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A Phase Ib Dose-Escalation and Expansion Study of the BCL2 Inhibitor Venetoclax Combined with Tamoxifen in ER and BCL2–Positive Metastatic Breast Cancer

Sheau W. Lok, James R. Whittle, François Vaillant, Charis E. Teh, Louisa L. Lo, Antonia N. Policheni, Alice R.T. Bergin, Jayesh Desai, Sarah Ftouni, Luke C. Gandolfo, Danny Liew, He K. Liu, G. Bruce Mann, Kate Moodie, Anand Murugasu, Bhupinder Pal, Andrew W. Roberts, Mark A. Rosenthal, Kylie Shackleton, Maria João Silva, Zhen R. Siow, Gordon K. Smyth, Leanne Taylor, Avraham Travers, Belinda Yeo, Miriam M. Yeung, Andjelija Zivanovic Bujak, Sarah-Jane Dawson, Daniel H.D. Gray, Jane E. Visvader and Geoffrey J. Lindeman
Sheau W. Lok
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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James R. Whittle
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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François Vaillant
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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  • ORCID record for François Vaillant
Charis E. Teh
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Louisa L. Lo
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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  • ORCID record for Louisa L. Lo
Antonia N. Policheni
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Alice R.T. Bergin
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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  • ORCID record for Alice R.T. Bergin
Jayesh Desai
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Sarah Ftouni
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Luke C. Gandolfo
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Danny Liew
4The University of Melbourne, Melbourne, Victoria, Australia.
5School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia.
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He K. Liu
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
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G. Bruce Mann
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
6The Royal Women's Hospital, Melbourne, Victoria, Australia.
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Kate Moodie
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Anand Murugasu
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
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Bhupinder Pal
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
7Olivia Newton-John Cancer Research Institute, Melbourne, Victoria, Australia.
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Andrew W. Roberts
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Mark A. Rosenthal
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Kylie Shackleton
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
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Maria João Silva
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Zhen R. Siow
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Gordon K. Smyth
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Leanne Taylor
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
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Avraham Travers
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Belinda Yeo
7Olivia Newton-John Cancer Research Institute, Melbourne, Victoria, Australia.
8Austin Health, Melbourne, Victoria, Australia.
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Miriam M. Yeung
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
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Andjelija Zivanovic Bujak
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Sarah-Jane Dawson
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Daniel H.D. Gray
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Jane E. Visvader
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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Geoffrey J. Lindeman
1The Royal Melbourne Hospital, Melbourne, Victoria, Australia.
2The Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
3The Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
4The University of Melbourne, Melbourne, Victoria, Australia.
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  • For correspondence: lindeman@wehi.edu.au
DOI: 10.1158/2159-8290.CD-18-1151 Published March 2019
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  • Figure 1.
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    Figure 1.

    A, Kaplan–Meier survival curve for ER+BCL2+ PDX 315 (n = 6–10 mice per arm). Mice were treated with vehicle, tamoxifen, venetoclax, or the combination at indicated doses. Venetoclax oral gavage, 5 days per week. Tamoxifen was injected subcutaneously daily. Mice, which remained otherwise healthy, were sacrificed when tumor size reached the experimental ethical endpoint (>600 mm3). Log-rank (Mantel–Cox) P value for combination therapy with ABT-199 25 mg/kg versus combination with ABT-199 100 mg/kg: P = 0.01. Tumor growth curves for individual mice from the PDX model 315 are shown in Supplementary Fig. S2. B, Study design and consort flow diagram. Patients with metastatic ER+BCL2+ breast cancer (MBC) were treated with tamoxifen and venetoclax (in escalating doses) in a 3 + 3 phase I design continuously until progression, unacceptable toxicity, or death. Once the RP2D was determined, an additional 18 patients were enrolled as of the reporting date. Pharmacodynamic studies were performed on plasma and tumor tissue as well as metabolic studies using FDG-PET. C, Clinical trial consort diagram shows the number of subjects entering the study from enrollment. D, IHC evaluation of BCL2 staining intensity. 0, negative; 1, weak; 2, moderate; 3, strong. Scale bar, 50 μm. ctDNA, circulating tumor DNA; PBMC, peripheral blood mononuclear cell.

  • Figure 2.
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    Figure 2.

    Efficacy assessment by subject. A, Waterfall plot of the best radiologic response for 33 evaluable patients treated. Best response was assessed per RECIST v1.1. B, Matching ctDNA for evaluable patients. Blue squares identify detection of mutation in ctDNA at study enrollment. C, Swimmer plot of time on treatment for 33 evaluable patients. Individual patients represented as lines.

  • Figure 3.
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    Figure 3.

    Biomarkers of response. A, Ki67 of individual patients at baseline and following 28 days of treatment. B, Posttreatment biopsy of patient 01-033 (28 days). Immunostaining of ER, PR, BCL-2, Ki67, and CC3. Scale bars, 50 μm. Black arrows indicate CC3 foci. C, Representative images of FDG-PET scans at baseline and following 28 days of treatment. White arrows for patient 01-019 indicate skull metastases. D, Waterfall plot of change in SUVmax and best radiographic response for 16 patients treated in dose-expansion cohort. For patient 01-024, the lateral component of the soft-tissue iliac mass seen was chosen as the target lesion. E, Numbers of mutations detected in ctDNA at baseline for 33 patients by targeted amplicon sequencing. F, Dynamic changes in ctDNA in response to treatment for patients 01-011 and 01-014 by droplet digital PCR. C, cycle; D, day; EOT, end of treatment.

  • Figure 4.
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    Figure 4.

    Effect of venetoclax on the innate and adaptive immune system. A, Clinical hematology values for patients treated in the dose-expansion cohort (800 mg venetoclax). WCC, white cell count. B–E, Characterization of representative mononuclear cell subsets and immunoglobulin. B, B cells;C, immunoglobulin levels; D, T cells; E, monocytes. Paired t test values are shown; *, P < 0.05; **, P < 0.005; ***, P < 0.001; ****, P < 0.0001.

Tables

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  • Table 1.

    Patient demographics and baseline characteristics

    ParameterDose escalation n = 15 (%)Dose expansion n = 18 (%)Overall n = 33 (%)
    Median age (range)65 (45–78)66 (43–75)65 (43–78)
    ECOG performance status
     07 (47%)14 (78%)21 (64%)
     18 (53%)4 (22%)12 (36%)
    Menopausal status, n (%)
     Premenopausal or perimenopausal2 (13%)1 (6%)3 (9%)
     Postmenopausal13 (87%)17 (94%)30 (91%)
    Histology
     Invasive ductal carcinoma/no special type10 (67%)15 (83%)25 (76%)
     Invasive lobular carcinoma4 (27%)1 (6%)5 (15%)
     Others or not specified1 (7%)2 (11%)3 (9%)
    Receptor statusa
     ER
      Strong12 (80%)17 (94%)29 (88%)
      Moderate3 (20%)1 (6%)4 (12%)
      Weak0 (0%)0 (0%)0 (0%)
     PgR
      Strong11 (73%)8 (44%)19 (58%)
      Moderate1 (7%)3 (17%)4 (12%)
      Weak2 (13%)3 (17%)5 (15%)
      Negative1 (7%)4 (22%)5 (15%)
     BCL2
      Strong11 (73%)17 (94%)28 (85%)
      Moderate4 (27%)1 (6%)5 (15%)
      Weak0 (0%)0 (0%)0 (0%)
     Median Ki67 % (range)10% (1–30)30% (5–60)15% (1–60)
    Sites of disease
     Bone14 (93%)12 (67%)26 (79%)
     Visceral metastases9 (60%)11 (61%)20 (61%)
     Liver3 (20%)8 (44%)11 (33%)
     Lung7 (47%)5 (28%)12 (36%)
     Nodal7 (47%)9 (50%)16 (48%)
    Adjuvant endocrine therapy (%)
     Tamoxifen only6 (40%)5 (28%)11 (33%)
     Aromatase inhibitor only2 (13%)4 (22%)6 (18%)
     Tamoxifen and aromatase inhibitor1 (7%)5 (28%)6 (18%)
     Other (toremefine)1 (7%)0 (0%)1 (3%)
     None5 (33%)4 (22%)9 (27%)
    Prior lines of metastatic therapy, n (%)
     03 (20%)8 (44%)11 (33%)
     13 (20%)4 (22%)7 (21%)
     ≥29 (60%)6 (33%)15 (45%)
     Mean prior lines of treatment (range)2.7 (0–6)1.5 (0–8)2.0 (0–8)
    Prior tamoxifen exposure (%)
     None5 (33%)7 (39%)12 (36%)
     Adjuvant setting only4 (27%)9 (50%)13 (39%)
     Metastatic setting only3 (20%)1 (6%)4 (12%)
     Adjuvant and metastatic3 (20%)1 (6%)4 (12%)
    Prior disease progression on tamoxifen
     Yes6 (40%)3 (17%)9 (27%)
     No9 (60%)15 (83%)24 (73%)
    Prior chemotherapy exposure (%)
     None5 (33%)7 (39%)12 (36%)
     Adjuvant setting only4 (27%)5 (28%)9 (27%)
     Metastatic setting only3 (20%)2 (11%)5 (15%)
     Adjuvant and metastatic3 (20%)4 (22%)7 (21%)
    • ↵Abbreviation: ECOG, Eastern Cooperative Oncology Group.aSixteen patients were enrolled based on results of archival tissue.

  • Table 2.

    Any grade treatment-related AEs reported in at least 10% of patients

    Adverse event<800 mg n = 9 n (%)800 mg n = 24 n (%)Total n = 33 n (%)
    Decreased white cell count8 (89)21 (88)29 (88)
    Lymphopenia9 (100)20 (83)29 (88)
    Neutropenia5 (56)19 (79)24 (73)
    Nausea6 (67)16 (67)22 (67)
    Anemia5 (56)8 (33)13 (39)
    Thrombocytopenia4 (44)7 (29)11 (33)
    Vomiting3 (33)8 (33)11 (33)
    Diarrhea2 (22)7 (29)9 (27)
    Infection (any)0 (0)9 (38)9 (27)
    Fatigue1 (33)5 (21)6 (18)
    Lethargy0 (0)4 (17)4 (12)
    Pruritis0 (0)4 (17)4 (12)
    Rash1 (33)3 (13)4 (12)
  • Table 3.

    Summary of efficacy data

    VariableDose escalationn = 15Dose expansionn = 18All patients n = 33800 mg cohort n = 24
    Best overall response, n (%)
     Complete response0 (0)1 (6)1 (3)1 (4)
     Partial response4 (27)a10 (56)14 (42)b12 (50)
     Stable disease6 (40)2 (11)8 (24)5 (21)
     Progressive disease5 (33)5 (28)10 (30)6 (25)
     Overall response rate4 (27)a11 (61)15 (45)b13 (54)
     Clinical benefit rate10 (67)13 (72)23 (70)18 (75)
    Median PFS (weeks)36483651
    Median duration of response (range)c61 (11–100+)39 (8–83+)42 (8–100+)42 (8–100+)
    • ↵aPR and ORR was 31% for the 13 patients with measurable disease.

    • ↵bPR and ORR were 45% and 48%, respectively, for the 31 patients with measurable disease.

    • cDuration of objective response shown for the cutoff date, with 8 patients from the 800-mg cohort remaining on study treatment.

Additional Files

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  • Supplementary Data

    • Supplementary Methods - Supplementary Methods
    • Tables S1-5 - Supplementary Tables S1-5
    • Table S6 - Supplementary Table S6
    • Table S7 - Supplementary Table S7
    • Table S8 - Supplementary Table S8
    • Table S9 - Supplementary Table S9
    • Figures S1-8 - Supplementary Figures
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Cancer Discovery: 9 (3)
March 2019
Volume 9, Issue 3
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A Phase Ib Dose-Escalation and Expansion Study of the BCL2 Inhibitor Venetoclax Combined with Tamoxifen in ER and BCL2–Positive Metastatic Breast Cancer
Sheau W. Lok, James R. Whittle, François Vaillant, Charis E. Teh, Louisa L. Lo, Antonia N. Policheni, Alice R.T. Bergin, Jayesh Desai, Sarah Ftouni, Luke C. Gandolfo, Danny Liew, He K. Liu, G. Bruce Mann, Kate Moodie, Anand Murugasu, Bhupinder Pal, Andrew W. Roberts, Mark A. Rosenthal, Kylie Shackleton, Maria João Silva, Zhen R. Siow, Gordon K. Smyth, Leanne Taylor, Avraham Travers, Belinda Yeo, Miriam M. Yeung, Andjelija Zivanovic Bujak, Sarah-Jane Dawson, Daniel H.D. Gray, Jane E. Visvader and Geoffrey J. Lindeman
Cancer Discov March 1 2019 (9) (3) 354-369; DOI: 10.1158/2159-8290.CD-18-1151

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A Phase Ib Dose-Escalation and Expansion Study of the BCL2 Inhibitor Venetoclax Combined with Tamoxifen in ER and BCL2–Positive Metastatic Breast Cancer
Sheau W. Lok, James R. Whittle, François Vaillant, Charis E. Teh, Louisa L. Lo, Antonia N. Policheni, Alice R.T. Bergin, Jayesh Desai, Sarah Ftouni, Luke C. Gandolfo, Danny Liew, He K. Liu, G. Bruce Mann, Kate Moodie, Anand Murugasu, Bhupinder Pal, Andrew W. Roberts, Mark A. Rosenthal, Kylie Shackleton, Maria João Silva, Zhen R. Siow, Gordon K. Smyth, Leanne Taylor, Avraham Travers, Belinda Yeo, Miriam M. Yeung, Andjelija Zivanovic Bujak, Sarah-Jane Dawson, Daniel H.D. Gray, Jane E. Visvader and Geoffrey J. Lindeman
Cancer Discov March 1 2019 (9) (3) 354-369; DOI: 10.1158/2159-8290.CD-18-1151
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