Proliferation markers and survival in early breast cancer: A systematic review and meta-analysis of 85 studies in 32,825 patients

Breast

Volumn 17, Issue 4, 2008, Pages 323-334

  Stuart Harris, R ^a   Caldas, C ^a   Pinder, S E ^b   Pharoah, P ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Early breast cancer; Meta analysis; Proliferation; Survival

Indexed keywords

BIOCHEMICAL MARKER; BROXURIDINE; CYCLINE; KI 67 ANTIGEN; THYMIDINE;

ARTICLE; BREAST CANCER; CANCER SURVIVAL; DISEASE FREE SURVIVAL; EARLY CANCER; EVIDENCE BASED MEDICINE; HUMAN; LABELING INDEX; MITOSIS INDEX; MULTIVARIATE ANALYSIS; OUTCOMES RESEARCH; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; PUBLISHING; SURVIVAL TIME; SYSTEMATIC REVIEW;

EID: 48849096940     PISSN: 09609776     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.breast.2008.02.002     Document Type: Article

References (96)

1. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365 (2005) 1687-1717
2. Lee A.H., Pinder S.E., Macmillan R.D., et al. Prognostic value of lymphovascular invasion in women with lymph node negative invasive breast carcinoma. Eur J Cancer 42 (2006) 357-362
3. Haybittle J.L., Blamey R.W., Elston C.W., et al. A prognostic index in primary breast cancer. Br J Cancer 45 (1982) 361-366
4. Sundquist M., Thorstenson S., Brudin L., and Nordenskjold B. Applying the Nottingham Prognostic Index to a Swedish breast cancer population. South East Swedish Breast Cancer Study Group. Breast Cancer Res Treat 53 (1999) 1-8
5. Rostgaard K., Mouridsen H.T., Vaeth M., Holst H., Olesen K.P., and Lynge E. A modified Nottingham prognostic index for breast cancer patients diagnosed in Denmark 1978-1994. Acta Oncol 40 (2001) 838-843
6. Blamey R.W., Ellis I.O., Pinder S.E., et al. Survival of invasive breast cancer according to the Nottingham Prognostic Index in cases diagnosed in 1990-1999. Eur J Cancer 43 (2007) 1548-1555
7. Blamey R.W., Pinder S.E., Ball G.R., et al. Reading the prognosis of the individual with breast cancer. Eur J Cancer 43 (2007) 1545-1547
8. Ravdin P.M., Siminoff L.A., Davis G.J., et al. Computer program to assist in making decisions about adjuvant therapy for women with early breast cancer. J Clin Oncol 19 (2001) 980-991
9. Olivotto I.A., Bajdik C.D., Ravdin P.M., et al. Population-based validation of the prognostic model ADJUVANT! for early breast cancer. J Clin Oncol 23 (2005) 2716-2725
10. Brenton J.D., Carey L.A., Ahmed A.A., and Caldas C. Molecular classification and molecular forecasting of breast cancer: ready for clinical application?. J Clin Oncol 23 (2005) 7350-7360
11. DerSimonian R., and Laird N. Meta-analysis in clinical trials. Control Clin Trials 7 (1986) 177-188
12. Higgins J.P., Thompson S.G., Deeks J.J., and Altman D.G. Measuring inconsistency in meta-analyses. BMJ 327 (2003) 557-560
13. Egger M., Davey Smith G., Schneider M., and Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 315 (1997) 629-634
14. Duval S., and Tweedie R. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56 (2000) 455-463
15. Jensen V., Ladekarl M., Holm-Nielsen P., Melsen F., and Soerensen F.B. The prognostic value of oncogenic antigen 519 (OA-519) expression and proliferative activity detected by antibody MIB-1 in node-negative breast cancer. J Pathol 176 (1995) 343-352
16. Keshgegian A.A., and Cnaan A. Proliferation markers in breast carcinoma. Mitotic figure count, S-phase fraction, proliferating cell nuclear antigen, Ki-67 and MIB-1. Am J Clin Pathol 104 (1995) 42-49
17. Pinder S.E., Wencyk P., Sibbering D.M., et al. Assessment of the new proliferation marker MIB1 in breast carcinoma using image analysis: associations with other prognostic factors and survival. Br J Cancer 71 (1995) 146-149
18. Querzoli P., Ferretti S., Albonico G., et al. Application of quantitative analysis to biologic profile evaluation in breast cancer. Cancer 76 (1995) 2510-2517
19. Veronese S.M., Maisano C., and Scibilia J. Comparative prognostic value of Ki-67 and MIB-1 proliferation indices in breast cancer. Anticancer Res 16 (1995) 2717-2722
20. Weikel W., Brumm C., Wilkens C., Beck T., and Knapstein P.G. Growth fractions (Ki-67) in primary breast cancers, with particular reference to node-negative tumors. Cancer Detect Prev 19 (1995) 446-450
21. Bevilacqua P., Verderio P., Barbareschi M., et al. Lack of prognostic significance of the monoclonal antibody Ki-S1, a novel marker of proliferative activity, in node-negative breast carcinoma. Breast Cancer Res Treat 37 (1996) 123-133
22. Brown R.W., Allred C.D., Clark G.M., Osborne C.K., and Hilsenbeck S.G. Prognostic value of Ki-67 compared to S-phase fraction in axillary node-negative breast cancer. Clin Cancer Res 2 (1996) 585-592
23. Domagala W., Markiewski M., Harezga B., Dukowicz A., and Osborn M. Prognostic significance of tumor cell proliferation rate as determined by the MIB-1 antibody in breast carcinoma: its relationship with vimentin and p53 protein. Clin Cancer Res 2 (1996) 147-154
24. Haerslev T., Jacobsen G.K., and Zedeler K. Correlation of growth fraction by Ki-67 and proliferating cell nuclear antigen (PCNA) immunohistochemistry with histopathological parameters and prognosis in primary breast carcinomas. Breast Cancer Res Treat 37 (1996) 101-113
25. Pierga J.Y., Leroyer A., Viehl P., Mosseri V., Chevillard S., and Magdelenat H. Long term prognostic value of growth fraction determination by Ki-67 immunostaining in primary operable breast cancer. Breast Cancer Res Treat 37 (1996) 57-64
26. Pietilainen T., Lipponen P., Aaltomaa S., Eskelinen M., Kosma V.M., and Syrjanen K. The important prognostic value of Ki-67 expression as determined by image analysis in breast cancer. J Cancer Res Clin Oncol 122 (1996) 687-692
27. Querzoli P., Albonico G., Ferretti S., et al. MIB-1 proliferative activity in invasive breast cancer measured by image analysis. J Clin Pathol 49 (1996) 926-930
28. Seshadri R., Leong A.S., McCaul K., Firgaira F.A., Setlur V., and Horsfall D.J. Relationship between p53 gene abnormalities and other tumour characteristics in breast-cancer prognosis. Int J Cancer 69 (1996) 135-141
29. Molino A., Micciolo R., Turazza M., et al. Ki-67 immunostaining in 322 primary breast cancers: associations with clinical and pathological variables and prognosis. Int J Cancer 74 (1997) 433-437
30. Railo M., Lundin J., Haglund C., von Smitten K., von Boguslawsky K., and NordlingKi-67p53 S. Er-receptors, ploidy and S-phase as prognostic factors in T1 node negative breast cancer. Acta Oncol 36 (1997) 369-374
31. Biesterfeld S., Kluppel D., Koch R., et al. Rapid and prognostically valid quantification of immunohistochemical reactions by immunohistometry of the most positive tumour focus. A prospective follow-up study on breast cancer using antibodies against MIB-1, PCNA, ER, and PR. J Pathol 185 (1998) 25-31
32. Clahsen P.C., van de Velde C.J., Duval C., et al. p53 protein accumulation and response to adjuvant chemotherapy in premenopausal women with node-negative early breast cancer. J Clin Oncol 16 (1998) 470-479
33. Harbeck N., Dettmar P., Thomssen C., et al. Prognostic impact of tumor biological factors on survival in node-negative breast cancer. Anticancer Res 18 (1998) 2187-2197
34. Iacopetta B., Grieu F., Powell B., Soong R., McCaul K., and Seshadri R. Analysis of p53 gene mutation by polymerase chain reaction-single strand conformation polymorphism provides independent prognostic information in node-negative breast cancer. Clin Cancer Res 4 (1998) 1597-1602
35. Jacquemier J.D., Penault-Llorca F.M., Bertucci F., et al. Angiogenesis as a prognostic marker in breast carcinoma with conventional adjuvant chemotherapy: a multiparametric and immunohistochemical analysis. J Pathol 184 (1998) 130-135
36. Jansen R.L., Hupperets P.S., Arends J.W., et al. MIB-1 labelling index is an independent prognostic marker in primary breast cancer. Br J Cancer 78 (1998) 460-465
37. Wiesener B., Hauser-Kronberger C.E., Zipperer E., Dietze O., Menzel C.H., and Hacker G.W. p34cdc2 in invasive breast cancer: relationship to DNA content, Ki67 index and c-erbB-2 expression. Histopathology 33 (1998) 522-530
38. Clahsen P.C., van de Velde C.J., Duval C., et al. The utility of mitotic index, oestrogen receptor and Ki-67 measurements in the creation of novel prognostic indices for node-negative breast cancer. Eur J Surg Oncol 25 (1999) 356-363
39. Lockwood C.A., Ricciardelli C., Raymond W.A., Seshadri R., McCaul K., and Horsfall D.J. A simple index using video image analysis to predict disease outcome in primary breast cancer. Int J Cancer 84 (1999) 203-208
40. Rudolph P., Olsson H., Bonatz G., et al. Correlation between p53, c-erbB-2, and topoisomerase II alpha expression, DNA ploidy, hormonal receptor status and proliferation in 356 node-negative breast carcinomas: prognostic implications. J Pathol 187 (1999) 207-216
41. Rudolph P., MacGrogan G., Bonichon F., et al. Prognostic significance of Ki-67 and topoisomerase II alpha expression in infiltrating ductal carcinoma of the breast. A multivariate analysis of 863 cases. Breast Cancer Res Treat 55 (1999) 61-71
42. Rudolph P., Alm P., Heidebrecht H.-J., et al. Immunologic proliferation marker Ki-S2 as prognostic indicator for lymph node-negative breast cancer. J Natl Cancer Inst 91 (1999) 271-278
43. Thor A.D., Liu S., Moore II D.H., and Edgerton S.M. Comparison of mitotic index, in vitro bromodeoxyuridine labeling, and MIB-1 assays to quantitate proliferation in breast cancer. J Clin Oncol 17 (1999) 470-477
44. Goodson III W.H., Moore II D.H., Ljung B.-M., et al. The prognostic value of proliferation indices: a study with in vivo bromodeoxyuridine and Ki-67. Breast Cancer Res Treat 59 (2000) 113-123
45. Leong A.C., Hanby A.M., Potts H.W., et al. Cell cycle proteins do not predict outcome in grade I infiltrating ductal carcinoma of the breast. Int J Cancer 89 (2000) 26-31
46. Lau R., Grimson R., Sansome C., Tornos C., and Moll U.M. Low levels of cell cycle inhibitor p27kip1 combined with high levels of Ki-67 predict shortened disease-free survival in T1 and T2 invasive breast carcinomas. Int J Oncol 18 (2001) 17-23
47. Liu S., Edgerton S.M., Moore II D.H., and Thor A.D. Measures of cell turnover (proliferation and apoptosis) and their association with survival in breast cancer. Clin Cancer Res 7 (2001) 1716-1723
48. Pinto A.E., Andre S., Pereira T., Nobrega S., and Soares J. Prognostic comparative study of S-phase fraction and Ki-67 index in breast carcinoma. J Clin Pathol 54 (2001) 543-549
49. Billgren A.-M., Tani E., Liedberg A., Skoog L., and Rutqvist L.E. Prognostic significance of tumor cell proliferation analyzed in fine needle aspirates from primary breast cancer. Breast Cancer Res Treat 71 (2002) 161-170
50. Molino A., Pedersini R., Micciolo R., et al. Relationship between the thymidine labeling and Ki-67 proliferative indices in 126 breast cancer patients. Appl Immunohistochem Mol Morphol 10 (2002) 304-309
51. Bukholm I.R., Bukholm G., Holm R., and Nesland J.M. Association between histology grade, expression of HsMCM2, and cyclin A in human invasive breast carcinomas. J Clin Pathol 56 (2003) 368-373
52. Gonzalez M.A., Pinder S.E., Callagy G., et al. Minichromosome maintenance protein 2 is a strong independent prognostic marker in breast cancer. J Clin Oncol 21 (2003) 4306-4313
53. Joensuu H., Isola J., Lundin M., et al. Amplification of erbB2 and erbB2 expression are superior to estrogen receptor status as risk factors for distant recurrence in pT1N0M0 breast cancer: a nationwide population-based study. Clin Cancer Res 9 (2003) 923-930
54. Offersen B.V., Sorensen F.B., Knoop A., Overgaard J., and Danish Breast Cancer Cooperative Tumour Biology Committee. The prognostic relevance of estimates of proliferative activity in early breast cancer. Histopathology 43 (2003) 573-582
55. Rudolph P., Kuhling H., Alm P., et al. Differential prognostic impact of the cyclins E and B in premenopausal and postmenopausal women with lymph node-negative breast cancer. Int J Cancer 105 (2003) 674-680
56. Trihia H., Murray S., Price K., et al. Ki-67 expression in breast carcinoma: its association with grading systems, clinical parameters, and other prognostic factors - a surrogate marker?. Cancer 97 (2003) 1321-1331
57. Yamashita H., Nishio M., Toyama T., et al. Coexistence of HER2 over-expression and p53 protein accumulation is a strong prognostic molecular marker in breast cancer. Breast Cancer Res 6 (2004) R24-R30
58. Biesterfeld S., Noll I., Noll E., Wohltmann D., and Bocking A. Mitotic frequency as a prognostic factor in breast cancer. Hum Pathol 26 (1995) 47-52
59. Jannink I., van Diest P.J., and Baak J.P. Comparison of the prognostic value of four methods to assess mitotic activity in 186 invasive breast cancer patients: classical and random mitotic activity assessments with correction for volume percentage of epithelium. Hum Pathol 26 (1995) 1086-1092
60. de Jong J.S., van Dienst P.J., and Baak J.P.A. Hot spot microvessel density and the mitotic activity index are strong additional prognostic indicators in invasive breast cancer. Histopathology 36 (2000) 306-312
61. Simpson J.F., Gray R., Dressler L.G., et al. Prognostic value of histologic grade and proliferative activity in axillary node-positive breast cancer: results from the Eastern Cooperative Oncology Group Companion Study, EST 4189. J Clin Oncol 18 (2000) 2059-2069
62. Biesterfeld S., and Reitmaier M. Re-evaluation of prognostic mitotic figure counting in breast cancer: results of a prospective clinical follow-up study. Anticancer Res 21 (2001) 589-594
63. Hasebe T., Sasaki S., Imoto S., and Ochiai A. Histological characteristics of tumors in blood vessels play an important role in tumor progression of invasive ductal carcinoma of the breast. Cancer Sci 94 (2003) 158-165
64. Hasebe T., Sasaki S., Imoto S., and Ochiai A. Significance of nodal metastatic tumor characteristics in nodal metastasis and prognosis of patients with invasive ductal carcinoma of the breast. Cancer Sci 94 (2003) 181-187
65. Manders P., Bult P., Sweep C.G.J., Tjan-Heijnen V.C.G., and Beex L.V. The prognostic value of the mitotic activity index in patients with primary breast cancer who were not treated with adjuvant systemic therapy. Breast Cancer Res Treat 77 (2003) 77-84
66. Medri L., Volpi A., Nanni O., et al. Prognostic relevance of mitotic activity in patients with node-negative breast cancer. Mod Pathol 16 (2003) 1067-1075
67. Michels J.J., Marnay J., Delozier T., Denoux Y., and Chasle J. Proliferative activity in primary breast carcinomas is a salient prognostic factor. Cancer 100 (2004) 455-464
68. Haerslev T., and Jacobsen G.K. An immunohistochemical study of p53 with correlations to histopathological parameters, c-erbB-2, proliferating cell nuclear antigen, and prognosis. Hum Pathol 26 (1995) 295-301
69. Schonborn I., Zschiesche W., Minguillon C., et al. Prognostic value of proliferating cell nuclear antigen and c-erbB-2 compared with conventional histopathological factors in breast cancer. J Cancer Res Clin Oncol 121 (1995) 115-122
70. Heimann R., Ferguson D., Recant W.M., and Hellmann S. Breast cancer metastatic phenotype as predicted by histologic tumor markers. Cancer J Sci Am 3 (1997) 224-229
71. Sheen-Chen S.-M., Eng H.-L., Chou F.-F., and Chen W.-J. The prognostic significance of proliferating cell nuclear antigen in patients with lymph node-positive breast cancer. Arch Surg 132 (1997) 264-267
72. Chu J.-S., Huang C.-S., and Chang K.-J. Proliferating cell nuclear antigen (PCNA) immunolabeling as a prognostic factor in invasive ductal carcinoma of the breast in Taiwan. Cancer Lett 131 (1998) 145-152
73. Horiguchi J., Iino Y., Takei H., et al. Long-term prognostic value of PCNA labeling index in primary operable breast cancer. Oncol Rep 5 (1998) 641-644
74. Kato T., Kimura T., Miyakawa R., et al. Clinicopathologic study associated with long-term survival in Japanese patients with node-negative breast cancer. Br J Cancer 82 (2000) 404-411
75. Paradiso A., Mangia A., Barletta A., et al. Heterogeneity of intratumour proliferative activity in primary breast cancer: biological and clinical aspects. Eur J Cancer 31A (1995) 911-916
76. Silvestrini R., Daidone M.G., Luisi A., et al. Biologic and clinicopathologic factors as indicators of specific relapse types in node-negative breast cancer. J Clin Oncol 13 (1995) 697-704
77. Silvestrini R., Daidone M.G., Luisi A., Mastore M., Leutner M., and Salvadori B. Cell proliferation in 3800 node-negative breast cancers: consistency over time of biological and clinical information provided by 3H-thymidine labelling index. Int J Cancer 74 (1997) 122-127
78. Daidone M.G., Veneroni S., Benini E., et al. Biological markers as indicators of response to primary and adjuvant chemotherapy in breast cancer. Int J Cancer 84 (1999) 580-586
79. Daidone M.G., Luisi A., Martelli G., et al. Biomarkers and outcome after tamoxifen treatment in node-positive breast cancers from elderly women. Br J Cancer 82 (2000) 270-277
80. Silvestrini R., Luisi A., Zambetti M., et al. Cell proliferation and outcome following doxorubicin plus CMF regimens in node-positive breast cancer. Int J Cancer 87 (2000) 405-411
81. Scarpi E., De Paola F., Sarti M., et al. Biomarker prediction of clinical outcome in operable breast cancer patients treated with tamoxifen. Breast Cancer Res Treat 68 (2001) 101-110
82. Ozmen V., Cabioglu N., Dolay K., et al. Biological considerations in locally advanced breast cancer treated with anthracycline-based neoadjuvant chemotherapy: thymidine labelling index is an independent indicator of clinical outcome. Breast Cancer Res Treat 68 (2001) 147-157
83. Mirza A.N., Mirza N.Q., Vlastos G., and Singletary S.E. Prognostic factors in node-negative breast cancer: a review of studies with sample size more than 200 and follow-up more than 5 years. Ann Surg 235 (2002) 10-26
84. Esteva F.J., and Hortobagyi G.N. Prognostic molecular markers in early breast cancer. Breast Cancer Res 6 (2004) 109-118
85. Rampaul R.S., Pinder S.E., Elston C.W., and Ellis I.O. Prognostic and predictive factors in primary breast cancer and their role in patient management: the Nottingham breast team. Eur J Surg Oncol 27 (2001) 229-238
86. Pereira H., Pinder S.E., Sibbering D.M., Galea M.H., and Elston C.W. Pathological prognostic factors in breast cancer. IV: should you be a typer or a grader? A comparative study of two histological prognostic features in operable breast carcinoma. Histopathology 27 (1995) 219-226
87. van Diest P.J., van der Wall E., and Baak J.P. Prognostic value of proliferation in invasive breast cancer: a review. J Clin Pathol 57 (2004) 675-681
88. Urruticoechea A., Smith I.E., and Dowsett M. Proliferation marker Ki-67 in early breast cancer. J Clin Oncol 23 (2005) 7212-7220
89. de Azambuja E., Cardoso F., de Castro Jr. G., et al. Ki-67 as a prognostic marker in early breast cancer: a meta-analysis of published studies involving 12 155 patients. Br J Cancer 96 (2007) 1504-1513
90. Marrelli D., Pinto E., Neri A., et al. Mib-1 proliferation index is an independent predictor of lymph node metastasis in invasive breast cancer: a prospective study on 675 patients. Oncol Rep 15 (2006) 425-429
91. Jalava P., Kuopio T., Juntti-Patinen L., Kotkansolo T., Kronqvist P., and Collan Y. Ki-67 immunohistochemistry: a valuable marker in prognostication but with a risk of misclassification: proliferation subgroups formed based on Ki67 immunoreactivity and standardized mitotic index. Histopathology 48 (2006) 674-682
92. Sotiriou C., and Piccart M.J. Taking gene-expression profiling to the clinic: when will molecular signatures become relevant to patient care?. Nat Rev Cancer 7 (2007) 545-553
93. Naderi A., Teschendorff A.E., Barbosa-Morais N.L., et al. A gene-expression signature to predict survival in breast cancer across independent data sets. Oncogene 26 (2007) 1507-1516
94. Teschendorff A.E., Naderi A., Barbosa-Morais N.L., et al. A consensus prognostic gene expression classifier for ER positive breast cancer. Genome Biol 7 (2006) R101
95. Teschendorff A.E., Miremadi A., Pinder S.E., Ellis I.O., and Caldas C. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol 8 (2007) R157
96. Callagy G.M., Pharoah P.D., Pinder S.E., et al. Bcl-2 is a prognostic marker in breast cancer independently of the Nottingham prognostic index. Clin Cancer Res 12 (2006) 2468-2475