The combination of Ki67, histological grade and estrogen receptor status identifies a low-risk group among 1,854 chemo-naïve women with N0/N1 primary breast cancer

SpringerPlus

Volumn 2, Issue 1, 2013, Pages 1-10

  Strand, Carina ^a   Bak, Martin ^b   Borgquist, Signe ^a   Chebil, Gunilla ^c   Falck, Anna Karin ^d   Fjällskog, Marie Louise ^e   Grabau, Dorthe ^a   Hedenfalk, Ingrid ^a   Jirström, Karin ^f   Klintman, Marie ^a   Malmström, Per ^a,g   Olsson, Hans ^h   Rydén, Lisa ^f   Stål, Olle ^h   Bendahl, Pär Ola ^a   Fernö, Mårten ^a  

^a LUND UNIVERSITY   (Sweden)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

^c Unilabs   (France)

^d HELSINGBORG HOSPITAL   (Sweden)

^e UPPSALA UNIVERSITY   (Sweden)

^f LUND UNIVERSITY   (Sweden)

^g LUND UNIVERSITY HOSPITAL   (Sweden)

^h LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Breast cancer; Chemo na ve; Ki67; Prognostic index; Proliferation

Indexed keywords

EID: 84876545565     PISSN: None     EISSN: 21931801     Source Type: Journal    
DOI: 10.1186/2193-1801-2-111     Document Type: Article

References (47)

1. Aebi S, Davidson T, Gruber G, Cardoso F (2011) Primary breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol Offic J Eur Soc Med Oncol/ESMO 22(Suppl 6):vi12-24.
2. Ahlin C, Zhou W, Holmqvist M, Holmberg L, Nilsson C, Jirstrom K, Blomqvist C, Amini RM, Fjallskog ML (2009) Cyclin A is a proliferative marker with good prognostic value in node-negative breast cancer. Canc Epidemiol Biomark Prev Publ Am Assoc Canc Res Cosponsored Am Soc Prev Oncol 18(9):2501-2506.
3. Aleskandarany MA, Rakha EA, Macmillan RD, Powe DG, Ellis IO, Green AR (2011) MIB1/Ki-67 labelling index can classify grade 2 breast cancer into two clinically distinct subgroups. Breast Cancer Res Treat 127(3):591-599.
4. Amadori D, Nanni O, Volpi A, Casadei Giunchi D, Marangolo M, Livi L, Ravaioli A, Rossi AP, Gambi A, Luzi Fedeli S, Perroni D, Scarpi E, Becciolini A, Silvestrini R (2008) Phase III randomized multicenter study on the effects of adjuvant CMF in patients with node-negative, rapidly proliferating breast cancer: twelve-year results and retrospective subgroup analysis. Breast Cancer Res Treat 108(2):259-264.
5. Baldini E, Camerini A, Sgambato A, Prochilo T, Capodanno A, Pasqualetti F, Orlandini C, Resta L, Bevilacqua G, Collecchi P (2006) Cyclin A and E2F1 overexpression correlate with reduced disease-free survival in node-negative breast cancer patients. Anticancer Res 26(6B):4415-4421.
6. Beresford MJ, Wilson GD, Makris A (2006) Measuring proliferation in breast cancer: practicalities and applications. Breast Cancer Res 8(6):216.
7. Borgquist S, Holm C, Stendahl M, Anagnostaki L, Landberg G, Jirstrom K (2008) Oestrogen receptors alpha and beta show different associations to clinicopathological parameters and their co-expression might predict a better response to endocrine treatment in breast cancer. J Clin Pathol 61(2):197-203.
8. Bukholm IR, Bukholm G, Nesland JM (2001) Over-expression of cyclin A is highly associated with early relapse and reduced survival in patients with primary breast carcinomas. Int J Canc J Int Canc 93(2):283-287.
9. Chebil G, Bendahl PO, Idvall I, Ferno M (2003) Comparison of immunohistochemical and biochemical assay of steroid receptors in primary breast cancer-clinical associations and reasons for discrepancies. Acta Oncol 42(7):719-725.
10. Colozza M, Azambuja E, Cardoso F, Sotiriou C, Larsimont D, Piccart MJ (2005) Proliferative markers as prognostic and predictive tools in early breast cancer: where are we now? Ann Oncol 16(11):1723-1739.
11. Cuzick J, Dowsett M, Pineda S, Wale C, Salter J, Quinn E, Zabaglo L, Mallon E, Green AR, Ellis IO, Howell A, Buzdar AU, Forbes JF (2011) Prognostic value of a combined estrogen receptor, progesterone receptor, Ki-67, and human epidermal growth factor receptor 2 immunohistochemical score and comparison with the Genomic Health recurrence score in early breast cancer. J Clin Oncol 29(32):4273-4278.
12. De Azambuja E, Cardoso F, de Castro G Jr, Colozza M, Mano MS, Durbecq V, Sotiriou C, Larsimont D, Piccart-Gebhart MJ, Paesmans M (2007) Ki-67 as prognostic marker in early breast cancer: a meta-analysis of published studies involving 12,155 patients. Br J Cancer 96(10):1504-1513.
13. Desmedt C, Haibe-Kains B, Wirapati P, Buyse M, Larsimont D, Bontempi G, Delorenzi M, Piccart M, Sotiriou C (2008) Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 14(16):5158-5165.
14. Dowsett M, Goldhirsch A, Hayes DF, Senn HJ, Wood W, Viale G (2007) International Web-based consultation on priorities for translational breast cancer research. Breast Cancer Res 9(6):81.
15. Dowsett M, Nielsen TO, A'Hern R, Bartlett J, Coombes RC, Cuzick J, Ellis M, Henry NL, Hugh JC, Lively T, McShane L, Paik S, Penault-Llorca F, Prudkin L, Regan M, Salter J, Sotiriou C, Smith IE, Viale G, Zujewski JA, Hayes DF (2011) Assessment of Ki67 in breast cancer: recommendations from the International Ki67 in Breast Cancer working group. J Natl Cancer Inst 103(22):1656-1664.
16. Eden P, Ritz C, Rose C, Ferno M, Peterson C (2004) "Good Old" clinical markers have similar power in breast cancer prognosis as microarray gene expression profilers. Eur J Cancer 40(12):1837-1841.
17. Ellis MJ, Tao Y, Luo J, A'Hern R, Evans DB, Bhatnagar AS, Chaudri Ross HA, von Kameke A, Miller WR, Smith I, Eiermann W, Dowsett M (2008) Outcome prediction for estrogen receptor-positive breast cancer based on postneoadjuvant endocrine therapy tumor characteristics. J Natl Cancer Inst 100(19):1380-1388.
18. Falck AK, Bendahl PO, Ingvar C, Isola J, Jonsson PE, Lindblom P, Lovgren K, Rennstam K, Ferno M, Rydén L (2012) Analysis of and prognostic information from disseminated tumour cells in bone marrow in primary breast cancer: a prospective observational study. BMC Cancer 12(1):403.
19. Goldhirsch A, Ingle JN, Gelber RD, Coates AS, Thurlimann B, Senn HJ (2009) Thresholds for therapies: highlights of the St Gallen International Expert Consensus on the primary therapy of early breast cancer 2009. Ann Oncol 20(8):1319-1329.
20. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ (2011) Strategies for subtypes--dealing with the diversity of breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 22(8):1736-1747.
21. Hansen S, Grabau DA, Sorensen FB, Bak M, Vach W, Rose C (2000) The prognostic value of angiogenesis by Chalkley counting in a confirmatory study design on 836 breast cancer patients. Clin Canc Res Offic J Am Assoc Canc Res 6(1):139-146.
22. Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S, Somerfield MR, Hayes DF, Bast RC Jr (2007) American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol 25(33):5287-5312.
23. Hietanen P, Blomqvist C, Wasenius VM, Niskanen E, Franssila K, Nordling S (1995) Do DNA ploidy and S-phase fraction in primary tumour predict the response to chemotherapy in metastatic breast cancer? Br J Cancer 71(5):1029-1032.
24. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JE, Liu ET, Bergh J, Kuznetsov VA, Miller LD (2006) Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 66(21):10292-10301.
25. Jones RL, Salter J, A'Hern R, Nerurkar A, Parton M, Reis-Filho JS, Smith IE, Dowsett M (2009) The prognostic significance of Ki67 before and after neoadjuvant chemotherapy in breast cancer. Breast Cancer Res Treat 116(1):53-68.
26. Klintman M, Bendahl PO, Grabau D, Lovgren K, Malmstrom P, Ferno M (2010) The prognostic value of Ki67 is dependent on estrogen receptor status and histological grade in premenopausal patients with node-negative breast cancer. Mod Pathol 23(2):251-259.
27. Kuhling H, Alm P, Olsson H, Ferno M, Baldetorp B, Parwaresch R, Rudolph P (2003) Expression of cyclins E, A, and B, and prognosis in lymph nodenegative breast cancer. J Pathol 199(4):424-431.
28. Luporsi E, Andre F, Spyratos F, Martin PM, Jacquemier J, Penault-Llorca F, Tubiana-Mathieu N, Sigal-Zafrani B, Arnould L, Gompel A, Egele C, Poulet B, Clough KB, Crouet H, Fourquet A, Lefranc JP, Mathelin C, Rouyer N, Serin D, Spielmann M, Haugh M, Chenard MP, Brain E, de Cremoux P, Bellocq JP (2012) Ki-67: level of evidence and methodological considerations for its role in the clinical management of breast cancer: analytical and critical review. Breast Cancer Res Treat 132(3):895-915.
29. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2005) Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 97(16):1180-1184.
30. Michalides R, van Tinteren H, Balkenende A, Vermorken JB, Benraadt J, Huldij J, van Diest P (2002) Cyclin A is a prognostic indicator in early stage breast cancer with and without tamoxifen treatment. Br J Cancer 86(3):402-408.
31. Munzone E, Botteri E, Sciandivasci A, Curigliano G, Nole F, Mastropasqua M, Rotmensz N, Colleoni M, Esposito A, Adamoli L, Luini A, Goldhirsch A, Viale G (2012) Prognostic value of Ki-67 labeling index in patients with nodenegative, triple-negative breast cancer. Breast Cancer Res Treat 134(1): 277-282.
32. Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, Hiller W, Fisher ER, Wickerham DL, Bryant J, Wolmark N (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Eng J Med 351(27):2817-2826.
33. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406(6797):747-752.
34. Peto R, Davies C, Godwin J, Gray R, Pan HC, Clarke M, Cutter D, Darby S, McGale P, Taylor C, Wang YC, Bergh J, Di Leo A, Albain K, Swain S, Piccart M, Pritchard K (2012) Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet 379(9814):432-444.
35. Ravdin PM, Siminoff LA, Davis GJ, Mercer MB, Hewlett J, Gerson N, Parker HL (2001) Computer program to assist in making decisions about adjuvant therapy for women with early breast cancer. J Clin Oncol 19(4):980-991
36. Rutgers E, Piccart-Gebhart MJ, Bogaerts J, Delaloge S, Veer LV, Rubio IT, Viale G, Thompson AM, Passalacqua R, Nitz U, Vindevoghel A, Pierga JY, Ravdin PM, Werutsky G, Cardoso F (2011) The EORTC 10041/BIG 03-04 MINDACT trial is feasible: results of the pilot phase. Eur J Cancer 47(18):2742-2749.
37. Rydén L, Jonsson PE, Chebil G, Dufmats M, Ferno M, Jirstrom K, Kallstrom AC, Landberg G, Stal O, Thorstenson S, Nordenskjold B (2005) Two years of adjuvant tamoxifen in premenopausal patients with breast cancer: a randomised, controlled trial with long-term follow-up. Eur J Cancer 41(2):256-264.
38. Schoenfeld DA (1983) Sample-size formula for the proportional-hazards regression model. Biometrics 39(2):499-503.
39. Skaland I, Janssen EA, Gudlaugsson E, Klos J, Kjellevold KH, Soiland H, Baak JP (2007) Phosphohistone H3 expression has much stronger prognostic value than classical prognosticators in invasive lymph node-negative breast cancer patients less than 55 years of age. Mod Pathol 20(12):1307-1315.
40. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lonning P, Borresen-Dale AL (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98(19):10869-10874.
41. Sotiriou C, Wirapati P, Loi S, Harris A, Fox S, Smeds J, Nordgren H, Farmer P, Praz V, Haibe-Kains B, Desmedt C, Larsimont D, Cardoso F, Peterse H, Nuyten D, Buyse M, Van de Vijver MJ, Bergh J, Piccart M, Delorenzi M (2006) Gene expression profiling in breast cancer: understanding the molecular basis of histologic grade to improve prognosis. J Natl Cancer Inst 98(4):262-272.
42. Strand C, Ahlin C, Bendahl PO, Fjallskog ML, Hedenfalk I, Malmstrom P, Ferno M (2012) Combination of the proliferation marker cyclin A, histological grade, and estrogen receptor status in a new variable with high prognostic impact in breast cancer. Breast Cancer Res Treat 131(1):33-40.
43. Swedish Breast Cancer Cooperative Group (1996) Randomized trial of two versus five years of adjuvant tamoxifen for postmenopausal early stage breast cancer. Swedish Breast Cancer Cooperative Group. J Natl Cancer Inst 88 (21):1543-1549.
44. Teschendorff AE, Miremadi A, Pinder SE, Ellis IO, Caldas C (2007) An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol 8(8):157.
45. Urruticoechea A, Smith IE, Dowsett M (2005) Proliferation marker Ki-67 in early breast cancer. J Clin Oncol 23(28):7212-7220.
46. Viale G, Regan MM, Mastropasqua MG, Maffini F, Maiorano E, Colleoni M, Price KN, Golouh R, Perin T, Brown RW, Kovacs A, Pillay K, Ohlschlegel C, Gusterson BA, Castiglione-Gertsch M, Gelber RD, Goldhirsch A, Coates AS (2008) Predictive value of tumor Ki-67 expression in two randomized trials of adjuvant chemoendocrine therapy for node-negative breast cancer. J Natl Cancer Inst 100(3):207-212.
47. Zujewski JA, Kamin L (2008) Trial assessing individualized options for treatment for breast cancer: the TAILORx trial. Future Oncol 4(5):603-610.