A Ki67/BCL2 index based on immunohistochemistry is highly prognostic in ER-positive breast cancer

Journal of Pathology

Volumn 226, Issue 1, 2012, Pages 97-107

  Ali, H Raza ^a,b   Dawson, Sarah Jane ^a,b,c   Blows, Fiona M ^d   Provenzano, Elena ^b,c,e   Leung, Samuel ^f   Nielsen, Torsten ^f   Pharoah, Paul D ^a,d,e   Caldas, Carlos ^a,b,c,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e Cambridge Experimental Cancer Medicine Centre ECMC   (United Kingdom)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

BCL2; breast cancer; ER positive; immunohistochemistry; Ki67; TMA

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; KI 67 ANTIGEN; PROGESTERONE RECEPTOR; PROTEIN BCL 2; TUMOR MARKER;

ARTICLE; BREAST CANCER; BREAST TUMOR; CANCER GRADING; CANCER GROWTH; CANCER INVASION; CANCER MORTALITY; CANCER RISK; CANCER SURVIVAL; EXTERNAL VALIDITY; FEMALE; FOLLOW UP; HIGH RISK PATIENT; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; PREDICTIVE VALUE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; TISSUE MICROARRAY; TUMOR VOLUME;

ADULT; AGED; BREAST NEOPLASMS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; KI-67 ANTIGEN; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ESTROGEN; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 82755182561     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2976     Document Type: Article

References (55)

1. Perou C, Sørlie T, Eisen M, et al., Molecular portraits of human breast tumours. Nature 2000; 406: 747-752.
2. van de Vijver MJ, He YD, van't Veer LJ, et al., A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 2002; 347: 1999-2009. (Pubitemid 35461656)
3. Paik S, Tang G, Shak S, et al., Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J Clin Oncol 2006; 24: 3726-3734. (Pubitemid 46622311)
4. Paik S,. Development and clinical utility of a 21-gene recurrence score prognostic assay in patients with early breast cancer treated with tamoxifen. Oncologist 2007; 12: 631-635. (Pubitemid 47036199)
5. Buyse M, Loi S, van't Veer L, et al., Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. J Natl Cancer Inst 2006; 98: 1183-1192. (Pubitemid 44390989)
6. Nielsen TO, Parker JS, Leung S, et al., A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer. Clin Cancer Res 2010; 16: 5222-5232.
7. Parker J, Mullins M, Cheang M, et al., Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009; 27: 1160-1167.
8. Sotiriou C, Wirapati P, Loi S, et al., Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst 2006; 98: 262-272. (Pubitemid 43264710)
9. Teschendorff AE, Naderi A, Barbosa-Morais NL, et al., A consensus prognostic gene expression classifier for ER positive breast cancer. Genome Biol 2006; 7: R101.
10. Naderi A, Teschendorff AE, Barbosa-Morais NL, et al., A gene-expression signature to predict survival in breast cancer across independent data sets. Oncogene 2007; 26: 1507-1516. (Pubitemid 46340809)
11. Reyal F, van Vliet M, Armstrong N, et al., A comprehensive analysis of prognostic signatures reveals the high predictive capacity of the proliferation, immune response and RNA splicing modules in breast cancer. Breast Cancer Res 2008; 10: R93.
12. Sørlie T, Perou C, Tibshirani R, et al., Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001; 98: 10869-10874. (Pubitemid 32878711)
13. Desmedt C, Haibe-Kains B, Wirapati P, et al., Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 2008; 14: 5158-5165.
14. Yerushalmi R, Woods R, Ravdin P, et al., Ki67 in breast cancer: prognostic and predictive potential. Lancet Oncol 2010; 11: 174-183.
15. Colozza M, Sidoni A, Piccart-Gebhart M,. Value of Ki67 in breast cancer: the debate is still open. Lancet Oncol 2010; 11: 414-415.
16. Stuart-Harris R, Caldas C, Pinder SE, et al., Proliferation markers and survival in early breast cancer: a systematic review and meta-analysis of 85 studies in 32,825 patients. Breast 2008; 17: 323-334.
17. Zinkel S, Gross A, Yang E,. BCL2 family in DNA damage and cell cycle control. Cell Death Differ 2006; 13: 1351-1359. (Pubitemid 44057470)
18. O'Reilly LA, Huang DC, Strasser A,. The cell death inhibitor Bcl-2 and its homologues influence control of cell cycle entry. EMBO J 1996; 15: 6979-6990. (Pubitemid 27023269)
19. Greider C, Chattopadhyay A, Parkhurst C, et al., BCL-x(L) and BCL2 delay Myc-induced cell cycle entry through elevation of p27 and inhibition of G1 cyclin-dependent kinases. Oncogene 2002; 21: 7765-7775. (Pubitemid 35398834)
20. Pietenpol JA, Papadopoulos N, Markowitz S, et al., Paradoxical inhibition of solid tumor cell growth by bcl2. Cancer Res 1994; 54: 3714-3717. (Pubitemid 24241185)
21. Hockenbery D, Nunez G, Milliman C, et al., Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 1990; 348: 334-336. (Pubitemid 120029101)
22. Huang DC, O'Reilly LA, Strasser A, et al., The anti-apoptosis function of Bcl-2 can be genetically separated from its inhibitory effect on cell cycle entry. EMBO J 1997; 16: 4628-4638. (Pubitemid 27326600)
23. Callagy G, Pharoah P, Pinder S, et al., Bcl-2 is a prognostic marker in breast cancer independently of the Nottingham Prognostic Index. Clin Cancer Res 2006; 12: 2468-2475.
24. Dawson SJ, Makretsov N, Blows FM, et al., BCL2 in breast cancer: a favourable prognostic marker across molecular subtypes and independent of adjuvant therapy received. Br J Cancer 2010; 103: 668-675.
25. Abdel-Fatah TM, Powe DG, Ball G, et al., Proposal for a modified grading system based on mitotic index and Bcl2 provides objective determination of clinical outcome for patients with breast cancer. J Pathol 2010; 222: 388-399.
26. Lesueur F, Pharoah P, Laing S, et al., Allelic association of the human homologue of the mouse modifier Ptprj with breast cancer. Hum Mol Genet 2005; 14: 2349-2356. (Pubitemid 41417997)
27. Cheang MC, Chia SK, Voduc D, et al., Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 2009; 101: 736-750.
28. Kononen J, Bubendorf L, Kallioniemi A, et al., Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nature Med 1998; 4: 844-847. (Pubitemid 28331029)
29. Brown LA, Irving J, Parker R, et al., Amplification of EMSY, a novel oncogene on 11q13, in high grade ovarian surface epithelial carcinomas. Gynecol Oncol 2006; 100: 264-270. (Pubitemid 43075259)
30. Pharoah PD, Caldas C,. Genetics: how to validate a breast cancer prognostic signature. Nature Rev Clin Oncol 2010; 7: 615-616.
31. Blows F, Driver K, Schmidt M, et al., Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10,159 cases from 12 studies. PLoS Med 2010; 7: e1000279.
32. Altman DG, Lyman GH,. Methodological challenges in the evaluation of prognostic factors in breast cancer. Breast Cancer Res Treat 1998; 52: 289-303. (Pubitemid 29056101)
33. Altman DG,. Prognostic models: a methodological framework and review of models for breast cancer. Cancer Invest 2009; 27: 235-243.
34. Hoppin JA, Tolbert PE, Taylor JA, et al., Potential for selection bias with tumor tissue retrieval in molecular epidemiology studies. Ann Epidemiol 2002; 12: 1-6. (Pubitemid 34003065)
35. Ali AM, Dawson SJ, Blows FM, et al., Comparison of methods for handling missing data on immunohistochemical markers in survival analysis of breast cancer. Br J Cancer 2011; 104: 693-699.
36. Royston P,. Multiple imputation of missing values. Stata J 2004; 4: 227-241.
37. Royston P,. Multiple imputation of missing values: further update of ice, with an emphasis on categorical variables. Stata J 2009; 9: 466-477.
38. Moons KGM, Donders RART, Stijnen T, et al., Using the outcome for imputation of missing predictor values was preferred. J Clin Epidemiol 2006; 59: 1092-1101. (Pubitemid 44389818)
39. Azzato E, Greenberg D, Shah M, et al., Prevalent cases in observational studies of cancer survival: do they bias hazard ratio estimates? Br J Cancer 2009; 100: 1806-1811.
40. McShane LM, Altman DG, Sauerbrei W, et al., REporting recommendations for tumor MARKer prognostic studies (REMARK). J Natl Cancer Inst 2005; 97: 1180-1184. (Pubitemid 41258223)
41. 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. (Pubitemid 40051905)
42. Aleskandarany MA, Rakha EA, Macmillan RD, et al., MIB1/Ki-67 labelling index can classify grade 2 breast cancer into two clinically distinct subgroups. Breast Cancer Res Treat 2011; 127: 591-599.
43. Gerdes J, Lemke H, Baisch H, et al., Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 1984; 133: 1710-1715. (Pubitemid 14035254)
44. Loddo M, Kingsbury SR, Rashid M, et al., Cell-cycle-phase progression analysis identifies unique phenotypes of major prognostic and predictive significance in breast cancer. Br J Cancer 2009; 100: 959-970.
45. Tsujimoto Y, Finger LR, Yunis J, et al., Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 1984; 226: 1097-1099. (Pubitemid 15217831)
46. Silvestrini R, Veneroni S, Daidone MG, et al., The Bcl-2 protein: a prognostic indicator strongly related to p53 protein in lymph node-negative breast cancer patients. J Natl Cancer Inst 1994; 86: 499-504. (Pubitemid 24111005)
47. Quinn CM, Ostrowski JL, Harkins L, et al., Loss of bcl-2 expression in ductal carcinoma in situ of the breast relates to poor histological differentiation and to expression of p53 and c-erbB-2 proteins. Histopathology 1998; 33: 531-536. (Pubitemid 28563378)
48. Ruiz C, Seibt S, Al Kuraya K, et al., Tissue microarrays for comparing molecular features with proliferation activity in breast cancer. Int J Cancer 2006; 118: 2190-2194.
49. Callagy G, Cattaneo E, Daigo Y, et al., Molecular classification of breast carcinomas using tissue microarrays. Diagn Mol Pathol 2003; 12: 27-34. (Pubitemid 36255267)
50. Rakha EA, Reis-Filho JS, Ellis IO,. Combinatorial biomarker expression in breast cancer. Breast Cancer Res Treat 2010; 120: 293-308.
51. Dunnwald L, Rossing M, Li C,. Hormone receptor status, tumor characteristics, and prognosis: a prospective cohort of breast cancer patients. Breast Cancer Res 2007; 9: R6.
52. Carey LA, Perou CM, Livasy CA, et al., Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. J Am Med Assoc 2006; 295: 2492-2502. (Pubitemid 43854964)
53. Cheang M, Voduc D, Bajdik C, et al., Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 2008; 14: 1368-1376. (Pubitemid 351413917)
54. Kennecke H, Yerushalmi R, Woods R, et al., Metastatic behavior of breast cancer subtypes. J Clin Oncol 2010; 28: 3271-3277.
55. Voduc KD, Cheang MC, Tyldesley S, et al., Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol 2010; 28: 1684-1691.