nitsche U, Zimmermann A, Späth C, Müller T, Maak M, Schuster T, et al. Mucinous and signet-ring cell colorectal cancers differ from classical adenocarcinomas in tumor biology and prognosis. Ann Surg 2013; 258(5): 775-782. Discussion pp. 782-783.
38. Thota R, Fang X, Subbiah S. Clinicopathological features and survival outcomes of primary signet ring cell and mucinous adenocarcinoma of colon: retrospective analysis of VACCR database. J Gastrointest Oncol 2014; 5(1): 18-24.
39. Sung CO, Seo JW, Kim KM, Do IG, Kim SW, Park CK. Clinical significance of signet-ring cells in colorectal mucinous adenocarcinoma. Mod Pathol 2008; 21(12): 1533-1541.
40. Pande R, Sunga A, Levea C, Wilding GE, Bshara W, Reid M, et al. Significance of signet-ring cells in patients with colorectal cancer. Dis Colon Rectum 2008; 51(1): 50-55.
41. Thirunavukarasu P, Sathaiah M, Singla S, Sukumar S, Karunamurthy A, Pragatheeshwar KD, et al. Medullary carcinoma of the large intestine: a population based analysis. Int J Oncol 2010; 37(4): 901-907.
42. Chetty R. Gastrointestinal cancers accompanied by a dense lymphoid component: an overview with special reference to gastric and colonic medullary and lymphoepithelioma-like carcinomas. J Clin Pathol 2012; 65(12): 1062-1065.
43. Verdú M, Román R, Calvo M, Rodón N, García B, González M, et al. Clinicopathological and molecular characterization of colorectal micropapillary carcinoma. Mod Pathol 2011; 24(5): 729-738.
44. Lee HJ, Eom DW, Kang GH, Han SH, Cheon GJ, Oh HS, et al. Colorectal micropapillary carcinomas are associated with poor prognosis and enriched in markers of stem cells. Mod Pathol 2013; 26(8): 1123-1131.
45. Betge J, Langner C. Vascular invasion, perineural invasion, and tumour budding: predictors of outcome in colorectal cancer. Acta Gastroenterol Belg 2011; 74(4): 516-529.
46. Jass JR, O’Brien J, Riddell RH, Snover DC. Association of Directors of Anatomic and Surgical Pathology. 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.
47. Betge J, Pollheimer MJ, Lindtner RA, Kornprat P, Schlemmer A, Rehak P, et al. Intramural and extramural vascular invasion in colorectal cancer: prognostic significance and quality of pathology reporting. Cancer 2012; 118(3): 628-638.
48. Messenger DE, Driman DK, Kirsch R. Developments in the assessment of venous invasion in colorectal cancer: implications for future practice and patient outcome. Hum Pathol 2012; 43(7): 965-973.
49. Harris EI, Lewin DN, Wang HL, Lauwers GY, Srivastava A, Shyr Y et al. Lymphovascular invasion in colorectal cancer: an interobserver variability study. Am J Surg Pathol 2008; 32(12): 1816-1821.
50. van Wyk HC, Roxburgh CS, Horgan PG, Foulis AF3, McMillan DC2. The detection and role of lymphatic and blood vessel invasion in predicting survival in patients with node negative operable primary colorectal cancer. Crit Rev Oncol Hematol 2014; 90(1): 77-90.
51. Liebig C, Ayala G, Wilks JA, Berger DH, Albo D. Perineural invasion in cancer: a review of the literature. Cancer 2009; 115(15): 3379-3391.
52. Poeschl EM, Pollheimer MJ, Kornprat P, Lindtner RA, Schlemmer A, Rehak P, et al. Perineural invasion: correlation with aggressive phenotype and independent prognostic variable in both colon and rectum cancer. J Clin Oncol 2010; 28(21): e358-360.
53. Liebig C, Ayala G, Wilks J, Verstovsek G, Liu H, Agarwal N, et al. Perineural invasion is an independent predictor of outcome in colorectal cancer. J Clin Oncol 2009; 27(31): 5131-5137.
54. Peng J, Sheng W, Huang D, Venook AP, Xu Y, Guan Z, et al. Perineural invasion in pT3N0 rectal cancer: the incidence and its prognostic effect. Cancer 2011; 117(7): 1415-1421.
55. Zlobec I, Lugli A. Invasive front of colorectal cancer. dynamic interface of pro-/anti-tumor factors. World J Gastroenterol 2009 15(47): 5898-5906.
56. 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.
57. Ueno H, Murphy J, Jass JR, Mochizuki H, Talbot IC. Tumour ‘budding’ as an index to estimate the potential of aggressiveness in rectal cancer. Histopathology 2002; 40(2): 127-132.
58. Lugli A, Karamitopoulou E, Zlobec I. Tumour budding: a promising parameter in colorectal cancer. Br J Cancer 2012; 106(11): 1713-1717.
59. Kanazawa H, Mitomi H, Nishiyama Y, Kishimoto I, Fukui N, Nakamura T, et al. Tumour budding at invasive margins and outcome in colorectal cancer. Colorectal Dis 2008;10(1):41-47.
60. Park KJ, Choi HJ, Roh MS, Kwon HC, Kim C. Intensity of tumor budding and its prognostic implications in invasive colon carcinoma. Dis Colon Rectum 2005; 48(8): 1597-1602.
61. 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(10): 1400-1406.
62. 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(5): 568–572.
63. Betge J, Kornprat P, Pollheimer MJ, Lindtner RA, Schlemmer A, Rehak P, et al. Tumor budding is an independent predictor of outcome in AJCC/UICC stage II colorectal cancer. Ann Surg Oncol 2012; 19(12): 3706-3712.
64. Mitrovic B, Schaeffer DF, Riddell RH, Kirsch R. Tumor budding in colorectal carcinoma: time to take notice. Mod Pathol 2012; 25(10): 1315-1325.
65. Quirke P, Risio M, Lambert R, von Karsa L, Vieth M. Quality assurance in pathology in colorectal cancer screening and diagnosis—European recommendations. Virchows Arch 2011; 458(1): 1-19.
66. Karamitopoulou E, Zlobec I, Kölzer V, Kondi-Pafiti A, Patsouris ES, Gennatas K, et al. Proposal for a 10-high-power-fields scoring method for the assessment of tumor budding in colorectal cancer. Mod Pathol 2013; 26(2): 295-301.
67. Horcic M, Koelzer VH, Karamitopoulou E, Terracciano L, Puppa G, Zlobec I, et al. Tumor budding score based on 10 high-power fields is a promising basis for a standardized prognostic scoring system in stage II colorectal cancer. Hum Pathol 2013; 44(5): 697-705.
68. Ueno H, Kajiwara Y, Shimazaki H, Shinto E, Hashiguchi Y, Nakanishi K, et al. New criteria for histologic grading of colorectal cancer. Am J Surg Pathol 2012; 36(2): 193-201.
69. Swinson DE, Jones JL, Richardson D, Cox G, Edwards JG, O’Byrne KJ. Tumour necrosis is an independent prognostic marker in non-small cell lung cancer: correlation with biological variables. Lung Cancer 2002; 37(3): 235-240.
70. Frank I, Blute ML, Cheville JC, Lohse CM, Weaver AL, Zincke H. An outcome prediction model for patients with clear cell renal cell carcinoma treated with radical nephrectomy based on tumor stage, size, grade and necrosis: the SSIGN score. J Urol 2002; 168(6): 2395-2400.
71. Langner C, Hutterer G, Chromecki T, Leibl S, Rehak P, Zigeuner R. Tumor necrosis as prognostic indicator in transitional cell carcinoma of the upper urinary tract. J Urol 2006; 176(3): 910-913;
72. Zigeuner R, Shariat SF, Margulis V, Karakiewicz PI, Roscigno M, Weizer A, et al. Tumour necrosis is an indicator of aggressive biology in patients with urothelial carcinoma of the upper urinary tract. Eur Urol 2010; 57(4): 575-581.
73. Pollheimer MJ, Kornprat P, Lindtner RA, Harbaum L, Schlemmer A, Rehak P, et al. Tumor necrosis is a new promising prognostic factor in colorectal cancer. Hum Pathol 2010; 41(12): 1749-1757.
74. Richards CH, Flegg KM, Roxburgh CS, Going JJ, Mohammed Z, Horgan PG, et al. The relationships between cellular components of the peritumoural inflammatory response, clinicopathological characteristics and survival in patients with primary operable colorectal cancer. Br J Cancer 2012; 106(12): 2010-2015.
75. Richards CH, Roxburgh CS, Anderson JH, McKee RF, Foulis AK, Horgan PG, et al. Prognostic value of tumour necrosis and host inflammatory responses in colorectal cancer. Br J Surg 2012; 99(2): 287-294.
76. Komori K, Kanemitsu Y, Kimura K, Hattori N, Sano T, Ito S, et al. Tumor necrosis in patients with TNM stage IV colorectal cancer without residual disease (R0 Status) is associated with a poor prognosis. Anticancer Res 2013; 33(3): 1099-1105.
77. Guthrie GJ, Roxburgh CS, Richards CH, Horgan PG, McMillan DC. Circulating IL-6 concentrations link tumour necrosis and systemic and local inflammatory responses in patients undergoing resection for colorectal cancer. Br J Cancer 2013; 109(1): 131-137.
78. Klintrup K, Mäkinen JM, Kauppila S, Väre PO, Melkko J, Tuominen H, et al. Inflammation and prognosis in colorectal cancer. Eur J Cancer 2005; 41(17): 2645-2654.
79. Roxburgh CS, Salmond JM, Horgan PG, Oien KA, McMillan DC. Tumour inflammatory infiltrate predicts survival following curative resection for node-negative colorectal cancer. Eur J Cancer 2009; 45(12): 2138-2145.
80. Ogino S, Nosho K, Irahara N, Meyerhardt JA, Baba Y, Shima K, 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(20): 6412-6420.
81. Greenson JK, Huang SC, Herron C, Moreno V, Bonner JD, Tomsho LP, et al. Pathologic predictors of microsatellite instability in colorectal cancer. Am J Surg Pathol 2009; 33(1): 126-33.
82. Nagtegaal ID, Marijnen CA, Kranenbarg EK, Mulder-Stapel A, Hermans J, van de Velde CJ, et al. Local and distant recurrences in rectal cancer patients are predicted by the nonspecific immune response; specific immune response has only a systemic effect--a histopathological and immunohistochemical study. BMC Cancer 2001; 1: 7.
83. Richards CH, Roxburgh CS, Powell AG, Foulis AK, Horgan PG, McMillan DC. The clinical utility of the local inflammatory response in colorectal cancer. Eur J Cancer 2014; 50(2): 309-319.
84. Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, et al. Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumours. J Pathol 2014; 232(2): 199-209.
85. Lugli A, Karamitopoulou E, Panayiotides I, Karakitsos P, Rallis G, Peros G, et al. CD8+ lymphocytes/ tumour-budding index: an independent prognostic factor representing a ‘pro-/anti-tumour’ approach to tumour host interaction in colorectal cancer. Br J Cancer 2009; 101(8): 1382-1392.
86. Nielsen HJ, Hansen U, Christensen IJ, Reimert CM, Brünner N, Moesgaard F. Independent prognostic value of eosinophil and mast cell infiltration in colorectal cancer tissue. J Pathol 1999; 189(4): 487-95.
87. Fernandez-Acenero MJ, Galindo-Gallego M, Sanz J, Aljama A. Prognostic influence of tumor-associated eosinophilic infiltrate in colorectal carcinoma. Cancer 2000; 88(7): 1544-1548.
88. Forssell J, Oberg A, Henriksson ML, Stenling R, Jung A, Palmqvist R. High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clin Cancer Res 2007; 13(5): 1472-1479.
89. Chaput N, Svrcek M, Aupérin A, Locher C, Drusch F, Malka D, et al. Tumour-infiltrating CD68+ and CD57+ cells predict patient outcome in stage II-III colorectal cancer. Br J Cancer 2013; 109(4): 1013-1022.
90. Bosch SL, Nagtegaal ID. The importance of the pathologist’s role in assessment of the quality of the mesorectum. Curr Colorectal Cancer Rep 2012; 8(2): 90-98.
91. 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.
92. van de Velde CJ, Boelens PG, Borras JM, Coebergh JW, Cervantes A, Blomqvist L, et al. EURECCA colorectal: multidisciplinary management: European consensus conference colon & rectum. Eur J Cancer 2014; 50(1): 1.e1-1.e34.
93. Quirke P, West NP, Nagtegaal ID. EURECCA consensus conference highlights about colorectal cancer clinical management: the pathologists expert review. Virchows Arch 2014; 464(2): 129-134.
94. 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.
95. Kudo S. Endoscopic mucosal resection of flat and depressed types of early colorectal cancer. Endoscopy 1993; 25(7): 455-461.
96. Kikuchi R, Takano M, Takagi K, Fujimoto N, Nozaki R, Fujiyoshi T, Uchida Y. Management of early invasive colorectal cancer. Risk of recurrence and clinical guidelines. Dis Colon Rectum 1995; 38(12): 1286-1295.
97. Sakuragi M, Togashi K, Konishi F, Koinuma K, Kawamura Y, Okada M, et al. Predictive factors for lymph node metastasis in T1 stage colorectal carcinomas. Dis Colon Rectum 2003; 46(12): 1626-1632.
98. Egashira Y, Yoshida T, Hirata I, Hamamoto N, Akutagawa H, Takeshita A, et al. Analysis of pathological risk factors for lymph node metastasis of submucosal invasive colon cancer. Mod Pathol 2004; 17(5): 503-511.
99. Tateishi Y, Nakanishi Y, Taniguchi H, Shimoda T, Umemura S. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol 2010 23(8): 1068-1072.
100. 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.
101. Ueno H, Mochizuki H, Hashiguchi Y, Shimazaki H, Aida S, Hase K, et al. Risk factors for an adverse outcome in early invasive colorectal carcinoma. Gastroenterology 2004; 127(2): 385-394.
102. Butte JM, Tang P, Gonen M, Shia J, Schattner M, Nash GM, et al. Rate of residual disease after complete endoscopic resection of malignant colonic polyp. Dis Colon Rectum 2012; 55(2): 122-127.
103. Williams JG, Pullan RD, Hill J, Horgan PG, Salmo E, Buchanan GN, et al. Management of the malignant colorectal polyp: ACPGBI position statement. Colorectal Dis 2013; 15 Suppl 2: 1-38.
104. Ramirez M, Schierling S, Papaconstantinou HT, Thomas JS. Management of the malignant polyp. Clin Colon Rectal Surg 2008; 21(4): 286-290.
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