Site-specific tumor grading system in colorectal cancer: Multicenter pathologic review of the value of quantifying poorly differentiated clusters

American Journal of Surgical Pathology

Volumn 38, Issue 2, 2014, Pages 197-204

  Ueno, Hideki ^a   Hase, Kazuo ^a   Hashiguchi, Yojiro ^b   Shimazaki, Hideyuki ^a   Tanaka, Masafumi ^g   Miyake, Ohki ^c   Masaki, Tadahiko ^d   Shimada, Yoshifumi ^h   Kinugasa, Yusuke ⁱ   Mori, Yoshiyuki ^j   Kishimoto, Mitsuo ^k   Kameoka, Shingo ^e   Sato, Yu ^l   Matsuda, Keiji ^b   Nakadoi, Koichi ^m   Shinto, Eiji ^a   Nakamura, Takahiro ^a   Sugihara, Kenichi ^f  

^a NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

^b TEIKYO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^d KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^f TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^g TAKANO HOSPITAL   (Japan)

^h NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

ⁱ SHIZUOKA CANCER CENTER   (Japan)

^j UNIVERSITY OF YAMANASHI   (Japan)

^k KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^l NATIONAL CANCER CENTER HOSPITAL EAST   (Japan)

^m HIROSHIMA UNIVERSITY HOSPITAL   (Japan)

more..

Author keywords

colorectal cancer; poorly differentiated clusters; prognostic marker; tumor grade

Indexed keywords

ADOLESCENT; ADULT; AGED; ARTICLE; CANCER GRADING; CANCER STAGING; CELL DIFFERENTIATION; COLORECTAL TUMOR; COMPARATIVE STUDY; DISEASE FREE SURVIVAL; EVALUATION STUDY; FEMALE; HUMAN; JAPAN; MALE; MIDDLE AGED; MORTALITY; MULTICENTER STUDY; MULTIVARIATE ANALYSIS; OBSERVER VARIATION; PATHOLOGY; PREDICTIVE VALUE; REPRODUCIBILITY; RISK FACTOR; SURVIVAL; TIME; TREATMENT OUTCOME; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; CELL DIFFERENTIATION; COLORECTAL NEOPLASMS; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; JAPAN; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM GRADING; NEOPLASM STAGING; OBSERVER VARIATION; PREDICTIVE VALUE OF TESTS; REPRODUCIBILITY OF RESULTS; RISK FACTORS; SURVIVAL ANALYSIS; TIME FACTORS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84893006967     PISSN: 01475185     EISSN: 15320979     Source Type: Journal    
DOI: 10.1097/PAS.0000000000000113     Document Type: Article

References (70)

1. Riddell RH, Petras RE, Williams GT, et al. Colorectal carcinoma. In: Rosai J, Sobin L, eds. Atlas of Tumor Pathology-Tumors of the Intestines. Washington: Armed Forces Institute of Pathology; 2002:133-188.
2. Dukes CE. The classification of cancer of the rectum. J Pathol Bacteriol. 1932;35:323-332.
3. Sobin LH, Gospodarowicz MK, Wittekind C. International Union Against Cancer: TNM Classification of Malignant Tumours. 7th edition. New York: Wiley-Blackwell; 2009.
4. Compton CC. Pathology report in colon cancer: what is prognos-tically important? Dig Dis. 1999;17:67-79.
5. Newland RC, Dent OF, Lyttle MNB, et al. Pathologic determinants of survival associated with colorectal cancer with lymph node metastases. Cancer. 1994;73:2076-2082.
6. Hamilton SR, Bosman FT, Boffetta P, et al. Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, et al, eds. WHO Classification of Tumours of the Digestive System. Lyon: International Agency for Research on Cancer (IARC); 2010:134-146.
7. National Comprehensive Cancer Network: NCCN clinical practice guidelines in oncology-colon cancer (version 3), 2013. Available at: http://www.nccn.org/ professionals/physician-gls/pdf/colon.pdf. Accessed May 9, 2013.
8. Schmoll HJ, Van Cutsem E, Stein A, et al. ESMO consensus guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Ann Oncol. 2012;23:2479-2516.
9. Watanabe T, Itabashi M, Shimada Y, et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol. 2009;17:1-29.
10. Morodomi T, Isomoto H, Shirouzu K, et al. 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.
11. Hase K, Shatney C, Johnson D, et al. Prognostic value of tumor "budding" in patients with colorectal cancer. Dis Colon Rectum. 1993;36:627-635.
12. Prall E. Tumour budding in colorectal carcinoma. Histopathology. 2007;50:151-162.
13. Lugli A, Karamitopoulou E, Zlobec I. Tumour budding: a promising parameter in colorectal cancer. Br J Cancer. 2012;106:1713-1717.
14. Ueno H, Murphy J, Jass JR, et al. Tumour "budding" as an index to estimate the potential of aggressiveness in rectal cancer. Histopa-thology. 2002;40:127-132.
15. Ueno H, Price AB, Wilkinson KH, et al. A new prognostic staging system for rectal cancer. Ann Surg. 2004;240:832-839.
16. Park K-J, Choi H-J, Roh M-S, et al. Intensity of tumor budding and its prognostic implications in invasive colon carcinoma. Dis Colon Rectum. 2005;48:1597-1602.
17. Choi H-J, Park K-J, Shin J-S, et al. Tumor budding as a prognostic marker in stage-III rectal cancer. Int J Colorectal Dis. 2007;22: 863-868.
18. 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.
19. Sy J, CL-S Fung, Dent OF, et al. Tumor budding and survival after potentially curative resection of node-positive colon cancer. Dis Colon Rectum. 2010;53:301-307.
20. Syk E, Lenander C, Nilsson PJ, et al. Tumour budding correlates with local recurrence of rectal cancer. Colorectal Dis. 2011;13:255-262.
21. Garcia-Solano J, Conesa-Zamora P, Trujillo-Santos J, et al. Tumour budding and other prognostic pathological features at invasive margins in serrated colorectal adenocarcinoma: a comparative study with conventional carcinoma. Histopathology. 2011;59:1046-1056.
22. Betge J, Kornprat P, Pollheimer MJ, et al. Tumor budding is an independent predictor of outcome in AJCC/UICC stage II color-ectal cancer. Ann Surg Oncol. 2012;19:3706-3712.
23. Du C, Xue W, Li J, et al. Morphology and prognostic value of tumor budding in rectal cancer after neoadjuvant radiotherapy. Hum Pathol. 2012;43:1061-1067.
24. Wang C, Huang H, Huang Z, et al. Tumor budding correlates with poor prognosis and epithelial-mesenchymal transition in tongue squamous cell carcinoma. J Oral Pathol Med. 2011;40:545-551.
25. Masuda R, Kijima H, Imamura N, et al. Tumor budding is a significant indicator of poor prognosis in lung squamous cell carcinoma patients. Mol Med Rep. 2012;6:937-943.
26. Taira T, Ishii G, Nagai K, et al. Characterization of the immuno-phenotype of the tumor budding and its prognostic implications in squamous cell carcinoma of the lung. Lung Cancer. 2012;76:423-430.
27. Roh MS, Lee JI, Choi PJ. Tumor budding as a useful prognostic marker in esophageal squamous cell carcinoma. Dis Esophagus. 2004;17:333-337.
28. Koike M, Kodera Y, Ito Y, et al. Multivariate analysis of the pathologic features of esophageal squamous cell cancer: tumor budding is a significant independent prognostic factor. Ann Surg Oncol. 2008;15:1977-1982.
29. Miyata H, Yoshioka A, Yamasaki M, et al. Tumor budding in tumor invasive front predicts prognosis and survival of patients with esophageal squamous cell carcinomas receiving neoadjuvant chemotherapy. Cancer. 2009;115:3324-3334.
30. Brown M, Sillah K, Griffiths EA, et al. Tumour budding and a low host inflammatory response are associated with a poor prognosis in oesophageal and gastro-oesophageal junction cancers. Histopathol-ogy. 2010;56:893-899.
31. Nakanishi Y, Ohara M, Doumen H, et al. Correlation between tumor budding and post-resection prognosis in patients with invasive squamous cell carcinoma of the thoracic esophagus. World J Surg. 2011;35:349-356.
32. Kai K, Kohya N, Kitahara K, et al. Tumor budding and dedifferentiation in gallbladder carcinoma: potential for the prognostic factors in T2 lesions. Virchows Arch. 2011;459:449-456.
33. Karamitopoulou E, Zlobec I, Born D, et al. Tumour budding is a strong and independent prognostic factor in pancreatic cancer. Eur J Cancer. 2013;49:1032-1039.
34. Ohiki N, Coban I, Kim GE, et al. Tumor budding as a strong prognostic indicator in invasive ampullary adenocarcinoma. Am J Surg Pathol. 2010;34:1417-1424.
35. Koyuncuoglu M, Okyay E, Saatli B, et al. Tumor budding and E-cadherin expression in endometrial carcinoma: are they prognostic factors in endometrial cancer? Gynecol Oncol. 2012;125:208-213.
36. Ueno H, Mochizuki H, Hashiguchi Y, et al. Histological grading of colorectal cancer: a simple and objective method. Ann Surg. 2008; 247:811-818.
37. 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.
38. Barresi V, Bonetti LR, Branca G, et al. Colorectal carcinoma grading by quantifying poorly differentiated cell clusters is more reproducible and provides more robust prognostic information than conventional grading. Virchows Arch. 2012;461:621-628.
39. Ueno H, Shimazaki H, Shinto E, et al. New criteria for histologic grading of colorectal cancer. Am J Surg Pathol. 2012;36:193-201.
40. Tateishi Y, Nakanishi Y, Taniguchi H, et al. Pathological prognostic factors predicting lymph node metastasis in submucosal invasive (T1) colorectal carcinoma. Mod Pathol. 2010;23:1068-1072.
41. Kazama S, Watanabe T, Ajioka Y, et al. 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.
42. 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.
43. 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.
44. Suzuki A, Togashi K, Nokubi M, et al. Evaluation of venous invasion by elastica van Gieson stain and tumor budding predicts local and distant metastases in patients with T1 stage colorectal cancer. Am J Surg Pathol. 2009;33:1601-1607.
45. Horcic M, Koelzer VH, Karamitopoulou E, 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;44:697-705.
46. Puppa G, Senore C, Sheahan K, et al. Diagnostic reproducibility of tumour budding in colorectal cancer: a multicentre, multinational study using virtual microscopy. Histopathology. 2012;61:562-575.
47. American Joint Committee on Cancer. In: Edge SB, Byrd DR, Compton CC, et al, eds. AJCC Cancer Staging Manual. 7th edition. New York: Springer; 2009.
48. Hamilton SR, Vogelstein B, Kudo S, et al. Carcinoma of the colon and rectum. In: Hamilton SR, Aaltonen LA, eds. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Digestive System. Lyon: International Agency for Research on Cancer (IARC); 2000:105-119.
49. Akaike H. Information Theory and an Extension of the Maximum Likelihood Principle. Budapest: Akademia Kiado; 1973.
50. Wang SJ, Lemieuz A, Kalpathy-Cramer J, et al. Nomogram for predicting the benefit of adjuvant chemoradiotherapy for resected gallbladder cancer. J Clin Oncol. 2011;29:4627-4632.
51. Ueno H, Mochizuki H, Akagi Y, et al. Optimal colorectal cancer staging criteria in TNM classification. J Clin Oncol. 2012;30: 1519-1526.
52. Hsu C-Y, Lee Y-H, Hsia C-Y, et al. Performance status in patients with hepatocellular carcinoma: determinants, prognostic impact, and ability to improve the Barcelona Clinic Liver Cancer System. Hepatology. 2013;57:112-119.
53. R Development Core Team. R:A language and environment for statistical computing. In: Vienna R. Foundation for Statistical Computing. 2006.
54. Rankin FW, Broders AC. Factors influencing prognosis in carcinoma of the rectum. Surg Gynecol Obstet. 1928;46:660-667.
55. Dukes C. Histological grading of rectal cancer. Proc R Soc Med. 1937;30:371-376.
56. Grinnell RS. The grading and prognosis of carcinoma of the colon and rectum. Ann Surg. 1939;109:500-533.
57. Halvorsen TB, Seim E. Degree of differentiation in colorectal adenocarcinomas: a multivariate analysis of the influence on survival. J Clin Pathol. 1988;41:532-537.
58. Chandler I, Houlston RS. Interobserver agreement in grading of colorectal cancers-findings from a nationwide web-based survey of histopathologists. Histopathology. 2008; 52: 494-499.
59. Jass JR, O'Brien MJ, Riddell RH, et al. Recommendations for the reporting of surgically resected specimens of colorectal carcinoma. Hum Pathol. 2007;38:537-545.
60. The Royal College of Pathologists of Australasia: Colorectal cancer structured reporting protocol, 1st edition, 2012. Available at: http://www.rcpa.edu.au. Accessed February 19, 2013.
61. Halvorsen TB, Seim E. Influence of mucinous components on survival in colorectal adenocarcinomas: a multivariate analysis. J Clin Pathol. 1988;41:1068-1072.
62. Langner C, Harbaum L, Pollheimer MJ, et al. Mucinous differentiation in colorectal cancer-indicator of poor prognosis? Histo-pathology. 2012;60:1060-1072.
63. Kim M-J, Hong S-M, Jang SJ, et al. Invasive colorectal micro-papillary carcinoma: an aggressive variant of adenocarcinoma. Hum Pathol. 2006;37:809-815.
64. Haupt B, Ro JY, Schwartz MR, et al. Colorectal adenocarcinoma with micropapillary pattern and its association with lymph node metastasis. Mod Pathol. 2007;20:729-733.
65. 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.
66. Jass JR, Love SB, Northover JMA. A new prognostic classification of rectal cancer. Lancet. 1987;6:1303-1306.
67. Harrison JC, Dean PJ, El-Zeky F, et al. From Dukes through Jass: pathological prognostic indicators in rectal cancer. Hum Pathol. 1994;25:498-505.
68. Williams GT, Quirke P, Shepherd NA, et al. Standards and datasets for reporting cancers. dataset for colorectal cancer, 2nd edition, 2007. Available at: http://www.rcpath.org/publications-media/publications/datasets/colorectal- cancer.htm. Accessed February 19, 2013.
69. Thomas GDH, Dixon MF, Smeeton NC, et al. Observer variation in the histological grading of rectal carcinoma. J Clin Pathol. 1983;36:385-391.
70. Deans GT, Heatley M, Anderson N, et al. Jass' classification revisited. J Am Coll Surg. 1994;179:11-17.