Second-line Endocrine Therapy of Hormone Receptor-positive/HER2- negative Advanced Breast Cancer: A Systematic Review and Network Meta-analysis

Page: [718 - 730] Pages: 13

  • * (Excluding Mailing and Handling)

Abstract

Background: The optimal second-line therapy for hormone receptor-positive (HR+)/ human epidermal growth factor receptor 2 negative (HER2−) advanced or metastatic breast cancer is yet to be established. Therefore, we conducted a network meta-analysis (NMA) of marketed drugs to compare their efficacy.

Methods: We searched the literature in PubMed, Embase, Web of Science databases, and the main international conferences in the past 5 years to find phase III clinical trials on drugs available in the market. Network meta-analysis of progression-free survival (PFS), overall survival (OS), and the objective response rate (ORR) was performed using R software. The efficiency of treatment options was compared using hazard ratios and 95% credibility intervals.

Results: Overall, 12 studies with 6120 patients were included in the analysis. In an indirect comparison of the five regimens, cyclin-dependent kinase 4 and 6 inhibitors (CDK4/6i) plus 500 mg fulvestrant (Ful500) gave the best PFS results; palbociclib ranked first with a surface under the cumulative ranking (SUCRA) of 94.99%, followed by mammalian target of rapamycin inhibitor (mTORi) plus everolimus (SUCRA=73.07%), phosphoinositide 3-kinase inhibitor (PI3Ki) plus Ful500 (SUCRA=66.73%), Ful500 alone (SUCRA=44.55%), and histone deacetylase inhibitor (HDACi) plus exemestane (SUCRA= 43.49%). However, no significant difference was found in the PFS rates of CDK4/6i, mTORi, and PI3Ki. For OS, CDK4/6i plus Ful500 ranked first; the SUCRA of ribociclib, abemaciclib, and palbociclib were 86.20%, 83.98%, and 78.52%, respectively. Alpelisib plus Ful500 (SUCRA=66.91%) ranked second but was not statistically different from CDK4/6i. The mTORi plus everolimus group had the best ORR (SUCRA=88.73%). In terms of safety, 81.56% of patients in the tucidinostat plus exemestane regimen developed neutropenia, suggesting strong hematological toxicity; 13.40% of patients developed grade 3-4 diarrhea after using abemaciclib plus Ful500.

Conclusion: For second-line endocrine therapy in HR+/HER2− advanced/metastatic breast cancer, CDK4/6i is a better choice than mTORi, PI3Ki, HDACi, and Ful; it shows good PFS and OS outcomes and a low probability for serious adverse events.

Graphical Abstract

[1]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[2]
Rugo, H.S.; Rumble, R.B.; Macrae, E.; Barton, D.L.; Connolly, H.K.; Dickler, M.N.; Fallowfield, L.; Fowble, B.; Ingle, J.N.; Jahanzeb, M.; Johnston, S.R.D.; Korde, L.A.; Khatcheressian, J.L.; Mehta, R.S.; Muss, H.B.; Burstein, H.J. Endocrine therapy for hormone receptor-positive metastatic breast cancer: American Society of Clinical Oncology guideline. J. Clin. Oncol., 2016, 34(25), 3069-3103.
[http://dx.doi.org/10.1200/JCO.2016.67.1487] [PMID: 27217461]
[3]
Turner, N.C.; Neven, P.; Loibl, S.; Andre, F. Advances in the treatment of advanced oestrogen-receptor-positive breast cancer. Lancet, 2017, 389(10087), 2403-2414.
[http://dx.doi.org/10.1016/S0140-6736(16)32419-9] [PMID: 27939057]
[4]
Reinert, T.; Barrios, C.H. Optimal management of hormone receptor positive metastatic breast cancer in 2016. Ther. Adv. Med. Oncol., 2015, 7(6), 304-320.
[http://dx.doi.org/10.1177/1758834015608993] [PMID: 26557899]
[5]
Cardoso, F.; Paluch-Shimon, S.; Senkus, E.; Curigliano, G.; Aapro, M.S.; André, F.; Barrios, C.H.; Bergh, J.; Bhattacharyya, G.S.; Biganzoli, L.; Boyle, F.; Cardoso, M.J.; Carey, L.A.; Cortés, J.; El Saghir, N.S.; Elzayat, M.; Eniu, A.; Fallowfield, L.; Francis, P.A.; Gelmon, K.; Gligorov, J.; Haidinger, R.; Harbeck, N.; Hu, X.; Kaufman, B.; Kaur, R.; Kiely, B.E.; Kim, S.B.; Lin, N.U.; Mertz, S.A.; Neciosup, S.; Offersen, B.V.; Ohno, S.; Pagani, O.; Prat, A.; Penault-Llorca, F.; Rugo, H.S.; Sledge, G.W.; Thomssen, C.; Vorobiof, D.A.; Wiseman, T.; Xu, B.; Norton, L.; Costa, A.; Winer, E.P. 5th ESO-ESMO international consensus guidelines for advanced breast cancer (ABC 5). Ann. Oncol., 2020, 31(12), 1623-1649.
[http://dx.doi.org/10.1016/j.annonc.2020.09.010] [PMID: 32979513]
[6]
Gradishar, W.J.; Moran, M.S.; Abraham, J.; Aft, R.; Agnese, D.; Allison, K.H.; Blair, S.L.; Burstein, H.J.; Dang, C.; Elias, A.D.; Giordano, S.H.; Goetz, M.P.; Goldstein, L.J.; Hurvitz, S.A.; Isakoff, S.J.; Jankowitz, R.C.; Javid, S.H.; Krishnamurthy, J.; Leitch, M.; Lyons, J.; Matro, J.; Mayer, I.A.; Mortimer, J.; O’Regan, R.M.; Patel, S.A.; Pierce, L.J.; Rugo, H.S.; Sitapati, A.; Smith, K.L.; Smith, M.L.; Soliman, H.; Stringer-Reasor, E.M.; Telli, M.L.; Ward, J.H.; Wisinski, K.B.; Young, J.S.; Burns, J.L.; Kumar, R. NCCN guidelines® insights: Breast cancer, version 4.2021: Featured updates to the NCCN guidelines. J. Natl. Compr. Canc. Netw., 2021, 19(5), 484-493.
[http://dx.doi.org/10.6004/jnccn.2021.0023] [PMID: 34794122]
[7]
Milani, A.; Geuna, E.; Mittica, G.; Valabrega, G. Overcoming endocrine resistance in metastatic breast cancer: Current evidence and future directions. World J. Clin. Oncol., 2014, 5(5), 990-1001.
[http://dx.doi.org/10.5306/wjco.v5.i5.990] [PMID: 25493235]
[8]
Sledge, G.W., Jr; Toi, M.; Neven, P.; Sohn, J.; Inoue, K.; Pivot, X.; Burdaeva, O.; Okera, M.; Masuda, N.; Kaufman, P.A.; Koh, H.; Grischke, E.M.; Frenzel, M.; Lin, Y.; Barriga, S.; Smith, I.C.; Bourayou, N.; Llombart-Cussac, A. MONARCH 2: Abemaciclib in combination with fulvestrant in women with HR+/HER2− advanced breast cancer who had progressed while receiving endocrine therapy. J. Clin. Oncol., 2017, 35(25), 2875-2884.
[http://dx.doi.org/10.1200/JCO.2017.73.7585] [PMID: 28580882]
[9]
Sledge, G.W., Jr; Toi, M.; Neven, P.; Sohn, J.; Inoue, K.; Pivot, X.; Burdaeva, O.; Okera, M.; Masuda, N.; Kaufman, P.A.; Koh, H.; Grischke, E.M.; Conte, P.; Lu, Y.; Barriga, S.; Hurt, K.; Frenzel, M.; Johnston, S.; Llombart-Cussac, A. The effect of abemaciclib plus fulvestrant on overall survival in hormone receptor-positive, ERBB2-negative breast cancer that progressed on endocrine therapy—MONARCH 2: A randomized clinical trial. JAMA Oncol., 2020, 6(1), 116-124.
[http://dx.doi.org/10.1001/jamaoncol.2019.4782] [PMID: 31563959]
[10]
Zhang, Q.Y.; Sun, T.; Yin, Y.M.; Li, H.P.; Yan, M.; Tong, Z.S.; Oppermann, C.P.; Liu, Y.P.; Costa, R.; Li, M.; Cheng, Y.; Ouyang, Q.C.; Chen, X.; Liao, N.; Wu, X.H.; Wang, X.J.; Feng, J.F.; Hegg, R.; Kanakasetty, G.B.; Coccia-Portugal, M.A.; Han, R.B.; Lu, Y.; Chi, H.D.; Jiang, Z.F.; Hu, X.C. MONARCH plus: Abemaciclib plus endocrine therapy in women with HR+/HER2- advanced breast cancer: the multinational randomized phase III study. Ther. Adv. Med. Oncol., 2020, 12, 1758835920963925.
[http://dx.doi.org/10.1177/1758835920963925] [PMID: 33149768]
[11]
Loibl, S.; Turner, N.C.; Ro, J.; Cristofanilli, M.; Iwata, H.; Im, S.A.; Masuda, N.; Loi, S.; André, F.; Harbeck, N.; Verma, S.; Folkerd, E.; Puyana Theall, K.; Hoffman, J.; Zhang, K.; Bartlett, C.H.; Dowsett, M. Palbociclib combined with fulvestrant in premenopausal women with advanced breast cancer and prior progression on endocrine therapy: PALOMA‐3 results. Oncologist, 2017, 22(9), 1028-1038.
[http://dx.doi.org/10.1634/theoncologist.2017-0072] [PMID: 28652278]
[12]
Turner, N.C.; Slamon, D.J.; Ro, J.; Bondarenko, I.; Im, S.A.; Masuda, N.; Colleoni, M.; DeMichele, A.; Loi, S.; Verma, S.; Iwata, H.; Harbeck, N.; Loibl, S.; André, F.; Puyana Theall, K.; Huang, X.; Giorgetti, C.; Huang Bartlett, C.; Cristofanilli, M. Overall survival with palbociclib and fulvestrant in advanced breast cancer. N. Engl. J. Med., 2018, 379(20), 1926-1936.
[http://dx.doi.org/10.1056/NEJMoa1810527] [PMID: 30345905]
[13]
Slamon, D.J.; Neven, P.; Chia, S.; Fasching, P.A.; De Laurentiis, M.; Im, S.A.; Petrakova, K.; Bianchi, G.V.; Esteva, F.J.; Martín, M.; Nusch, A.; Sonke, G.S.; De la Cruz-Merino, L.; Beck, J.T.; Pivot, X.; Vidam, G.; Wang, Y.; Rodriguez Lorenc, K.; Miller, M.; Taran, T.; Jerusalem, G. Phase III randomized study of ribociclib and fulvestrant in hormone receptor-positive, human epidermal growth factor receptor 2-negative advanced breast cancer: MONALEESA-3. J. Clin. Oncol., 2018, 36(24), 2465-2472.
[http://dx.doi.org/10.1200/JCO.2018.78.9909] [PMID: 29860922]
[14]
Slamon, D.J.; Neven, P.; Chia, S.; Fasching, P.A.; De Laurentiis, M.; Im, S.A.; Petrakova, K.; Bianchi, G.V.; Esteva, F.J.; Martín, M.; Nusch, A.; Sonke, G.S.; De la Cruz-Merino, L.; Beck, J.T.; Pivot, X.; Sondhi, M.; Wang, Y.; Chakravartty, A.; Rodriguez-Lorenc, K.; Taran, T.; Jerusalem, G. Overall survival with ribociclib plus fulvestrant in advanced breast cancer. N. Engl. J. Med., 2020, 382(6), 514-524.
[http://dx.doi.org/10.1056/NEJMoa1911149] [PMID: 31826360]
[15]
Jiang, Z.; Li, W.; Hu, X.; Zhang, Q.; Sun, T.; Cui, S.; Wang, S.; Ouyang, Q.; Yin, Y.; Geng, C.; Tong, Z.; Cheng, Y.; Pan, Y.; Sun, Y.; Wang, H.; Ouyang, T.; Gu, K.; Feng, J.; Wang, X.; Wang, S.; Liu, T.; Gao, J.; Cristofanilli, M.; Ning, Z.; Lu, X. Tucidinostat plus exemestane for postmenopausal patients with advanced, hormone receptor-positive breast cancer (ACE): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol., 2019, 20(6), 806-815.
[http://dx.doi.org/10.1016/S1470-2045(19)30164-0] [PMID: 31036468]
[16]
Yardley, D.A.; Noguchi, S.; Pritchard, K.I.; Burris, H.A., III; Baselga, J.; Gnant, M.; Hortobagyi, G.N.; Campone, M.; Pistilli, B.; Piccart, M.; Melichar, B.; Petrakova, K.; Arena, F.P.; Erdkamp, F.; Harb, W.A.; Feng, W.; Cahana, A.; Taran, T.; Lebwohl, D.; Rugo, H.S. Everolimus plus exemestane in postmenopausal patients with HR(+) breast cancer: BOLERO-2 final progression-free survival analysis. Adv. Ther., 2013, 30(10), 870-884.
[http://dx.doi.org/10.1007/s12325-013-0060-1] [PMID: 24158787]
[17]
Piccart, M.; Hortobagyi, G.N.; Campone, M.; Pritchard, K.I.; Lebrun, F.; Ito, Y.; Noguchi, S.; Perez, A.; Rugo, H.S.; Deleu, I.; Burris, H.A., III; Provencher, L.; Neven, P.; Gnant, M.; Shtivelband, M.; Wu, C.; Fan, J.; Feng, W.; Taran, T.; Baselga, J. Everolimus plus exemestane for hormone-receptor-positive, human epidermal growth factor receptor-2-negative advanced breast cancer: Overall survival results from BOLERO-2. Ann. Oncol., 2014, 25(12), 2357-2362.
[http://dx.doi.org/10.1093/annonc/mdu456] [PMID: 25231953]
[18]
André, F.; Ciruelos, E.; Rubovszky, G.; Campone, M.; Loibl, S.; Rugo, H.S.; Iwata, H.; Conte, P.; Mayer, I.A.; Kaufman, B.; Yamashita, T.; Lu, Y.S.; Inoue, K.; Takahashi, M.; Pápai, Z.; Longin, A.S.; Mills, D.; Wilke, C.; Hirawat, S.; Juric, D. Alpelisib for PIK3CA-mutated, hormone receptor-positive advanced breast cancer. N. Engl. J. Med., 2019, 380(20), 1929-1940.
[http://dx.doi.org/10.1056/NEJMoa1813904] [PMID: 31091374]
[19]
André, F.; Ciruelos, E.M.; Juric, D.; Loibl, S.; Campone, M.; Mayer, I.A.; Rubovszky, G.; Yamashita, T.; Kaufman, B.; Lu, Y.S.; Inoue, K.; Pápai, Z.; Takahashi, M.; Ghaznawi, F.; Mills, D.; Kaper, M.; Miller, M.; Conte, P.F.; Iwata, H.; Rugo, H.S. Alpelisib plus fulvestrant for PIK3CA-mutated, hormone receptor-positive, human epidermal growth factor receptor-2-negative advanced breast cancer: Final overall survival results from SOLAR-1. Ann. Oncol., 2021, 32(2), 208-217.
[http://dx.doi.org/10.1016/j.annonc.2020.11.011] [PMID: 33246021]
[20]
Rugo, H.S.; Lerebours, F.; Ciruelos, E.; Drullinsky, P.; Ruiz-Borrego, M.; Neven, P.; Park, Y.H.; Prat, A.; Bachelot, T.; Juric, D.; Turner, N.; Sophos, N.; Zarate, J.P.; Arce, C.; Shen, Y.M.; Turner, S.; Kanakamedala, H.; Hsu, W.C.; Chia, S. Alpelisib plus fulvestrant in PIK3CA-mutated, hormone receptor-positive advanced breast cancer after a CDK4/6 inhibitor (BYLieve): One cohort of a phase 2, multicentre, open-label, non-comparative study. Lancet Oncol., 2021, 22(4), 489-498.
[http://dx.doi.org/10.1016/S1470-2045(21)00034-6] [PMID: 33794206]
[21]
Reeves, C. San antonio breast cancer symposium 2021. Lancet Oncol., 2022, 23(1), e18.
[http://dx.doi.org/10.1016/S1470-2045(21)00727-0] [PMID: 34922646]
[22]
Bardia, A.; Hurvitz, S.A.; DeMichele, A.; Clark, A.S.; Zelnak, A.; Yardley, D.A.; Karuturi, M.; Sanft, T.; Blau, S.; Hart, L.; Ma, C.; Rugo, H.S.; Purkayastha, D.; Moulder, S. Phase I/II trial of exemestane, ribociclib, and everolimus in women with HR+/HER2- advanced breast cancer after progression on CDK4/6 inhibitors (TRINITI-1). Clin. Cancer Res., 2021, 27(15), 4177-4185.
[http://dx.doi.org/10.1158/1078-0432.CCR-20-2114] [PMID: 33722897]
[23]
Howell, S.J.; Krebs, M.G.; Lord, S. ; et al. 265P Study of samuraciclib (CT7001), a first-in-class, oral, selective inhibitor of CDK7, in combination with fulvestrant in patients with advanced hormone receptor positive HER2 negative breast cancer (HR+BC). Ann. Oncol., 2021, 32, S477-S478.
[http://dx.doi.org/10.1016/j.annonc.2021.08.548]
[24]
Gourgou-Bourgade, S; Cameron, D; Poortmans, P Guidelines for time-toevent end point definitions in breast cancer trials: results of the DATECAN initiative (Definition for the assessment of time-to-event endpoints in cancer trials). Ann Oncol., 2015, 26(5), 873-879.
[25]
Higgins, JPT; Altman, DG; Gotzsche, PC The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ, 2011, 343, d5928-d5928.
[http://dx.doi.org/10.1136/bmj.d5928]
[26]
Salanti, G.; Ades, A.E.; Ioannidis, J.P.A. Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial. J. Clin. Epidemiol., 2011, 64(2), 163-171.
[http://dx.doi.org/10.1016/j.jclinepi.2010.03.016] [PMID: 20688472]
[27]
Miller, T.W.; Balko, J.M.; Arteaga, C.L. Phosphatidylinositol 3-kinase and antiestrogen resistance in breast cancer. J. Clin. Oncol., 2011, 29(33), 4452-4461.
[http://dx.doi.org/10.1200/JCO.2010.34.4879] [PMID: 22010023]
[28]
Miller, T.W.; Rexer, B.N.; Garrett, J.T.; Arteaga, C.L. Mutations in the phosphatidylinositol 3-kinase pathway: Role in tumor progression and therapeutic implications in breast cancer. Breast Cancer Res., 2011, 13(6), 224.
[http://dx.doi.org/10.1186/bcr3039] [PMID: 22114931]
[29]
Zardavas, D.; Baselga, J.; Piccart, M. Emerging targeted agents in metastatic breast cancer. Nat. Rev. Clin. Oncol., 2013, 10(4), 191-210.
[http://dx.doi.org/10.1038/nrclinonc.2013.29] [PMID: 23459626]
[30]
Falkenberg, K.J.; Johnstone, R.W. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat. Rev. Drug Discov., 2014, 13(9), 673-691.
[http://dx.doi.org/10.1038/nrd4360] [PMID: 25131830]
[31]
Brabletz, T. To differentiate or not-routes towards metastasis. Nat. Rev. Cancer, 2012, 12(6), 425-436.
[http://dx.doi.org/10.1038/nrc3265] [PMID: 22576165]
[32]
Huang, H.W.; Huang, L.S.; Xu, Q.N.; Wang, H.B.; Li, X.Y.; Lin, J.Z. CDK4/6 inhibition versus mTOR blockade as second-line strategy in postmenopausal patients with hormone receptor-positive advanced breast cancer. Medicine, 2019, 98(1), e13909.
[http://dx.doi.org/10.1097/MD.0000000000013909] [PMID: 30608416]
[33]
Giuliano, M.; Schettini, F.; Rognoni, C.; Milani, M.; Jerusalem, G.; Bachelot, T.; De Laurentiis, M.; Thomas, G.; De Placido, P.; Arpino, G.; De Placido, S.; Cristofanilli, M.; Giordano, A.; Puglisi, F.; Pistilli, B.; Prat, A.; Del Mastro, L.; Venturini, S.; Generali, D. Endocrine treatment versus chemotherapy in postmenopausal women with hormone receptor-positive, HER2-negative, metastatic breast cancer: A systematic review and network meta-analysis. Lancet Oncol., 2019, 20(10), 1360-1369.
[http://dx.doi.org/10.1016/S1470-2045(19)30420-6] [PMID: 31494037]
[34]
Liu, S.; Sun, X.; Xu, X.; Lin, F. Comparison of endocrine therapies in hormone receptor-positive and human epidermal growth factor receptor 2-negative locally advanced or metastatic breast cancer: A network meta-analysis. J. Breast Cancer, 2020, 23(5), 460-483.
[http://dx.doi.org/10.4048/jbc.2020.23.e55] [PMID: 33154823]
[35]
Xu, B.; Zhang, Q.; Zhang, P.; Hu, X.; Li, W.; Tong, Z.; Sun, T.; Teng, Y.; Wu, X.; Ouyang, Q.; Yan, X.; Cheng, J.; Liu, Q.; Feng, J.; Wang, X.; Yin, Y.; Shi, Y.; Pan, Y.; Wang, Y.; Xie, W.; Yan, M.; Liu, Y.; Yan, P.; Wu, F.; Zhu, X.; Zou, J. Dalpiciclib or placebo plus fulvestrant in hormone receptor-positive and HER2-negative advanced breast cancer: A randomized, phase 3 trial. Nat. Med., 2021, 27(11), 1904-1909.
[http://dx.doi.org/10.1038/s41591-021-01562-9] [PMID: 34737452]
[36]
Hurvitz, S.A.; Park, Y.H.; Bardia, A. Elacestrant. Ann. Oncol., 2021, 32, S1285-S1286.
[http://dx.doi.org/10.1016/j.annonc.2021.08.2086]
[37]
Connolly, R.M.; Zhao, F.; Miller, K.D.; Lee, M.J.; Piekarz, R.L.; Smith, K.L.; Brown-Glaberman, U.A.; Winn, J.S.; Faller, B.A.; Onitilo, A.A.; Burkard, M.E.; Budd, G.T.; Levine, E.G.; Royce, M.E.; Kaufman, P.A.; Thomas, A.; Trepel, J.B.; Wolff, A.C.; Sparano, J.A. E2112: Randomized phase iii trial of endocrine therapy plus entinostat or placebo in hormone receptor-positive advanced breast cancer. A trial of the ECOG-ACRIN cancer research group. J. Clin. Oncol., 2021, 39(28), 3171-3181.
[http://dx.doi.org/10.1200/JCO.21.00944] [PMID: 34357781]
[38]
Finn, R.S.; Crown, J.P.; Lang, I.; Boer, K.; Bondarenko, I.M.; Kulyk, S.O.; Ettl, J.; Patel, R.; Pinter, T.; Schmidt, M.; Shparyk, Y.; Thummala, A.R.; Voytko, N.L.; Fowst, C.; Huang, X.; Kim, S.T.; Randolph, S.; Slamon, D.J. The cyclin-dependent kinase 4/6 inhibitor palbociclib in combination with letrozole versus letrozole alone as first-line treatment of oestrogen receptor-positive, HER2-negative, advanced breast cancer (PALOMA-1/TRIO-18): A randomised phase 2 study. Lancet Oncol., 2015, 16(1), 25-35.
[http://dx.doi.org/10.1016/S1470-2045(14)71159-3] [PMID: 25524798]
[39]
Finn, R.S.; Crown, J.P.; Ettl, J.; Schmidt, M.; Bondarenko, I.M.; Lang, I.; Pinter, T.; Boer, K.; Patel, R.; Randolph, S.; Kim, S.T.; Huang, X.; Schnell, P.; Nadanaciva, S.; Bartlett, C.H.; Slamon, D.J. Efficacy and safety of palbociclib in combination with letrozole as first-line treatment of ER-positive, HER2-negative, advanced breast cancer: Expanded analyses of subgroups from the randomized pivotal trial PALOMA-1/TRIO-18. Breast Cancer Res., 2016, 18(1), 67.
[http://dx.doi.org/10.1186/s13058-016-0721-5] [PMID: 27349747]
[40]
Finn, RS; Crown, J; Lang, I Overall survival results from the randomized phase II study of palbociclib (P) in combination with letrozole (L) vs letrozole alone for frontline treatment of ER+/HER2-advanced breast cancer (PALOMA-1; TRIO-18). J. Clinical Oncol., 2020, 183(2), 419-428.
[41]
Finn, R.S.; Martin, M.; Rugo, H.S.; Jones, S.; Im, S.A.; Gelmon, K.; Harbeck, N.; Lipatov, O.N.; Walshe, J.M.; Moulder, S.; Gauthier, E.; Lu, D.R.; Randolph, S.; Diéras, V.; Slamon, D.J. Palbociclib and letrozole in advanced breast cancer. N. Engl. J. Med., 2016, 375(20), 1925-1936.
[http://dx.doi.org/10.1056/NEJMoa1607303] [PMID: 27959613]
[42]
Hortobagyi, G.N.; Stemmer, S.M.; Burris, H.A.; Yap, Y.S.; Sonke, G.S.; Paluch-Shimon, S.; Campone, M.; Blackwell, K.L.; André, F.; Winer, E.P.; Janni, W.; Verma, S.; Conte, P.; Arteaga, C.L.; Cameron, D.A.; Petrakova, K.; Hart, L.L.; Villanueva, C.; Chan, A.; Jakobsen, E.; Nusch, A.; Burdaeva, O.; Grischke, E.M.; Alba, E.; Wist, E.; Marschner, N.; Favret, A.M.; Yardley, D.; Bachelot, T.; Tseng, L.M.; Blau, S.; Xuan, F.; Souami, F.; Miller, M.; Germa, C.; Hirawat, S.; O’Shaughnessy, J. Ribociclib as first-line therapy for HR-positive, advanced breast cancer. N. Engl. J. Med., 2016, 375(18), 1738-1748.
[http://dx.doi.org/10.1056/NEJMoa1609709] [PMID: 27717303]
[43]
Hortobagyi, G.N.; Stemmer, S.M.; Burris, H.A.; Yap, Y.S.; Sonke, G.S.; Paluch-Shimon, S.; Campone, M.; Petrakova, K.; Blackwell, K.L.; Winer, E.P.; Janni, W.; Verma, S.; Conte, P.; Arteaga, C.L.; Cameron, D.A.; Mondal, S.; Su, F.; Miller, M.; Elmeliegy, M.; Germa, C.; O’Shaughnessy, J. Updated results from MONALEESA-2, a phase III trial of first-line ribociclib plus letrozole versus placebo plus letrozole in hormone receptor-positive, HER2-negative advanced breast cancer. Ann. Oncol., 2018, 29(7), 1541-1547.
[http://dx.doi.org/10.1093/annonc/mdy155] [PMID: 29718092]
[44]
Tripathy, D.; Im, S.A.; Colleoni, M.; Franke, F.; Bardia, A.; Harbeck, N.; Hurvitz, S.A.; Chow, L.; Sohn, J.; Lee, K.S.; Campos-Gomez, S.; Villanueva Vazquez, R.; Jung, K.H.; Babu, K.G.; Wheatley-Price, P.; De Laurentiis, M.; Im, Y.H.; Kuemmel, S.; El-Saghir, N.; Liu, M.C.; Carlson, G.; Hughes, G.; Diaz-Padilla, I.; Germa, C.; Hirawat, S.; Lu, Y.S. Ribociclib plus endocrine therapy for premenopausal women with hormone-receptor-positive, advanced breast cancer (MONALEESA-7): A randomised phase 3 trial. Lancet Oncol., 2018, 19(7), 904-915.
[http://dx.doi.org/10.1016/S1470-2045(18)30292-4] [PMID: 29804902]
[45]
Im, S.A.; Lu, Y.S.; Bardia, A.; Harbeck, N.; Colleoni, M.; Franke, F.; Chow, L.; Sohn, J.; Lee, K.S.; Campos-Gomez, S.; Villanueva-Vazquez, R.; Jung, K.H.; Chakravartty, A.; Hughes, G.; Gounaris, I.; Rodriguez-Lorenc, K.; Taran, T.; Hurvitz, S.; Tripathy, D. Overall survival with ribociclib plus endocrine therapy in breast cancer. N. Engl. J. Med., 2019, 381(4), 307-316.
[http://dx.doi.org/10.1056/NEJMoa1903765] [PMID: 31166679]
[46]
Goetz, M.P.; Toi, M.; Campone, M.; Sohn, J.; Paluch-Shimon, S.; Huober, J.; Park, I.H.; Trédan, O.; Chen, S.C.; Manso, L.; Freedman, O.C.; Garnica Jaliffe, G.; Forrester, T.; Frenzel, M.; Barriga, S.; Smith, I.C.; Bourayou, N.; Di Leo, A. MONARCH 3: Abemaciclib as initial therapy for advanced breast cancer. J. Clin. Oncol., 2017, 35(32), 3638-3646.
[http://dx.doi.org/10.1200/JCO.2017.75.6155] [PMID: 28968163]
[47]
Kalinsky, K; Accordino, MK; Chiuzan, C A randomized, phase II trial of fulvestrant or exemestane with or without ribociclib after progression on anti-estrogen therapy plus cyclin-dependent kinase 4/6 inhibition (CDK 4/6i) in patients (pts) with unresectable or hormone receptor-positive (HR+), HER2-negative metastatic breast cancer (MBC): MAINTAIN trial. J. Clin. Oncol., 2022, 40(Suppl. 17)
[48]
Turner, N. GS3-04 Capivasertib and fulvestrant for patients with aromatase inhibitor-resistant hormone receptor-positive/human epidermal growth factor receptor 2-negative advanced breast cancer: results from the Phase III CAPItello-291 trial. San Antonio Breast Cancer Symposium, Texas, USA; 2022.
[49]
Bardia, A. GS3-01 EMERALD phase 3 trial of elacestrant versus standard of care endocrine therapy in patients with ER+/HER2- metastatic breast cancer: Updated results by duration of prior CDK4/6i in metastatic setting. San Antonio Breast Cancer Symposium, Texas, USA; 2022.
[50]
Oliviera, M. GS3-02 Camizestrant, a next generation oral SERD vs fulvestrant in post-menopausal women with advanced ER-positive HER2-negative breast cancer: Results of the randomized, multidose Phase 2 SERENA-2 trial. San Antonio Breast Cancer Symposium, Texas, USA; 2022.
[51]
Martin, M.; Zielinski, C.; Ruiz-Borrego, M.; Carrasco, E.; Turner, N.; Ciruelos, E.M.; Muñoz, M.; Bermejo, B.; Margeli, M.; Anton, A.; Kahan, Z.; Csöszi, T.; Casas, M.I.; Murillo, L.; Morales, S.; Alba, E.; Gal-Yam, E.; Guerrero-Zotano, A.; Calvo, L.; de la Haba-Rodriguez, J.; Ramos, M.; Alvarez, I.; Garcia-Palomo, A.; Huang Bartlett, C.; Koehler, M.; Caballero, R.; Corsaro, M.; Huang, X.; Garcia-Sáenz, J.A.; Chacón, J.I.; Swift, C.; Thallinger, C.; Gil-Gil, M. Palbociclib in combination with endocrine therapy versus capecitabine in hormonal receptor-positive, human epidermal growth factor 2-negative, aromatase inhibitor-resistant metastatic breast cancer: a phase III randomised controlled trial—PEARL. Ann. Oncol., 2021, 32(4), 488-499.
[http://dx.doi.org/10.1016/j.annonc.2020.12.013] [PMID: 33385521]
[52]
Johnston, S.R.D.; Kilburn, L.S.; Ellis, P.; Dodwell, D.; Cameron, D.; Hayward, L.; Im, Y.H.; Braybrooke, J.P.; Brunt, A.M.; Cheung, K.L.; Jyothirmayi, R.; Robinson, A.; Wardley, A.M.; Wheatley, D.; Howell, A.; Coombes, G.; Sergenson, N.; Sin, H.J.; Folkerd, E.; Dowsett, M.; Bliss, J.M. Fulvestrant plus anastrozole or placebo versus exemestane alone after progression on non-steroidal aromatase inhibitors in postmenopausal patients with hormone-receptorpositive locally advanced or metastatic breast cancer (SoFEA): A composite, multicentre, phase 3 randomised trial. Lancet Oncol., 2013, 14(10), 989-998.
[http://dx.doi.org/10.1016/S1470-2045(13)70322-X] [PMID: 23902874]
[53]
Chia, S.; Gradishar, W.; Mauriac, L.; Bines, J.; Amant, F.; Federico, M.; Fein, L.; Romieu, G.; Buzdar, A.; Robertson, J.F.R.; Brufsky, A.; Possinger, K.; Rennie, P.; Sapunar, F.; Lowe, E.; Piccart, M. Double-blind, randomized placebo controlled trial of fulvestrant compared with exemestane after prior nonsteroidal aromatase inhibitor therapy in postmenopausal women with hormone receptor-positive, advanced breast cancer: Results from EFECT. J. Clin. Oncol., 2008, 26(10), 1664-1670.
[http://dx.doi.org/10.1200/JCO.2007.13.5822] [PMID: 18316794]
[54]
Howell, A.; Robertson, J.F.R.; Quaresma Albano, J.; Aschermannova, A.; Mauriac, L.; Kleeberg, U.R.; Vergote, I.; Erikstein, B.; Webster, A.; Morris, C. Fulvestrant, formerly ICI 182,780, is as effective as anastrozole in postmenopausal women with advanced breast cancer progressing after prior endocrine treatment. J. Clin. Oncol., 2002, 20(16), 3396-3403.
[http://dx.doi.org/10.1200/JCO.2002.10.057] [PMID: 12177099]
[55]
Osborne, C.K.; Pippen, J.; Jones, S.E.; Parker, L.M.; Ellis, M.; Come, S.; Gertler, S.Z.; May, J.T.; Burton, G.; Dimery, I.; Webster, A.; Morris, C.; Elledge, R.; Buzdar, A. Double-blind, randomized trial comparing the efficacy and tolerability of fulvestrant versus anastrozole in postmenopausal women with advanced breast cancer progressing on prior endocrine therapy: results of a North American trial. J. Clin. Oncol., 2002, 20(16), 3386-3395.
[http://dx.doi.org/10.1200/JCO.2002.10.058] [PMID: 12177098]
[56]
Leo, A.D.; Jerusalem, G.; Petruzelka, L.; Torres, R.; Bondarenko, I.N.; Khasanov, R.; Verhoeven, D.; Pedrini, J.L.; Smirnova, I.; Lichinitser, M.R.; Pendergrass, K.; Malorni, L.; Garnett, S.; Rukazenkov, Y.; Martin, M. Final overall survival: Fulvestrant 500 mg vs. 250 mg in the randomized CONFIRM Trial. J. Natl. Cancer Inst., 2014, 106(1), djt337-djt337.
[http://dx.doi.org/10.1093/jnci/djt337] [PMID: 24317176]
[57]
Leo, AD; Jerusalem, G; Petruzelka, L Results of the CONFIRM phase III trial comparing fulvestrant 250 mg with fulvestrant 500 mg in postmenopausal women with estrogen receptor-positive advanced breast cancer. J Clin Oncol., 2010, 28(30), 4594-600.