Overcoming resistance to endocrine therapy in hormone receptor-positive human epidermal growth factor receptor 2-negative (HR<sup>+</sup>/HER2<sup>--</sup>) advanced breast cancer: a meta-analysis and systemic review of randomized clinical trials

doi:10.1007/s11684-020-0795-4

Front. Med.

2021, Vol. 15

Issue (2) : 208-220 https://doi.org/10.1007/s11684-020-0795-4

REVIEW

Overcoming resistance to endocrine therapy in hormone receptor-positive human epidermal growth factor receptor 2-negative (HR⁺/HER2^--) advanced breast cancer: a meta-analysis and systemic review of randomized clinical trials

Wenjie Zhu, Binghe Xu(

)

National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences, and Peking Union Medical College, Beijing 100021, China

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Abstract

New targeted therapies have been developed to overcome resistance to endocrine therapy (ET) and improve the outcome of HR⁺/HER2^-- advanced breast cancer (ABC). We conducted a meta-analysis and systemic review on randomized controlled trials evaluating various targeted therapies in combination with ET in HR⁺/HER2^-- ABC. PUBMED and EMBASE databases were searched for eligible trials. Hazard ratios (HRs) for progression-free survival (PFS), odds ratios (ORs) for objective response rate (ORR), clinical benefit rate (CBR), and toxicity were meta-analyzed. Twenty-six studies with data on 10 347 patients were included and pooled. The addition of cyclin-dependent kinase 4/6 inhibitors to ET significantly improved median PFS (pooled HR= 0.547, P<0.001), overall survival (pooled HR= 0.755, P<0.001), and tumor response rates (ORR, pooled OR= 1.478, P<0.001; CBR, pooled OR= 1.201, P<0.001) with manageable toxicities (pooled OR= 3.280, P<0.001). The mammalian targets of rapamycin inhibitors and exemestane were not clinically beneficial for this pooled population including ET-naïve and ET-resistant patients. Moderate improvement in PFS (pooled HR= 0.686, P<0.001) yet pronounced toxicities (pooled OR=2.154, P<0.001) were noted in the combination of phosphatidylinositol-4,5-bisphosphate 3-kinase inhibitors with fulvestrant. Future studies are warranted to optimize the population and the dosing sequence of these available options.

Keywords endocrine-resistant HR⁺/HER2⁻ advanced breast cancer randomized clinical trials meta-analysis targeted therapy

Corresponding Author(s): Binghe Xu

Just Accepted Date: 16 October 2020 Online First Date: 12 November 2020 Issue Date: 23 April 2021

Cite this article:

Wenjie Zhu,Binghe Xu. Overcoming resistance to endocrine therapy in hormone receptor-positive human epidermal growth factor receptor 2-negative (HR⁺/HER2^--) advanced breast cancer: a meta-analysis and systemic review of randomized clinical trials[J]. Front. Med., 2021, 15(2): 208-220.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-020-0795-4
https://academic.hep.com.cn/fmd/EN/Y2021/V15/I2/208

Fig.1 Flow chart of literature review and study selection process.

Study	Trial name	Size	Therapy	Menopausal status	Study design
Study	Trial name	Size	Therapy	Menopausal status	Intervention group	N	Control group	N
Cristofanilli, 2016	PALOMA-3	521	CDK4/6 inhibitor	Any	Palbociclib + fulvestrant	345	Fulvestrant	172
Tripathy, 2018	MONALEESA-7	672	CDK4/6 inhibitor	Premenopausal	Ribociclib+ TAM/AI+ OFI	335	TAM/AI+ OFI	337
Sledge, 2017	MONARCH 2	669	CDK4/6 inhibitor	Any	Abemaciclib+ fulvestrant	446	Fulvestrant	223
Sonke, 2018	MONALEESA-2	668	CDK4/6 inhibitor	Postmenopausal	Ribociclib+ letrozole	334	Letrozole	334
Goetz, 2017	MONARCH 3	493	CDK4/6 inhibitor	Postmenopausal	Abemaciclib+ NSAI	328	NSAI	165
Finn, 2016	PALOMA-2	666	CDK4/6 inhibitor	Postmenopausal	Palbociclib+ letrozole	444	Letrozole	222
Finn, 2015	PALOMA-1	165	CDK4/6 inhibitor	Postmenopausal	Palbociclib+ letrozole	83	Letrozole	77
Slamon, 2018	MONALEESA-3	780	CDK4/6 inhibitor	Postmenopausal	Ribociclib+ fulvestrant	484	Fulvestrant	242
Baselga, 2017	BELLA-2	1147	PI3K inhibitor	Postmenopausal	Buparlisib+ fulvestrant	576	Fulvestrant	571
Di Leo, 2017	BELLA-3	432	PI3K inhibitor	Postmenopausal	Buparlisib+ fulvestrant	289	Fulvestrant	143
Andre, 2019 (Cohort 1)	SOLAR-1 (PIK3CA mutation+ cohort)	341	PI3K inhibitor	Postmenopausal	Alpelisib+ fulvestrant	169	Fulvestrant	172
Andre, 2019 (Cohort 2)	SOLAR-1 (PIK3CA mutation- cohort)	230	PI3K inhibitor	Postmenopausal	Alpelisib+ fulvestrant	115	Fulvestrant	115
Krop, 2016 (PART 1)	FERGI, PART1	168	PI3K inhibitor	Postmenopausal	Piclitisib+ fulvestrant	89	Fulvestrant	79
Krop, 2016 (PART 2)	FERGI, PART2, PIK3CA mutation+ cohort	61	PI3K inhibitor	Postmenopausal	Piclitisib+ fulvestrant	41	Fulvestrant	20
Bachelot, 2012	GINECO	111	mTOR inhibitor	Postmenopausal	Everolimus+ tamoxifen	54	Tamoxifen	57
Pritchard, 2013	BOLERO-2	724	mTOR inhibitor	Postmenopausal	Everolimus+ exemestane	485	Exemestane	239
Wolff, 2013	HORIZON	1112	mTOR inhibitor	Postmenopausal	Temsirolimus+ letrozole	550	Letrozole	553
Mosulino, 2017	NCT01528345	97	TKI	Postmenopausal	Dovitinib+ fulvestrant	47	Fulvestrant	50
Cristofanilli, 2010	NCT00077025	93	TKI	Postmenopausal	Gefitinib+ anastrozole	43	Anastrozole	50
Osborne, 2011	NCT00229697	289	TKI	Any	Gefitinib+ tamoxifen	153	Tamoxifen	136
Clemons, 2014	OCOG ZAMBONEY	129	TKI	Postmenopausal	Vandetanib+ fulvestrant	61	Fulvestrant	68
Dickler, 2016	Alliance	343	Anti-angiogenesis	Postmenopausal	Bevacizumab+ letrozole	150	Letrozole	153
Hyams, 2013	NCT00454805	62	Anti-angiogenesis	Postmenopausal	Cediranib+ fulvestrant	31	Fulvestrant	31
Martín, 2015	LEA	374	Anti-angiogenesis	Postmenopausal	Bevacizumab+ letrozole/fulvestrant	190	Letrozole/fulvestrant	184
Jiang, 2019	NCT02482753	365	HDAC inhibitor	Postmenopausal	Tucidinostat+ exemestane	244	Exemestane	121
Yardley, 2013	ENCORE 301	130	HDAC inhibitor	Postmenopausal	Entinostat+ exemestane	64	Exemestane	66
Robertson, 2013	NCT00626106	156	Monoclonal antibody	Postmenopausal	Ganitumab+ fulvestrant/exemestane	106	Fulvestrant/exemestane	50
Ibrahim, 2011	/	110	Monoclonal antibody	Postmenopausal	AS1402+ letrozole	56	Letrozole	53

Tab.1 Characteristics of eligible studies

Study	PFS (month)							Objective response (N)		Clinical benefit (N)		Adverse event (Grade 3/4, N)
	Intervention group	Control group	HR	95% CI		Pvalue	Follow-up	Intervention group	Control group	Intervention group	Control group	Intervention group	Control group
	Intervention group	Control group	HR	LL	UL	Pvalue	Follow-up	Intervention group	Control group	Intervention group	Control group	Intervention group	Control group
Cristofanilli, 2016	9.5	4.6	0.46	0.36	0.59	0.0001	8.9	66	15	231	69	251	38
Tripathy, 2018	23.8	13	0.55	0.44	0.69	0.0001	19.2	137	100	265	235	257	100
Sledge, 2017	16.4	9.3	0.553	0.449	0.681	0.001	19.5	157	36	322	125	267	51
Sonke, 2018	25.3	16	0.56	0.43	0.72	0.0001	15.3	136	92	266	243	271	108
Goetz, 2017	NR	14.7	0.54	0.41	0.72	0.000021	17.8	158	57	256	118	180	35
Finn, 2016	27.6	14.5	0.58	0.46	0.72	0.001	23	187	77	377	156	336	54
Finn, 2015	20.2	10.2	0.488	0.319	0.748	0.0004	29.6	36	27	68	47	63	16
Slamon, 2018	20.5	12.8	0.593	0.48	0.732	0.001	20.4	157	52	340	152	392	16
Baselga, 2017	6.9	5	0.78	0.67	0.89	0.00021	37.6	68	44	252	240	447	192
Di Leo, 2017	3.9	1.8	0.67	0.53	0.84	0.0003	16.3	22	3	96	29	177	47
Andre, 2019 (Cohort 1)	11	5.7	0.65	0.5	0.85	0.001	20	45	22	104	78	216	102
Andre, 2019 (Cohort 2)	7.4	5.6	0.85	0.58	1.25	0.794	20	Unknown	Unknown	Unknown	Unknown	216	102
Krop, 2016 (PART 1)	6.6	5.1	0.74	0.52	1.06	0.096	17.5	7	5	22	14	54	22
Krop, 2016 (PART 2)	5.4	10	1.07	0.53	2.18	0.84	12.9	3	1	8	7	15	7
Bachelot, 2012	8.6	4.5	0.54	0.36	0.81	0.0021	23.7	5	5	33	24	32	35
Pritchard, 2013	7.8	3.2	0.45	0.38	0.54	0.0001	18	61	4	249	63	330	13
Wolff, 2013	9	8.9	0.9	0.76	1.07	0.25	9.5	151	149	245	254	203	134
Mosulino, 2017	5.5	5.5	0.68	0.41	1.14	Unknown	20.5	13	5	31	21	32	19
Cristofanilli, 2010	14.7	8.4	0.55	0.32	0.94	Unknown	13.8	1	6	21	17	6	2
Osborne, 2011	10.9	8.8	0.84	0.59	1.18	0.314	Unknown	13	15	67	57	63	21
Clemons, 2014	5.8	4.8	0.94	0.64	1.36	0.73	Unknown	0	3	9	17	14	9
Dickler, 2016	20.2	15.6	0.75	0.59	0.96	0.016	42	68	49	78	80	79	23
Hyams, 2013	8	4	0.867	0.45	1.669	0.669	8	4	1	13	13	21	10
Martín, 2015	19.3	14.4	0.83	0.65	1.06	0.125	23.7	58	32	146	124	97	24
Jiang, 2019	7.4	3.8	0.75	0.58	0.98	0.033	13.9	45	11	114	43	184	20
Yardley, 2013	4.28	2.27	0.73	0.5	1.07	0.11	26.4	4	3	18	17	31	17
Robertson, 2013	3.9	5.7	1.17	0.91	1.5	0.44	Unknown	5	4	22	10	41	11
Ibrahim, 2011	Unknown	Unknown	0.947	0.496	1.805	Unknown	Unknown	7	14	39	41	34	35

Fig.2 Forest plots of the analyses about efficacy of cyclin-dependent kinase (CDK) 4/6 inhibitors plus endocrine therapy (ET) compared with ET alone in terms of progression-free survival (PFS, A), objective response rate (ORR, B), clinical benefit rate (CBR, C), and toxicity (D). Fixed (A, B) and random (C, D) effect models were used as the pooling method.

Fig.3 Forest plots of the analyses about efficacy of phosphatidylinositol-4,5-bisphosphate 3-kinase (PI3K) inhibitors plus endocrine therapy (ET) compared with ET alone in terms of progression-free survival (PFS, A), objective response rate (ORR, B), and clinical benefit rate (CBR, C) in PIK3CA mutant patients. For PIK3CA nonmutant patients, pooled effect sizes regarding PFS (D) and ORR (E) were shown. Toxicity (F) of PI3K inhibitors was analyzed in the total nonselected population. Fixed (A, B, D, E, F) and random (C) effect models were used as the pooling methods.

Fig.4 Forest plots of the analyses about efficacy of mammalian target of rapamycin (mTOR) inhibitors plus endocrine therapy (ET) compared with ET alone in terms of progression-free survival (PFS, A), objective response rate (ORR, B), clinical benefit rate (CBR, C), and toxicity (D). Random effect model was used as the pooling method.

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