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. 2023 May 31;9:45. doi: 10.1038/s41523-023-00533-2

Table 2.

Clinical data from patients with breast cancer (organized by neoadjuvant, extended adjuvant, metastatic).

Article Trial type/indication ER-targeting agent HER2-targeting agent Other agent Key summaries
Neoadjuvant
Masuda 201893

Open label phase II

(Neo-LaTH)

Invasive breast cancer, neoadjuvant (n = 215)

Leuprorelin 11.25 mg (weeks 1-13) + TAM 20 mg/day or letrozole 2.5 mg/day Lapatinib (1000 mg/day initially, then 750 mg/day), trastuzumab (4 mg/kg in Week 1 and then 2 mg/kg) Paclitaxel (80 mg/m2)

Japanese patients; HER2+

• Lapatinib + trastuzumab followed by lapatinib + trastuzumab + paclitaxel with or without prolongation of anti-HER2, with or without ET

○ 47.9% achieved CpCR (ER−, 63.0%; ER+, 36.1%; P = 0.0034)

○ 42.2% achieved pCR with pN0 (ER−, 57.6%; ER+, 30.3%)

Harbeck 201791

Open label phase II

(WGSG ADAPT)

Early breast cancer, neoadjuvant (n = 375)

TAM or AI T-DM1 (3.6 mg/kg) and trastuzumab (8 mg/kg loading, then 6 mg/kg) None

HER2+/HR+

• T-DM1 vs. T-DM1 + ET vs. trastuzumab + ET

pCR at 12 weeks, 41.0% vs. 41.5% vs. 15.1% (P < 0.001)

Prat Aparicio 201792

Open label phase II

(PAMELA)

Stage I-IIIA HER2+ breast cancer, neoadjuvant (n = 151)

Letrozole or tamoxifen Lapatinib and trastuzumab None

HER2+

• Overall pCR at 18 weeks was 30.5% (HR+, 18.2%; HR−, 43.2%)

• Rate of pCR was 40.6% in HER2-E and 10.0% in non–HER2-E (P < 0.0001)

• Within HR+ disease, pCR rates were 31.6% in HER2-E and 5.3% in non–HER2-E (P = 0.006)

Within HR− disease, pCR rates were 46.0% in HER2-E and 27.3% in non–HER2-E (P = 0.331)

Gluz 202090

Open label, phase II

(WSG TP-II)

HR+/HER2+ EBC, neoadjuvant (n = 207)

Standard ET Trastuzumab and pertuzumab Paclitaxel 80 mg/m2

HR+/HER2+

• ET+ trastuzumab + pertuzumab vs. paclitaxel + trastuzumab + pertuzumab

• pCR (at 12 weeks), was 24% vs. 57% (P < 0.001)

Gianni 201869

Open label phase II

(NA-PHER2)

Invasive breast cancer, neoadjuvant (n = 36)

Fulvestrant 400 mg (SERD) Trastuzumab (8 mg/kg loading, then 6 mg/kg) and pertuzumab (800 mg loading then 420 mg; mAb) Palbociclib 125 mg/day (checkpoint inhibitor)

ER+/HER2+

• Change in mean Ki67 expression

○ At BL, 31.9

○ At 2 weeks, 4.3 (P < 0.0001)

○ At time of surgery, 12.1 (P = 0.013)

• Change in apoptosis from BL to surgery

○ 1.2−0.4 (P = 0.019)

• Presurgery objective response in 29/30 (97%) patients

Park 201678

Open label phase II

(Neo-ALL-IN)

Stage II-III breast cancer, neoadjuvant (n = 24)

Letrozole 2.5 mg/day (non-steroidal AI) Lapatinib 1500 mg/day (TKI) None

Asian patients; ER+/HER2+ tumors

• Clinical overall response rate, 62.5% (1 CR; 0 pCR)

• Potential biomarkers: TILs, ER expression, IHC ER Allred score, 18F-FES PET-CT

Rimawi 201371

Open label phase II

(TBCRC 006)

Stage II-III breast cancer, neoadjuvant (n = 64)

Letrozole (non-steroidal AI) Lapatinib 1000 mg/day (TKI) and trastuzumab (4 mg/kg loading, then 2 mg/kg; mAb) None

Stage II-III, HER2+; ER+ (n = 40)

• In-breast pCR, 27% (ER+ , 21%; ER−, 36%)

• Overall pathologic response rate, 49%

• Low-volume residual disease rate, 22% (ER+, 33%; ER−, 4%)

Rimawi 202094

Open label phase II

(TBCRC023)

Stage II-III breast cancer, neoadjuvant (n = 97)

Letrozole 2.5 mg/day (non-steroidal AI) Lapatinib 1000 mg/day (TKI) and trastuzumab (4 mg/kg loading, then 2 mg/kg) None

Stage II-III, HER2+ (n = 97)

• 12 vs. 24 weeks of lapatinib + trastuzumab (+ letrozole if ER+)

○ 12-week pCR, 12% (ER+, 9%; ER−, 20%)

○ 24-week pCR, 28% (ER+, 33%; ER−, 18%)

Guarneri 201435

Phase IIb RCT

Stage II-IIIA breast cancer, neoadjuvant/adjuvant (n = 92)

Letrozole 2.5 mg/day (non-steroidal AI) Lapatinib 1500 mg/day (TKI) None

HR+/HER2− 

• Letrozole + lapatinib vs. letrozole alone

○ Clinical response rate (CR + PR), 70% vs. 63%

○ Ki-67 and pAkt expression were significantly decreased from BL to surgery in both arms

○ ORR in patients with PIK3CA mutation, 93% vs. 63% (P = 0.04)

Rimawi 201776

Phase III RCT

(NSABP B-52)

Breast cancer in the neoadjuvant setting

(n = 315)

AI Trastuzumab and pertuzumab Docetaxel, carboplatin, estrogen deprivation (goserelin and AI)

HR+/HER2+

• TCHP + estrogen deprivation therapy vs. TCHP alone

○ pCR (breast and nodes), 46.1% vs. 40.9% (P = 0.36)

○ pCR (breast), 47.4% vs. 44.2% (P = 0.57)

Extended adjuvant

Chan 20167

Martin 201779

Chan 202189

Phase III RCT

(ExeteNET)

Stage I-IIIc operable breast cancer, post-adjuvant

(n = 2,840)

None Neratinib 240 mg/day (TKI) after trastuzumab (mAb)–based neoadjuvant and adjuvant therapy None

HER2+

• Neratinib vs. placebo

○ iDFS events at 2 years, 70 vs. 109 events (hazard ratio, 0.67; P = 0.0091)

○ iDFS events at 5-year follow-up, 116 vs. 163 events (hazard ratio, 0.73; P = 0.0083)

○ DFS rate at 2 (93.9% vs. 91.6%) and 5 (90.2% vs. 87.7%) years

○ DFS benefit with neratinib was observed in HR+ patients, but not in HR− 

○ OS rate at 8 years, 91.3% vs 82.2% (hazard ratio, 0.47)

Tolaney 202182

Phase III RCT

(eMonarcHER)

High-risk breast cancer (planned n = 2450)

Standard ET

None

Abemaciclib 150 mg (CDK4/6 inhibitor) None • Planned to start
Dieci 202288

Phase III

(Short-HER)

HER2+/HR+ early breast cancer (n = 1254)

AI and/or TAM Trastuzumab Anthracycline-taxane chemotherapy

HER2+/HR+

• 9 weeks vs. 1 year of adjuvant trastuzumab + anthracycline-taxane chemotherapy + adjuvant ET

• 7-year DFS with AI was 87.3% vs. 81.7% with TAM or TAM-AI (hazard ratio, 1.46; log-rank P = 0.017)

Advanced/metastatic
Jhaveri 202287

Open label phase II

(SUMMIT)

Metastatic breast cancer and prior CDK4/6i (n = 55)

Fulvestrant 500 mg Neratinib (240 mg/day), trastuzumab (8 mg/kg initially, then 6 mg/kg) None

HR+, HER2− 

• Neratinib + trastuzumab + fulvestrant (n = 45)

○ ORR, 38%

○ Median DOR, 14.4 months

○ Clinical benefit, 47%

○ Median PFS, 8.2 months

Ciruelos 202086

Open label phase II

(PATRICIA)

Advanced breast cancer (n = 71)

Letrozole Palbociclib (200 mg/day), trastuzumab (8 mg/kg loading, then 6 mg/kg IV or 600 mg SC) None

HER2+

• Palbociclib + trastuzumab (ER−)

○ 6-month PFS, 33.3%

• Palbociclib + trastuzumab (ER+)

○ 6-month PFS, 42.8%

• Palbociclib + trastuzumab + letrozole (ER+)

○ 6-month PFS, 46.4%

Hua 202285

Open label phase III

(SYSUCC-002)

Metastatic breast cancer (n = 392)

Investigator’s choice ET (ER modulator or AI) Trastuzumab (8 mg/kg loading, then 6 mg/kg) Chemotherapy (investigator’s choice of taxanes, capecitabine, or vinorelbine)

Patients in China, HER2+

• Trastuzumab + ET vs. trastuzumab + chemotherapy

○ Median PFS, 19.2 vs. 14.8 months (P < 0.0001)

Swain 202084

Phase III RCT

(CLEOPATRA)

Metastatic breast cancer (n = 808)

None Trastuzumab (8 mg/kg loading, then 6 mg/kg) and pertuzumab (840 mg loading, then 420 mg) Docetaxel (75 mg/m2 escalating to 100 mg/m2 if tolerated)

HER2+

• Trastuzumab + docetaxel + pertuzumab

○ Median OS, 57.1 months

○ 8-year OS rate, 37%

• Trastuzumab + docetaxel + placebo

○ Median OS, 40.8 months

○ 8-year OS rate, 23%

Chu 200874

Open label phase I

Advanced solid tumors (n = 34)

Letrozole 2.5 mg/day (non-steroidal AI) Lapatinib 1250–1500 mg/day (TKI) None

HR+ (n = 18)

• In the breast cancer cohort:

○ PR, n = 1

○ SD, n = 2 (lasting 247 and 289 days)

• Well tolerated

• No pharmacokinetic interaction

Fumoleau 201477

Open label phase I

Metastatic breast cancer (n = 23)

Tamoxifen 20 mg/day (SERM) Lapatinib 1500 mg/day (TKI) None

HR+ irrespective of HER2 status

• SD, 8/23 (36.4%)

• Median PFS, 2.7 months

• Well tolerated

Koeberle 201175

Open label phase I

AI- and trastuzumab-resistant breast cancer (n = 13)

Letrozole (non-steroidal AI) Trastuzumab (mAb) None

ER+/HER2+ breast cancer

• Trastuzumab alone (step 1) then trastuzumab + letrozole upon disease progression (step 2)

• CBR (primary outcome)

○ Step 1, 46%

○ Step 2, 73%

• Median TTP 188 days

Shagisultanova 201980

Phase Ib/II trial

Metastatic breast cancer (n = 20)

Letrozole 2.5 mg/day (non-steroidal AI) Tucatinib 300 mg BID (TKI) Palbociclib 125 mg/day (CDK4/6 inhibitor)

• Safety consistent with previous reports

• Longest time on trial is 10 months (no CNS disease at BL) and 6 months (CNS disease at BL)

Recommended phase II dose is tucatinib 300 mg bid

Marcom 200770

Open label phase II

Advanced breast cancer (n = 31)

Letrozole (non-steroidal AI) Trastuzumab (mAb) None

ER+ and/or PR+ and HER2+

• Overall response rate, 26%

• CBR, 52%

• Median TTP, 5.5 months

• Median DOR, 20.6+ months

Ma 202197

Ma 202283

Open label phase II

(MutHER)

Metastatic breast cancer (n = 31)

Fulvestrant Neratinib 240 mg/day (TKI) None

Patients with prior fulvestrant treatment

• ORR, 25%

• SD (≥24 weeks), 15%

• Median PFS, 24 weeks

• CBR, 38%

Fulvestrant-naïve patients

• ORR, 30%

• SD (≥ 24 weeks), 0

• Median PFS, 20 weeks

• CBR, 30%

Exploratory ER− cohort

• CBR, 25%

Villanueva 201372

Open label phase II

Metastatic breast cancer (n = 24)

Letrozole 2.5 mg/day (non-steroidal AI) Lapatinib 1500 mg/day (TKI) None

AI-resistant, HR+ breast

• ORR (at 12 weeks), 4%

• SD, 25%

• CBR, 21%

• Median PFS, 3.4 months

Smyth 202096

Open label phase II

(SUMMIT)

Metastatic breast cancer (n = 81)

Fulvestrant 500 mg every 4 weeks (SERD) Neratinib 240 mg/day (TKI) None

Neratinib monotherapy vs. neratinib + fulvestrant (70 patients with ER+/HER2+ tumors)

• ORR, 17.4% vs. 14.0%

• CBR, 30.4% vs. 46.8%

• Median PFS, 3.6 vs. 5.4 months

Rimawi 201838

Phase II RCT

(PERTAIN)

Metastatic or locally advanced breast cancer (n = 129)

Anastrozole 1 mg/day or letrozole 2.5 mg/day (non-steroidal AI) Trastuzumab (8 mg/kg loading, then 6 mg/kg every 3 weeks) and pertuzumab (840 mg loading, then 420 mg every 3 weeks; mAb) Induction chemotherapy allowed

HR+/HER2+

• Pertuzumab + trastuzumab + AI vs. trastuzumab + AI

○ Median PFS (stratified by induction chemotherapy), 18.89 vs. 15.80 months (hazard ratio, 0.66; P = 0.007)

○ CR, 7.3% vs. 0.9%

○ CBR, 68.8% vs. 67.0%

○ Median DOR for CR/PR, 27.10 vs. 15.11 months

Huober 201273

Phase III open label

(eLEcTRA)

Metastatic breast cancer (n = 57)

Letrozole 2.5 mg/day (non-steroidal AI) Trastuzumab (4 mg/kg loading, then 2 mg/kg; mAb) None

HR+/HER2+; HR+/HER2−(n = 35)

• Letrozole + trastuzumab vs. letrozole alone

○ Median TTP, 14.1 vs. 3.3 months (hazard ratio, 0.71; P = 0.03)

○ CBR, 65% vs. 39% (odds ratio, 2.99; P = 0.0636)

○ ORR,13% vs. 27%

Johnston 200965

Schwartzberg 201066

Phase III RCT

(EGF30008)

Metastatic breast cancer (N = 1,286)

Letrozole 2.5 mg/day (non-steroidal AI) Lapatinib 1500 mg/day (TKI) None

HR+/HER2+ (n = 219)

• Letrozole + lapatinib vs. letrozole alone

○ Median PFS, 8.2 vs. 3.0 months (hazard ratio, 0.71; P = 0.019)

○ CBR, 48% vs. 29% (odds ratio, 0.4; P = 0.003)

○ ORR, 28% vs. 15% (odds ratio, 0.4; P = 0.021)

○ Median OS, 33.3 vs. 32.3 months

Kaufman 200967

Phase III RCT

(TAnDEM)

Metastatic breast cancer (n = 207)

Anastrozole 1 mg/day (non-steroidal AI) Trastuzumab (4 mg/kg loading, then 2 mg/kg every week) (mAb) None

HR+/HER2+

• Anastrozole + trastuzumab vs. anastrozole alone

○ Median PFS, 4.8 vs. 2.4 months (hazard ratio, 0.63; P = 0.0016)

○ Median OS, 28.5 vs. 23.9 months (P = 0.325)

○ 70% of patients in the anastrozole-alone arm crossed over to combination therapy after progression

○ Median TTP, 4.8 vs. 2.4 months (P = 0.0007)

○ CBR, 42.7% vs. 27.9% (P = 0.026)

○ Median DOR, 9.5 vs. 10.0 months

Johnston 202195

Phase III RCT

(ALTERNATIVE)

Metastatic breast cancer (n = 355)

Letrozole, anastrozole, or exemestane (non-steroidal or steroidal AI) Lapatinib and trastuzumab (mAb) None

HR+/HER2+

• Lapatinib + trastuzumab plus AI vs. trastuzumab + AI

○ Median PFS, 11.0 vs. 5.7 months (hazard ratio, 0.62; P = 0.0064)

○ Overall response rate, 31.7% vs. 13.7%

○ CBR, 41% vs. 31%

• Lapatinib + AI vs. trastuzumab + AI

○ Median PFS, 8.3 vs. 5.7 months (hazard ratio, 0.71; P = 0.0361)

○ Overall response rate, 18.6% vs. 13.7%

○ CBR, 33% vs. 31%

Tolaney 202037

Open label phase II

(monarchHER)

Metastatic breast cancer (n = 237)

Fulvestrant 500 mg (SERD) Trastuzumab (mAb) Abemaciclib 150 mg (CDK4/6 inhibitor)

• No chemotherapy

• Tolerable safety profile

• PFS for abemaciclib, trastuzumab, and fulvestrant vs. standard-of-care chemotherapy and trastuzumab (8.3 vs. 5.7 months, 5.4–7.0; hazard ratio, 0.67 [95% CI, 0.45–1.00]; P = 0.051)

Zhang 202181

Phase Ib/II trial

Metastatic breast cancer (n = 15)

Letrozole 2.5 mg/day (non-steroidal AI) Pyrotinib 400 mg/day (TKI) SHR6390 150 mg/day (CDK4/6 inhibitor)

• Ongoing

• 10 of 15 patients had achieved confirmed PRs

Italic text indicates gene names.

18F-FES PET-CT 18F-fluoroestradiol positron emission tomography combined with computed tomography, AI aromatase inhibitor, BID twice daily, BL baseline, CBR clinical benefit rate, CNS central nervous system, CpCR comprehensive pathological complete response, CR complete response, DFS disease-free survival, DOR duration of response, EBC early breast cancer, ER estrogen receptor, ET endocrine therapy, HER2 human epidermal growth factor receptor 2, HER2-E HER2-enriched, HR hormone receptor, iDFS invasive disease-free survival, IHC immunohistochemical, mAb monoclonal antibody, ORR objective response rate, OS overall survival, pCR pathologic complete response, PFS progression-free survival, pN0 pathologically node negative, PR partial response, RCT randomized controlled trial, SERD selective estrogen receptor degrader, SD stable disease, SERM selective estrogen receptor modulator, TAM tamoxifen, TCHP docetaxel, carboplatin, trastuzumab, and pertuzumab, T-DM1 trastuzumab emtansin, TKI tyrosine kinase inhibitor, TTP time to progression.