Triple Negative Breast Cancer
Authors:
J. Navrátil 1; P. Fabian 2; M. Palacova 1; K. Petrakova 1; R. Vyzula 1; M. Svoboda 1,3,4
Authors place of work:
Klinika komplexní onkologické péče, Masarykův onkologický ústav, Brno
1; Oddělení onkologické patologie, Masarykův onkologický ústav, Brno
2; Oddělení epidemiologie a genetiky nádorů, Masarykův onkologický ústav, Brno
3; Lékařská fakulta, MU, Brno
4
Published in the journal:
Klin Onkol 2015; 28(6): 405-415
Category:
Přehledy
doi:
https://doi.org/10.14735/amko2015405
Summary
Background:
In the Czech Republic, around 6,500 women get breast cancer each year; out of this number, nearly 1,000 women are triple negative subtype. Triple negative breast cancer is characterized by lack of expression of α-estrogen, progesterone, and HER2 receptors. Vast majority of these cases are low-differentiated carcinomas, majority belonging to the basal-like subgroup defined originally by DNA chips. Clinically, they are characterized by greater aggressiveness, frequent rate of local recurrence and organ metastases. They are more common in younger women and are associated with the occurrence of hereditary forms of breast cancer caused by pathogenic mutations in the BRCA1 gene and in rare cases also BRCA2.
Aim:
The objective of this review is to provide comprehensive information about current knowledge of triple negative breast cancer. This paper summarizes information about epidemiology and etiopathogenesis of this disease, describes risk factors for both sporadic and hereditary forms of triple negative breast cancer, addresses histopathologic and molecular classification of triple negative breast cancer, and these characteristics associates with treatment and prediction of disease development. The article also addresses new anticancer drugs tested for triple negative breast cancer.
Conclusion:
Triple negative breast cancer is a heterogeneous group of diseases with limited therapeutic options. The key to further shift in therapy is detailed knowledge of its clinical and molecular diversity and identification of predictive biomarkers. Further improvement of therapy results of triple negative breast cancer cannot be expected before targeted therapy of this disease is found.
Key words:
breast cancer – triple negative breast cancer – BRCA mutation – chemotherapy – basal-like
This work was supported by grant MH CZ – RVO (MMCI, 00209805) and No. NT/14599-32013.
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE recommendation for biomedical papers.
Submitted:
26. 11. 2015
Accepted:
3. 12. 2015
Zdroje
1. Úzis.cz [internetová stránka]. Ústav zdravotnických informací a statistiky ČR. Národní onkologický registr. UZIS ČR 2010– 2014 [citováno 1. září 2015]. Dostupné z: www.uzis.cz/ registry-nzis/ nor.
2. Svoboda M, Navrátil J, Fabián P. Triple-negativní karcinom prsu: analýza souboru pacientek diagnostikovaných a/ nebo léčených v Masarykově onkologickém ústavu v letech 2004 až 2009. Klin Onkol 2012; 25(3): 188– 198. doi: 10.14735/ amko2012188.
3. Dietze EC, Sistrunk C, Carboni MG et al. Triple-negative breast cancer in African-American women: disparities versus biology. Nat Rev Cancer 2015; 15(4): 248– 254. doi: 10.1038/ nrc3896.
4. Kurian AW, Fish K, Shema SJ et al. Lifetime risks of specific breast cancer subtypes among women in four racial/ ethnic groups. Breast Cancer Res 2010; 12(6): R99. doi: 10.1186/ bcr2780.
5. Giordano SH. A review of the diagnosis and management of male breast cancer. Oncologist 2005; 10(7): 471– 479.
6. Giordano SH, Cohen DS, Buzdar AU et al. Breast carcinoma in men: a population-based study. Cancer 2004; 101(1): 51– 57.
7. Boyle P. Triple-negative breast cancer: epidemiological considerations and recommendations. Ann Oncol 2005; 16 (Suppl 6): vi7– vi12.
8. Amirikia KC, Mills P, Bush J et al. Higher population-based incidence rates of triple-negative breast cancer among young African-American women: implications for breast cancer screening recommendations. Cancer 2011; 117(12): 2747– 2753. doi: 10.1002/ cncr.25862.
9. Pijpe A, Andrieu N, Easton DF et al. Exposure to diagnostic radiation and risk of breast cancer among carriers of BRCA1/ 2 mutations: retrospective cohort study (GENE-RAD-RISK). BMJ 2012; 345: e5660. doi: 10.1136/ bmj.e5660.
10. Shinde SS, Forman MR, Kuerer HM et al. Higher parity and shorter breastfeeding duration: association with triple-negative phenotype of breast cancer. Cancer 2010; 16(21): 4933– 4943. doi: 10.1002/ cncr.25443.
11. Collaborative Group on Hormonal Factors in Breast Cancer. Breast cancer and hormonal contraceptives: collaborative reanalysis of individual data on 53,297 women with breast cancer and 100,239 women without breast cancer from 54 epidemiological studies. Lancet 1996, 347(9017): 1713– 1727.
12. Jernström H, Lerman C, Ghadirian P et al. Pregnancy and risk of early breast cancer in carriers of BRCA1 and BRCA2. Lancet 1999; 354(9193): 1846– 1850.
13. Who.int [homepage on the Internet]. World Health Organization. Classification of Tumours of the Breast; 2012 [cited 2014 Oct 10]. Available from: http:/ / www.who.int/ .
14. Goldhirsch A, Winer EP, Coates AS et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol 2013; 24(9): 2206– 2223. doi: 10.1093/ annonc/ mdt303.
15. Badve S, Dabbs DJ, Schnitt SJ et al. Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod Pathol 2011; 24(2): 157– 167. doi: 10.1038/ modpathol.2010.200.
16. Nielsen TO, Hsu FD, Jensen K et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004; 10(16): 5367– 5674.
17. 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(5): 1368– 1376. doi: 10.1158/ 1078-0432.CCR-07-1658.
18. Elsheikh SE, Green AR, Rakha EA et al. Caveolin 1 and Caveolin 2 are associated with breast cancer basal-like and triple-negative immunophenotype. Br J Cancer 2008; 99(2): 327– 334. doi: 10.1038/ sj.bjc.6604463.
19. Gautam KM, Xiangshan Z, Hamid B et al. Histological, molecular and functional subtypes of breast cancers. Cancer Biol Ther 2010; 10(10): 955– 960.
20. Prat A, Parker JS, Karginova O et al. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12(5): R68. doi: 10.1186/ bcr2635.
21. Perou C. Molecular stratification of triple-negative breast cancers. Oncologist 2010; 15 (Suppl 5): 39– 48. doi: 10.1634/ theoncologist.2010-S5-39.
22. Gelmon K, Dent R, Mackey JR et al. Targeting triple-negative breast cancer: optimising therapeutic outcomes. Ann Oncol 2012; 23(9): 2223– 2234. doi: 10.1093/ annonc/ mds067.
23. Lehmann BD, Bauer JA, Chen X et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121(7): 2750– 2767. doi: 10.1172/ JCI45014.
24. Mackay A, Weigelt B, Grigoriadis A et al. Microarray-based class discovery for molecular classification of breast cancer: analysis of interobserver agreement. J Natl Cancer Inst 2011; 103(8): 662– 673. doi: 10.1093/ jnci/ djr071.
25. Pistelli M, Caramanti M, Biscotti T et al. Androgen receptor expression in early triple-negative breast cancer: clinical significance and prognostic associations. Cancers (Basel) 2014; 6(3): 1351–1362. doi: 10.3390/cancers6031351.
26. Prat A, Perou C. Mammary development meets cancer genomics. Nat Med 2009; 15(8): 842– 844. doi: 10.1038/ nm0809-842.
27. Mayer I, Abramson V, Lehmann B et al. New strategies for triple negative breast cancer-deciphering the heterogenity. Clin Cancer Res 2014; 20(4): 782– 790. doi: 10.1158/ 1078-0432.CCR-13-0583.
28. Robertson L, Hanson H, Seal S et al. BRCA1 testing should be offered to individuals with triple-negative breast cancer diagnosed below 50 years. Br J Cancer 2012; 106(6): 1234–1238. doi: 10.1038/bjc.2012.31.
29. Weigelt B, Geyer FC, Reis-Filho JS. Histological types of breast cancer: how special are they? Mol Oncol 2010; 4(3): 192–208. doi: 10.1016/j.molonc.2010.04.004.
30. Navrátil J, Svoboda M, Navrátilová M et al. Výskyt zárodečných mutací BRCA1 a BRCA2 genu v konsekutivní kohortě pacientek s triple-negativním karcinomem prsu léčených v MOÚ. In: Sborník abstrakt. XXXVIII. brněnských onkologických dnů a XXVIII. konference pro nelékařské zdravotnické pracovníky. Brno, 24.– 25. dubna, 2014, s. 51.
31. Plevová P, Novotný J, Petráková K et al. Syndrom hereditárního karcinomu prsu a ovarií. Klin Onkol 2009; 22 (Suppl): S8– S11. doi: 10.14735/ amko2009S8.
32. Linkos.cz [internetová stránka]. Foretová L, Macháčková E. Zásady testovani BRCA1/ 2 genů. [citováno 15. září 2014]. Dostupné z: http:/ / www.linkos.cz/ cinnost-skupiny-1/ zasady-testovani-BRCA1-2-genu/ .
33. Bartoňková H, Foretová L, Helmichová E et al. Doporučené zásady péče o nemocné s nádory prsu a vaječníků a zdravé osoby se zárodečnými mutacemi genů BRCA1 nebo BRCA2. Klin Onkol 2003; 16(1): 28– 34.
34. Welcsh PL, Owens KN, King MC. Insights into the functions of BRCA1 and BRCA2. Trends Genet 2000; 16(2): 69– 74.
35. Bertucci F, Finetti P, Birnbaum D. Basal breast cancer: a complex and deadly moleculas subtype. Curr Mol Med 2012; 12(1): 96– 110.
36. Atchley DP, Albarracin CT, Lopez A et al. Clinical and pathologic characteristics of patients with BRCA-positive and BRCA-negative breast cancer. J Clin Oncol 2008; 26(26): 4282– 4288. doi: 10.1200/ JCO.2008.16.6231.
37. Lakhani SR, Reis-Filho JS, Fulford L et al. Prediction of BRCA1 status in patients with breast cancer using estrogen receptor and basal phenotype. Clin Cancer Res 2005; 11(14): 5175– 5180.
38. Lee LJ, Alexander B, Schnitt SJ et al. Clinical outcome of triple negative breast cancer in BRCA1 mutation carriers and noncarriers. Cancer 201; 117(14): 3093– 3100. doi: 10.1002/ cncr.25911.
39. Rocca A, Viale G, Gelber RD et al. Pathologic complete remission rate after cisplatin-based primary chemotherapy in breast cancer: correlation with p63 expression. Cancer Chemother Pharmacol 2008; 61(6): 965– 971.
40. Minami CA, Chung DU, Chang HR. Management options in triple-negative breast cancer. Breast Cancer (Auckl) 2011; 5: 175– 199. doi: 10.4137/ BCBCR.S6562.
41. Dent R, Trudeau M, Pritchard KI et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007; 13(1): 4429– 4434.
42. von Minckwitz G, Untch M, Nüesch E, et al. Impact of treatment characteristics on response of different breast cancer phenotypes: pooled analysis of the German neo-adjuvant chemotherapy trials. Breast Cancer Res Treat 2011; 125(1): 145– 156. doi: 10.1007/ s10549-010-1228-x.
43. Liedtke C, Mazouni C, Hess KR et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 2008; 26(8): 1275– 1281. doi: 10.1200/ JCO.2007.14.4147.
44. Mehta RS. Dose-dense and/ or metronomic schedules of specific chemotherapies consolidate the chemosensitivity of triple-negative breast cancer: a step toward reversing triple-negative paradox. J Clin Oncol 2008; 26(19): 3286– 3288. doi: 10.1200/ JCO.2008.17.1116.
45. Foulkes W, Smith I, Reis-Filho S. Triple-negative breastcancer. N Engl J Med 2010; 363(20): 1938– 1948. doi: 10.1056/ NEJMra1001389.
46. Silver D, Richardson A, Eklund A et al. Efficacy of neoadjuvant cisplatin in triple-negative breast cancer. J Clin Oncol 2010; 28(7): 1145– 1153. doi: 10.1200/ JCO.2009.22.4725.
47. Leong CO, Vidnovic N, DeYoung MP et al. The p63/ p73 network mediates chemosensitivity to cisplatin in a biologically defined subset of primary breast cancers. J Clin Incest 2007; 117(5): 1370– 1380.
48. Byrski T, Gronwald J, Huzarski T. Pathologic complete response rates in young women with BRCA1-positive breast cancers after neoadjuvant chemotherapy. J Clin Oncol 2010; 28(3): 375– 379. doi: 10.1200/ JCO.2008.20.7019.
49. Gronwald J, Byrski T, Huzarski T et al. Neoadjuvant therapy with cisplatin in BRCA1-positive breast cancer patients. J Clin Oncol (Meeting Abstracts) 2009; 27 (Suppl 15): abstr. 502.
50. Joensuu H, Gligorov J. Adjuvant treatments for triple-negative breast cancers. Ann Oncol 2012; 23 (Suppl 6): vi40– vi44.
51. Kaplan HG, Malmgren JA, Atwood M. T1N0 triple negative breast cancer: risk of recurrence and adjuvant chemotherapy. Breast J 2009; 15(5): doi: 10.1111/ j.15244741.2009.00789.x.
52. Wang J, Shi M, Ling R et al. Adjuvant chemotherapy and radiotherapy in triple-negative breast carcinoma: a prospective randomized controlled multi-center trial. Radiother Oncol 2001; 100(2): 200– 204. doi: 10.1016/ j.radonc.2011.07.007.
53. Laporte S, Jones S, Chapelle C et al. Consistency of effect of docetaxel-containing adjuvant chemotherapy in patients with early stage breast cancer independent of nodal status: meta-analysis of 12 randomized clinical trials. Cancer Res 2009; 69 (Suppl 1): abstr. 605.
54. Martin M, Segui MA, Anton A et al. Adjuvant docetaxel for high-risk, node-negative breast cancer. N Engl J Med 2010; 363(23): 2200– 2210. doi: 10.1056/ NEJMoa0910320.
55. Hugh J, Hanson J, Cheang MC et al. Breast cancer subtypes and response to docetaxel in node-positive breast cancer: use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol 2009; 27(8): 1168– 1176. doi: 10.1200/ JCO.2008.18.1024.
56. Hayes DF, Thor AD, Dressler LG et al. HER2 and response to paclitaxel in node-positive breast cancer. N Engl J Med 2007; 357(15): 1496– 1506.
57. Citron ML, Berry DA, Cirrincione C et al: Randomized trial of dose-dense versus conventionally scheduled and sequential versus concurrent combination chemotherapy as postoperative adjuvant treatment of node-positive primary breast cancer: first report of Intergroup Trial C9741/ Cancer and Leukemia Group B Trial 9741. J Clin Oncol 2003; 21(8): 1431– 1439.
58. Staudacher L, Cottu PH, Dieras V et al. Platinum-based chemotherapy in metastatic triple-negative breast cancer: the Institut Curie experience. Ann Oncol 2011; 22(4): 848– 856. doi: 10.1093/ annonc/ mdq461.
59. Cortes J, O‘Shaughnessy J, Loesch D et al. Eribulin monotherapy versus treatment of physician‘s choice in patients with metastatic breast cancer (EMBRACE): a phase 3open-label randomized study. Lancet 2011; 377(9769): 914– 923. doi: 10.1016/ S0140-6736(11)60070-6.
60. Bouchalova K, Svoboda M, Kharaishvili G et al. BRCA-mutation status combined with BCL2 protein in prediction of relapse in triple-negative breast cancer (TNBC) treated with adjuvant anthracycline-based chemotherapy. J Clin Oncol 2014; 32 (Suppl 5): abstr. 1132.
61. Mrklic I, Capkun V, Pogorelic Z et al. Prognostic value of Ki-67 proliferating index in triple negative breast carcinomas. Pathol Res Pract 2013; 209(5): 296– 301. doi: 10.1016/ j.prp.2013.02.012.
62. Linderholm BK, Hellborg H, Johansson U et al. Significantly higher levels of vascular endothelial growth factor (VEGF) and shorter survival times for patients with primary operable triple-negative breast cancer. Ann Oncol 2009; 20(10): 1639– 1646. doi: 10.1093/ annonc/ mdp062.
63. Bear HD, Tang G, Rastogi P et al. Bevacizumab added to neoadjuvant chemotherapy for breast cancer. N Engl J Med 2012; 366(4): 310– 320. doi: 10.1056/ NEJMoa1111097.
64. Sikov WM, Berry DA, Perou CM et al. Impact of the addition of carboplatin and/ or bevacizumab to neoadjuvant once-per-week paclitaxel followed by dose-dense doxorubicin and cyclophosphamide on pathologic complete response rates in stage II to III triple-negative breast cancer: CALGB 40603 (Alliance). J Clin Oncol 2015; 33(1): 13– 21. doi: 10.1200/ JCO.2014.57.0572.
65. von Minckwitz G, Eidtmann H, Rezai M et al. Neoadjuvant chemotherapy and bevacizumab for HER2-negative breast cancer. N Engl J Med 2012; 366(4): 299– 309. doi: 10.1056/ NEJMoa1111065.
66. Cameron D, Brown J, Dent R. Adjuvant bevacizumab-containing therapy in triple-negative breast cancer (BEATRICE): primary results of a randomised, phase 3 trial. Lancet Oncol 2013; 14(10): 933– 942. doi: 10.1016/ S1470-2045(13)70335-8.
67. Miller K, Wang M, Gralow J et al. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med 2007; 357(26): 2666– 2676.
68. Miles DW, Chan A, Dirix LY et al. Phase III study of bevacizumab plus docetaxel compared with placebo plus docetaxel for the first-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer. J Clin Oncol 2010; 28(20): 3239– 3247. doi: 10.1200/ JCO.2008.21.6457.
69. Miles D, Diéras V, Cortés J et al. First-line bevacizumab in combination with chemotherapy for HER2-negative metastatic breast cancer: pooled and subgroup analyses of data from 2,447 patients. Ann Oncol 2013; 24(11): 2773– 2780. doi: 10.1093/ annonc/ mdt276.
70. O‘Shaughnessy J, Brufsky AM. RiBBON 1 and RiBBON 2: phase III trials of bevacizumab with standard chemotherapy for metastatic breast cancer. Clin Breast Cancer 2008, 8(4): 370– 373. doi: 10.3816/ CBC.2008.n.045.
71. Curigliano G, Pivot X, Cortés J et al. Randomized phase IIstudy of sunitinib versus standard of care for patients with previously treated advanced triple-negative breast cancer. Breast 2013; 22(5): 650– 656. doi: 10.1016/ j.breast.2013.07.037.
72. Gonzalez-Angulo AM, Akcakanat A, Liu S et al. Open-label randomized clinical trial of standard neoadjuvant chemotherapy with paclitaxel followed by FEC versus the combination of paclitaxel and everolimus followed by FEC in women with triple receptor-negative breast cancer. Ann Oncol 2014; 25(6): 1122– 1127. doi: 10.1093/ annonc/ mdu124.
73. Singh J, Novik Y, Stein S et al. Phase 2 trial of everolimus and carboplatin combination in patients with triple negative metastatic breast cancer. Breast Cancer Res 2014, 16(2): R32. doi: 10.1186/ bcr3634.
74. Baselga J, Stemmer S, Pego A et al. Cetuximab + cisplatin in estrogen receptor-negative, progesterone receptor-negative, HER2-negative (triple-negative) metastatic breast cancer: results of the randomized phase II BALI-1 trial. Cancer Res 2010; 70: abstr. PD01-01.
75. Finn RS, Press MF, Dering J et al. Estrogen receptor, progesterone receptor, human epidermal growth factor receptor 2 (HER2), and epidermal growth factor receptor expression and benefit from lapatinib in a randomized trial of paclitaxel with lapatinib or placebo as first-line treatment in HER2-negative or unknown metastatic breast cancer. J Clin Oncol 2009; 27(24): 3908– 3915. doi: 10.1200/ JCO.2008.18.1925.
76. O‘Shaughnessy J, Schwartzberg LS, Danso MA et al. A randomized phase III study of iniparib (BSI-201) in combination with gemcitabine/ carboplatin (G/ C) in metastatic triple-negative breast cancer (TNBC). J Clin Oncol 2011; 29 (Suppl): abstr. 1007.
77. Tutt A, Robson M, Garber JE et al. Phase II trial of the oral PARP inhibitor olaparib in BRCA-deficient advanced breast cancer. J Clin Oncol 2009; 27 (Suppl 18): CRA501.
78. McGhan LJ, McCullough AE, Protheroe CA et al. Androgen receptor-positive triple negative breast cancer: a unique breast cancer subtype. Ann Surg Oncol 2014; 21(2): 361– 367. doi: 10.1245/ s10434-013-3260-7.
79. Palácová M, Navrátil J, Fabian P et al. Exprese androgenového receptoru (AR) a estrogenového receptoru beta (ER-beta) u triple negativního karcinomu prsu a jejich klinický význam. In: Sborník abstrakt. XXXVIII. brněnských onkologických dnů a XXVIII. konference pro nelékařské zdravotnické pracovníky. Brno, 24.– 25. dubna, 2014, s. 136.
80. Gucalp A, Tolaney S, Isakoff SJ et al. Phase II trial of bicalutamide in patients with androgen receptor-positive, estrogen receptor-negative metastatic Breast Cancer. Clin Cancer Res 2013; 19(19): 5505– 5512. doi: 10.1158/ 1078-0432.CCR-12-3327.
Štítky
Dětská onkologie Chirurgie všeobecná OnkologieČlánek vyšel v časopise
Klinická onkologie
![Číslo 6](https://www.prolekare.cz/media/cache/resolve/journal_issue/media/image_pdf/300f9471eef909096e9ec873771fb38d.jpeg)
2015 Číslo 6
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Perorální antivirotika jako vysoce efektivní nástroj prevence hospitalizací kvůli COVID-19 − otázky a odpovědi pro praxi
- Nejasný stín na plicích – kazuistika
- Ze života konopného pacienta
- Proces hojení ran krok za krokem a co ho může zkomplikovat
Nejčtenější v tomto čísle
- Triple negativní karcinom prsu
- Případ pozdně diagnostikovaného akrolentiginózního melanomu
- Imunoterapie v prevenci a léčbě karcinomu prsu
-
Onkologie v obrazech
Kolizní duplicitní nádory