Tumour budding and other prognostic pathological features at invasive margins in serrated colorectal adenocarcinoma: A comparative study with conventional carcinoma

Histopathology

Volumn 59, Issue 6, 2011, Pages 1046-1056

  García Solano, José ^a   Conesa Zamora, Pablo ^a   Trujillo Santos, Javier ^a   Mäkinen, Markus J ^b   Pérez Guillermo, Miguel ^a  

^a Hospital Universitario Santa Maria Del Rosell   (Spain)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

Colorectal cancer; Lymphocytic response; Pseudo cytoplasmic fragments; Serrated adenocarcinoma; Tumour budding; Tumour growth pattern

Indexed keywords

ADULT; AGED; ARTICLE; CANCER GRADING; CANCER INFILTRATION; CANCER LOCALIZATION; CANCER PATIENT; CANCER SURVIVAL; COLORECTAL CARCINOMA; CONVENTIONAL COLORECTAL CARCINOMA; CYTOPLASM PSEUDOFRAGMENT; CYTOPLASM VESICLE; FEMALE; HISTOPATHOLOGY; HUMAN; LYMPH NODE METASTASIS; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROGNOSIS; SERRATED COLORECTAL ADENOCARCINOMA; TUMOR BUDDING; TUMOR GROWTH;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; COLORECTAL NEOPLASMS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MALE; MIDDLE AGED; PROGNOSIS; PROPORTIONAL HAZARDS MODELS;

EID: 84855952004     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/j.1365-2559.2011.04043.x     Document Type: Article

References (48)

1. Mäkinen MJ. Colorectal serrated adenocarcinoma. Histopathology 2007; 50; 131-150.
2. O'Brien MJ, Ynag S, Mack C et al. Comparison of microsatellite instability, CpG island methylation phenotype, BRAF and KRAS status in serrated polyps and traditional adenomas indicates separate pathways to distinct colorectal carcinoma end points. Am. J. Surg. Pathol. 2006; 30; 1491-1501.
3. García-Solano J, Pérez-Guillermo M, Conesa-Zamora P et al. Clinicopathologic study of 85 colorectal serrated adenocarcinomas: further insights into the full recognition of a new subset of colorectal carcinoma. Hum. Pathol. 2010; 41; 1359-1368.
4. Hase K, Shatney C, Johnson D, Trollope M, Vierra M. Prognostic value of tumour 'budding' in patients with colorectal cancer. Dis. Colon Rectum 1993; 36; 627-635.
5. 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.
6. Nakamura T, Mitomi H, Kikuchi S, Ohtani Y, Sato K. Evaluation of the usefulness of tumor budding on the prediction of metastasis to the lung and liver after curative excision of colorectal cancer. Hepatogastroenterology 2005; 52; 1432-1435.
7. 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; 127-132.
8. Prall F, Nizze H, Barten M. Tumour budding as prognostic factor in stage I/II colorectal carcinoma. Histopathology 2005; 47; 17-24.
9. Hörkkö TT, Klintrup K, Mäkinen JM et al. Budding invasive margin and prognosis in colorectal cancer-no direct association with beta-catenin expression. Eur. J. Cancer 2006; 42; 964-971.
10. Zlobec I, Lugli A, Baker K et al. Role of APAF-1, E-cadherin and peritumoral lymphocytic infiltration in tumour budding in colorectal cancer. J. Pathol. 2007; 212; 260-268.
11. Shinto E, Mochizuki H, Ueno H, Matsubara O, Jass JR. A novel classification of tumour budding in colorectal cancer based on the presence of cytoplasmic pseudo-fragments around budding foci. Histopathology 2005; 47; 25-31.
12. Jass JR. Lymphocytic infiltration and survival in rectal cancer. J. Clin. Pathol. 1986; 39; 585-589.
13. Jass JR, Love SB, Northover JM. A new prognostic classification of rectal cancer. Lancet 1987; 1; 1303-1306.
14. 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.
15. Klintrup K, Mäkinen JM, Kauppila S et al. Inflammation and prognosis in colorectal cancer. Eur. J. Cancer 2005; 41; 2645-2654.
16. 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; 2138-2145.
17. Jass JR, Ajioka Y, Allen JP et al. Assessment of invasive growth pattern and lymphocytic infiltration in colorectal cancer. Histopathology 1996; 28; 543-548.
18. 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; 437-459.
19. Shinto E, Jass JR, Tsuda H et al. Differential prognostic significance of morphologic invasive markers in colorectal cancer: tumor budding and cytoplasmic podia. Dis. Colon Rectum 2006; 49; 1422-1430.
20. Yang AD, Fan F, Camp ER et al. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin. Cancer Res. 2006; 12; 4147-4153.
21. Imai T, Enjoji M. On metastasis of gastric carcinoma. Gan 1954; 45; 213-216.
22. Morodomi T, Isomoto H, Shirouzu K, Kakegawa K, Irie K, Morimatsu M. An index for estimating the probability of lymph node metastasis in rectal cancers. Lymph node metastasis and the histopathology of actively invasive regions of cancer. Cancer 1989; 63; 539-543.
23. 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; 1182-1192.
24. Kaneko I, Tanaka S, Oka S et al. Immunohistochemical molecular markers as predictors of curability of endoscopically resected submucosal colorectal cancer. World J. Gastroenterol. 2007; 13; 3829-3835.
25. Kanazawa H, Mitomi H, Nishiyama Y et al. Tumour budding at invasive margins and outcome in colorectal cancer. Colorectal. Dis. 2008; 10; 41-47.
26. Yasuda K, Inomata M, Shiromizu A, Shiraishi N, Higashi H, Kitano S. Risk factors for occult lymph node metastasis of colorectal cancer invading the submucosa and indications for endoscopic mucosal resection. Dis. Colon Rectum 2007; 50; 1370-1376.
27. Ishikawa Y, Akishima-Fukasawa Y, Ito K et al. Histopathologic determinants of regional lymph node metastasis in early colorectal cancer. Cancer 2008; 112; 924-933.
28. Yamauchi H, Togashi K, Kawamura YJ et al. Pathological predictors for lymph node metastasis in T1 colorectal cancer. Surg. Today 2008; 38; 905-910.
29. Choi DH, Sohn DK, Chang HJ, Lim SB, Choi HS, Jeong SY. Indications for subsequent surgery after endoscopic resection of submucosally invasive colorectal carcinomas: a prospective cohort study. Dis. Colon Rectum 2009; 52; 438-445.
30. 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.
31. 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; 134-141.
32. 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; 2068-2072.
33. Zlobec I, Baker K, Minoo P, Jass JR, 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; 143-1438.
34. 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.
35. Jass JR, Barker M, Fraser L et al. APC mutation and tumour budding in colorectal cancer. J. Clin. Pathol. 2003; 56; 69-73.
36. Tanaka M, Hashiguchi Y, Ueno H, Hase K, Mochizuki H. Tumor budding at the invasive margin can predict patients at high risk of recurrence after curative surgery for stage II, T3 colon cancer. Dis. Colon Rectum 2003; 46; 1054-1059.
37. Ohtsuki K, Koyama F, Tamura T et al. Prognostic value of immunohistochemical analysis of tumor budding in colorectal carcinoma. Anticancer Res. 2008; 28; 1831-1836.
38. Sy J, Fung CL, Dent OF, Chapuis PH, Bokey L, Chan C. Tumor budding and survival after potentially curative resection of node-positive colon cancer. Dis. Colon Rectum 2010; 53; 301-307.
39. Prall F. Tumour budding in colorectal carcinoma. Histopathology 2007; 50; 151-162.
40. Tuppurainen K, Mäkinen JM, Junttila O et al. Morphology and microsatellite instability in sporadic serrated and non-serrated colorectal cancer. J Pathol. 2005; 207; 285-294.
41. Jenkins MA, Hayashi S, O'Shea AM et al. Pathology features in Bethesda guidelines predict colorectal cancer microsatellite instability: a population-based study. Gastroenterology 2007; 133; 48-56.
42. Hamilton SR, Bosman FT, Boffetta P 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. Lyon, France: IARC Press, 2010; 134-151.
43. Redston M. Epithelial neoplasms of the large intestine. In Odze RD, Goldblum JR, Crawford JM eds. Surgical pathology of the GI tract, liver, biliary tract, and pancreas. Philadelphia, PA: Saunders, 2009; 614-615.
44. Cooper HS. Intestinal neoplasms. In Mills SE ed. Sternberg's diagnostic surgical pathology. Philadelphia, PA: Lippincott Williams & Wilkins, 2009; 1368-1431.
45. 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.
46. Turner RR, Li C, Compton CC. Newer pathologic assessment techniques for colorectal carcinoma. Clin. Cancer Res. 2007; 13; 6871s-6876s.
47. Lugli A, Karamitopoulou E, Panayiotides I 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; 1382-1392.
48. Noffsinger AE. Serrated polyps and colorectal cancer: new pathway to malignancy. Annu. Rev. Pathol. 2009; 4; 343-464.