Identification of prognostically relevant and reproducible subsets of endometrial adenocarcinoma based on clustering analysis of immunostaining data

Modern Pathology

Volumn 20, Issue 11, 2007, Pages 1156-1165

  Alkushi, Abdulmohsen ^a   Clarke, Blaise A ^b   Akbari, Majid ^c   Makretsov, Nikita ^b   Lim, Peter ^d   Miller, Dianne ^d   Magliocco, Anthony ^c   Coldman, Andrew ^d   Van De Rijn, Matt ^e   Huntsman, David ^b   Parker, Robin ^c   Gilks, C Blake ^b  

^a KING FAHAD NATIONAL GUARD HOSPITAL   (Saudi Arabia)

^b VANCOUVER GENERAL HOSPITAL   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d BRITISH COLUMBIA CANCER AGENCY   (Canada)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenocarcinoma; Clustering analysis; Endometrial cancer; Immunohistochemistry; Reproducibility; Subclassification

Indexed keywords

BIOLOGICAL MARKER;

ADULT; AGE; AGED; ARTICLE; CANCER CLASSIFICATION; CANCER SURVIVAL; CELL TYPE; CLUSTER ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE MARKER; DISEASE SEVERITY; ENDOMETRIUM CARCINOMA; FEMALE; FISHER EXACT TEST; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; LOG RANK TEST; MAJOR CLINICAL STUDY; MULTIVARIATE ANALYSIS; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; REPRODUCIBILITY; STATISTICAL SIGNIFICANCE; SURVIVAL RATE; TISSUE MICROARRAY; UNIVARIATE ANALYSIS;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; CLUSTER ANALYSIS; ENDOMETRIAL NEOPLASMS; FEMALE; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIERS ESTIMATE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEOPLASM STAGING; PROGNOSIS; REPRODUCIBILITY OF RESULTS; SURVIVAL ANALYSIS; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 35348984917     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.3800950     Document Type: Article

References (54)

1. Greenlee RT, Murray T, Bolden S, et al. Cancer statistics, 2000. CA Cancer J Clin 2000;50:7-33.
2. Tavassoli FA, Devilee P. WHO Classification of Tumors: Pathology and Genetics Tumors of the Breast and Female Genital Organs. IARC Press: Lyon, France, 2003.
3. Goff B. Uterine papillary serous carcinoma: what have we learned over the past quarter century? Gynecol Oncol 2005;98:341-343.
4. Prat J. Prognostic parameters of endometrial carcinoma. Hum Pathol 2004;35:649-662.
5. Alkushi A, Abdul-Rahman ZH, Lim P, et al. Description of a novel system for grading of endometrial carcinoma and comparison with existing grading systems. Am J Surg Pathol 2005;29:295-304.
6. Nedergaard L, Jacobsen M, Andersen JE. Interobserver agreement for tumour type, grade of differentiation and stage in endometrial carcinomas. APMIS 1995;103:511-518.
7. Nielsen AL, Thomsen HK, Nyholm HC. Evaluation of the reproducibility of the revised 1988 International Federation of Gynecology and Obstetrics grading system of endometrial cancers with special emphasis on nuclear grading. Cancer 1991;68:2303-2309.
8. Nordstrom B, Strang P, Lindgren A, et al. Carcinoma of the endometrium: do nuclear grade and DNA ploidy provide more prognostic information than do the FIGO and WHO classifications? Int J Gynecol Pathol 1996;15:191-201.
9. Lax SF, Kurman RJ, Pizer ES, et al. A binary architectural grading system for uterine endometrial endometrioid carcinoma has superior reproducibility compared with FIGO grading and identifies subsets of advance-stage tumors with favorable and unfavorable prognosis. Am J Surg Pathol 2000;24:1201-1208.
10. Scholten AN, Smit VTHBM, Beerman H, et al. Prognostic significance and interobserver variability of histologic grading systems for endometrial carcinoma. Cancer 2004;100:764-772.
11. Taylor RR, Zeller J, Lieberman RW, et al. An analysis of two versus three grades for endometrial carcinoma. Gynecol Oncol 1999;74:3-6.
12. Zaino RJ, Kurman RJ, Diana KL, et al. The utility of the revised international federation of gynecology and obstetrics histologic grading of endometrial adenocarcinoma using a defined nuclear grading system. A Gynecologic Oncology Group study. Cancer 1995;75:81-86.
13. Al-Kushi A, Irving J, Hsu F, et al. Immunoprofile of cervical and endometrial adenocarcinomas using a tissue microarray. Virchows Archiv 2003;442:271-277.
14. Eisen MB, Spellman PT, Brown PO, et al. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998;95:14863-14868.
15. Makretsov NA, Huntsman DG, Nielsen TO, et al. Hierarchical clustering analysis of tissue microarray immunostaining data identifies prognostically significant groups of breast carcinoma. Clin Cancer Res 2004;15:6143-6151.
16. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000;403:503-511.
17. Garber ME, Troyanskaya OG, Schluens K, et al. Diversity of gene expression in adenocarcinoma of the lung. Proc Natl Acad Sci USA 2001;98:13784-13789.
18. Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 2003;100:8418-8423.
19. van't Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-536.
20. Paik S, Shak S, Tang G, et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004;351:2817-2826.
21. Callagy G, Cattaneo E, Daigo Y, et al. Molecular classification of breast carcinomas using TMAs. Diagn Mol Pathol 2003;12:27-34.
22. Dalia M, El-Rehim A, Ball G, et al. High-throughput protein expression analysis using tissue microarray technology of a well-characterized series identifies biologically distinct classes of breast cancer confirming recent cDNA expression analyses. Int J Cancer 2005;3:340-350.
23. Jacquemier J, Ginestier C, Rougemont J, et al. Protein expression profiling identifies subclasses of breast cancer and predicts prognosis. Cancer Res 2005;65:767-779.
24. Creasman WT. Announcements: FIGO stages - 1988 revision. Gynecol Oncol 1989;35:125-127.
25. Sherman ME, Bitterman P, Rosenshein NB, et al. Uterine serous carcinoma. A morphologically diverse neoplasm with unifying clinicopathologic features. Am J Surg Pathol 1992;16:600-610.
26. Alkushi A, Lim P, Coldman A, et al. Interpretation of p53 immunohistochemical staining in endometrial carcinoma: establishing a clinically relevant cut-off. Int J Gynecol Pathol 2004;23:129-137.
27. Liu CL, Prapong W, Natkunam Y, et al. Software tools for high-throughput analysis and archiving of immunohistochemistry staining data obtained with TMAs. Am J Pathol 2002;161:1557-1565.
28. Al-Kushi M, Lim P, Aquino-Parsons C, et al. Markers of proliferative activity are predictors of patient outcome for low-grade endometrioid carcinoma but not papillary serous carcinoma of the endometrium. Mod Pathol 2002;15:365-371.
29. Bokhman JV. Two pathogenetic types of endometrial carcinoma. Gynecol Oncol 1983;15:10-17.
30. Koshiyama M, Ueta M. Two kinds of endometrial neoplasia arising from different origins in the uterine corpus: comparison of p53 expression and sex steroid receptor status. Eur J Obstet Gynecol Reprod Biol 2002;104:167-170.
31. Lax SF, Kurman RJ. A dualistic model for endometrial carcinogenesis based on immunohistochemical and molecular genetic analyses. Verh Dtsch Ges Pathol 1997;81:228-232.
32. Lax SF, Kendall B, Tashiro H, et al. The frequency of p53, K-ras mutations, and microsatellite instability differs in uterine endometrioid and serous carcinoma: evidence of distinct molecular genetic pathways. Cancer 2000;88:814-824.
33. Matias-Guiu X, Catasus L, Bussaglia E, et al. Molecular pathology of endometrial hyperplasia and carcinoma. Hum Pathol 2001;32:569-577.
34. Sherman ME. Theories of endometrial carcinogenesis: a multidisciplinary approach. Mod Pathol 2000;13:295-308.
35. Hendrickson MR, Longacre TA, Kempson RI. The uterine corpus. In: Mills SE (ed). Sternberg's Diagnostic Surgical Pathology. Lippincott, Williams and Wilkins: Philadelphia, PA, 2004, pp 2460-2484.
36. Silverman MB, Roche PC, Kho RM, et al. Molecular and cytogenetic pretreatment risk assessment in endometrial carcinoma. Gynecol Oncol 2000;77:1-7.
37. Risinger JI, Hayes K, Maxwell GL, et al. PTEN mutation in endometrial cancers is associated with favorable clinical and pathological characteristics. Clin Cancer Res 1998;4:3005-3010.
38. Terakawa N, Kanamori Y, Yoshida S, et al. Loss of PTEN expression followed by Akt phosphorylation is a poor prognostic factor for patients with endometrial cancer. Endocr Relat Cancer 2003;10:203-208.
39. Carcangiu ML, Chambers JT, Voynick I, et al. Immunohistochemical evaluation of estrogen and progesterone receptor content in 183 patients with endometrial carcinoma. Part II: correlation between biochemical and immunohistochemical methods and survival. Am J Clin Pathol 1990;93:255-260.
40. Kadar N, Malfetano JH, Homesley HD. Steroid receptor concentrations in endometrial carcinoma: effect on survival in surgically staged patients. Gynecol Oncol 1993;50:281-286.
41. Berchuk A, Rodriguez G, Keeney RB, et al. Overexpression of HER-2/neu in endometrial cancer is associated with advanced stage disease. Am J Obstet Gynecol 1991;164:15-21.
42. Erdem O, Erdem M, Dursun A, et al. Angiogenesis, p53, and bcl-2 expression as prognostic indicators in endometrial cancer: comparison with traditional clinicopathologic variables. Int J Gynecol Pathol 2003;22:254-260.
43. Santin AD, Ballone S, Van Stedman S, et al. Amplification of c-erbB2 oncogene: a major prognostic indicator in uterine serous papillary carcinoma. Cancer 2005;104:1391-1397.
44. Prat J, Oliva E, Lerma E, et al. Uterine papillary serous adenocarcinoma: a 10-case study of p53 and c-erbB-2 expression and DNA content. Cancer 1994;74:1778-1783.
45. Sakuragi N, Ohkouchi T, Hareyama H, et al. Bcl-2 expression and prognosis of patients with endometrial carcinoma. Int J Cancer 1998;79:153-158.
46. Israels ED, Israels LG. The cell cycle. Oncologist 2000;5:510-513.
47. Kazanjian A, Wallis D, Au N, et al. Growth factor independence-1 is expressed in primary human neuroendocrine lung carcinomas and mediates the differentiation of murine pulmonary neuroendocrine cells. Cancer Res 2004;64:6874-6882.
48. Au N, Gown A, Cheang M, et al. P63 expression in lung carcinoma: a tissue microarray study of 408 cases. Appl Immunohistochem Mol Morphol 2004;12:240-247.
49. Hsu F, Nielsen TO, Alkushi A, et al. Multiple tumor microarrays are an effective quality assurance tool for diagnostic immunohistochemistry laboratories. Mod Pathol 2002;15:1374-1380.
50. Ordonez N. Role of immunohistochemistry in distinguishing epithelial peritoneal mesotheliomas from peritoneal and ovarian serous carcinomas. Am J Surg Pathol 1998;22:1203-1214.
51. Bair E, Tibshirani R. Semi-supervised methods to predict patient survival from gene expression data. PLoS Biology 2004;2:e108.
52. Carcangiu M, Chambers JT. Uterine papillary serous carcinoma: a study of 108 cases with emphasis on prognostic significance of associated endometrioid carcinoma, absence of invasion, and concomitant ovarian carcinoma. Gynecol Oncol 1992;47:298-305.
53. Pallares J, Bussaglia E, Martinez-Guitarte JL, et al. Immunohistochemical analysis of PTEN in endometrial carcinoma: a tissue microarray study with a comparison of four commercial antibodies in correlation with molecular abnormalities. Mod Pathol 2005;18:719-727.
54. Parker R, Huntsman DG, Lesack D, et al. Assessment of interlaboratory variation in the immunohistochemical determination of estrogen receptor status using a breast cancer tissue microarray. Am J Clin Path 2002;117:723-728.