Practical Guidance and Strategies for PARP Inhibition. Nicoletta Colombo, MD University of Milan-Bicocca European Institute of Oncology Milan, Italy
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1 Practical Guidance and Strategies for PARP Inhibition Nicoletta Colombo, MD University of Milan-Bicocca European Institute of Oncology Milan, Italy
2 Clinical Data Maintenance therapy : BRCA-mutated or all comers? Single-agent activity of PARP inhibitors: which, when? Side effects: how to manage? Combination approach: which partner? Impact on clinical practice: how to integrate?
3 PARP Inhibitors in Ovarian Cancer Company Cytotoxicity (IC90 um) PARP Trapping Potency (Relative to Olaparib Set As 1) Class Veliparib AbbVie >50 <0.2 Class 1 Olaparib AstraZeneca Class 2 Rucaparib Clovis 3 1 Class 2 Tesaro Class 2 Talazoparib Pfizer Class 2 Pommier Y, et al. Sci Transl Med. 2016;8(362):362ps17.
4 Maintenance: Olaparib Study 19 Whole Population With HGSOC Subpopulation With BRCA Mutation Ledermann J, et al. N Engl J Med. 2012;366(15): Ledermann J, et al. Lancet Oncol. 2014;15(8):
5 Updated Survival of Study 19 Randomized trial of maintenance olaparib in platinum-sensitive high-grade serous relapsed OC Overall Population BRCAm Population required threshold for statistical significance (p<0 0095) Ledermann J et al. Lancet Oncol. 2016;17(11): Maturity 77 % Maturity 70%
6 : ENGOT-OV16/ NOVA Trial Platinum-Sensitive Recurrent High-Grade Serous Ovarian Cancer Treatment with 4-6 cycles of platinum-based Therapy Response to platinum treatment gbrcamut Non-gBRCAmut 2:1 Randomization 2:1 Randomization 300 mg once daily 300 mg once daily Treat until progression of disease Tested at 100 events to achieve P<.05 Treat until progression of disease Primary Endpoint: PFS by central, blinded review HRD-positive population Tested at 100 events to achieve P<.05; If test was positive, then: Test overall non-gbrcamut cohort (P<.05) Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
7 Progression free Survival (%) Progression-Free Survival: gbrcamut Time Since Randomization (months) Treatment N = 138 N = 65 PFS, Median Mo (95% CI) 21.0 (12.9, NR) 5.5 (3.8, 7.2) Hazard Ratio (95% CI) P value.27 (0.173, 0.410) P<.0001 % of Patients Without Progression or Death 12 Mo 18 Mo 62% 50% 16% 16% PFS was analyzed using a 2-sided log-rank test using randomization stratification factors, and summarized using the Kaplan-Meier methodology. Hazard ratios with 2-sided 95% confidence intervals were estimated using a stratified Cox proportional hazards model, with the stratification factors used in randomization. NR, not reached Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
8 Progression-Free Survival: Non-gBRCAmut Progression free Survival (%) Treatment N = 234 N = 116 PFS, Median Mo (95% CI) 9.3 (7.2, 11.2) 3.9 (3.7, 5.5) Hazard Ratio (95% CI) P value 0.45 (0.338, 0.607) P<.0001 % of Patients Without Progression or Death 12 Mo 18 Mo 41% 30% 14% 12% Time Since Randomization (months) PFS was analyzed using a 2-sided log-rank test using randomization stratification factors, and summarized using the Kaplan-Meier methodology. Hazard ratios with 2-sided 95% confidence intervals were estimated using a stratified Cox proportional hazards model, with the stratification factors used in randomization. Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
9 Progression-Free Survival: Non-gBRCAmut HRD+ Progression free Survival (%) Treatment N = 106 N = 56 PFS, Median Mo (95% CI) 12.9 (8.1, 15.9) 3.8 (3.5, 5.7) Hazard Ratio (95% CI) P value 0.38 (0.243, 0.586) P<.0001 % of Patients Without Progression or Death 12 Mo 18 Mo 51% 37% 13% 9% Time Since Randomization (months) PFS was analyzed using a 2-sided log-rank test using randomization stratification factors, and summarized using the Kaplan-Meier methodology. Hazard ratios with 2-sided 95% confidence intervals were estimated using a stratified Cox proportional hazards model, with the stratification factors used in randomization. Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
10 Exploratory Analysis: PFS in Subgroups of Non-gBRCAmut Cohort HRD Positive HRD Negative sbrcamut BRCAwt Treatment N = 35 N = 12 PFS, Median Mo (95% CI) 20.9 (9.7, NR) 11.0 (2.0, NR) Hazard Ratio (95% CI) P value 0.27 (0.081, 0.903) P =.0248 % of Patients Without Progression or Death 12 Mo 18 Mo 62% 52% 19% 19% Treatment N = 71 N = 44 PFS, Median Mo (95% CI) 9.3 (5.8, 15.4) 3.7 (3.3, 5.6) Hazard Ratio (95% CI) P value 0.38 (0.231, 0.628) P =.0001 % of Patients Without Progression or Death 12 Mo 18 Mo 45% 27% 11% 6% Treatment N = 92 N = 42 PFS, Median Mo (95% CI) 6.9 (5.6, 9.6) 3.8 (3.7, 5.6) Hazard Ratio (95% CI) P value 0.58 (0.361, 0.922) P =.0226 % of Patients Without Progression or Death 12 mo 18 mo 27% 19% 7% 7% Progression free Survival (%) Progression free Survival (%) Progression free Survival (%) Time Since Randomization (months) Time Since Randomization (months) Time Since Randomization (months) NR, Not reached Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
11 Maintenance in Platinum-Sensitive Relapse: What Is Missing? March 30 - April 2, 2014 Sheraton Sonoma County Petaluma, California AZ 19 ENGOT-OV16 NOVA Status Reported Reported Population HGSC gbrcamut or Non gbrca HGSC Design Phase II Phase III Regimen Olaparib placebo placebo Primary endpoint PFS PFS n (randomization) 265 (2:1) 553 (2:1)
12 Maintenance in Platinum-Sensitive Relapse: What Is Missing? March 30 - April 2, 2014 Sheraton Sonoma County Petaluma, California AZ 19 ENGOT-OV16 NOVA Status Reported Reported Population HGSC gbrcamut or Non gbrca HGSC SOLO 2 ARIEL 3 Completed Ongoing gbrcamut HGSC or Endometrioid Design Phase II Phase III Regimen Olaparib placebo placebo Primary endpoint PFS PFS n (randomization) 265 (2:1) 553 (2:1) Phase III Olaparib PFS 440 (2:1) Phase III Rucaparib PFS 540 (2:1)
13 Maintenance in Platinum-Sensitive Relapse: What Is Missing? March 30 - April 2, 2014 Sheraton Sonoma County Petaluma, California AZ 19 ENGOT-OV16 NOVA Status Reported Reported Population HGSC gbrcamut or Non gbrca HGSC SOLO 2 ARIEL 3 Completed Ongoing gbrcamut HGSC or Endometrioid Design Phase II Phase III Regimen Olaparib placebo placebo Primary endpoint PFS PFS n (randomization) 265 (2:1) 553 (2:1) Phase III Olaparib PFS 440 (2:1) Phase III Rucaparib PFS 540 (2:1)
14 Single-Agent Data on PARP Inhibitors Olaparib Olaparib similar activity to PLD in BRCA-m recurrent ovarian cancer (study 12) Kaye SB, et al. J Clin Oncol. 2012;30(4): Ovarian cancer BRCA-m (193): platinum resistant or not suitable for further platinum therapy, median N. of prior line: 4,3 RR:31.1% Kaufman B, et al. J Clin Oncol. 2014;33(3):
15 Single-Agent Data on PARP Inhibitors Olaparib Olaparib similar activity to PLD in BRCA-m recurrent ovarian cancer (study 12) Kaye SB, et al. J Clin Oncol. 2012;30(4): Ovarian cancer BRCA-m (193): platinum resistant or not suitable for further platinum therapy, median N. of prior line: 4,3 RR:31.1% Kaufman B, et al. J Clin Oncol. 2014;33(3):
16 Rucaparib in Relapsed, Platinum-Sensitive High-Grade Ovarian Carcinoma (ARIEL2 Part 1): An International, Multicenter, Open-Label, Phase II Trial BRCAm RECIST = 80% RECIST +CA125 = 85% BRCAwt, LOH high RECIST = 29% RECIST +CA125 = 44% BRCAwt, LOH low RECIST = 10% RECIST +CA125 = 20% Swisher EM, et al. Lancet Oncol. 2017;18(1):75-87.
17 Rucaparib in Patients With BRCAm After 2 Lines Pooled Analysis Of ARIEL 2 And Study 10 (Platinum Sensitive and Resistant) Kristeleit RS, et al. Ann Oncol. 2016;27(Suppl 6): Abstract 8560.
18 December 19, 2014 Olaparib accelerated approval Germline BRCA mutation 3 prior lines FDA approval does not distinguish between platinum sensitive and platinum resistant December 19, 2016 Rucaparib accelerated approval Deleterious BRCA mutation (germline and/or somatic) 2 prior lines
19 QUADRA: Ovarian Cancer Phase II Trial Design Patients with advanced, relapsed, high-grade serous epithelial ovarian, fallopian tube, or primary peritoneal cancer who have received 3 or 4 previous chemotherapy regimens Amendment 3 HRD+ only 300 mg Endpoint assessment Primary Endpoint Key Secondary Endpoints ORR (overall response rate) defined as the proportion of patients achieving CR or PR ORR and duration of response in patients with gbrca mut and HRD-positive patients Durability of anticancer activity Disease-control rate (DCR) PFS Overall survival Safety and tolerability CR, complete response; PR, partial response; HRD, homologous recombination deficiency National Institutes of Health. Accessed January 19,
20 PARPi Therapy in Recurrent Ovarian Cancer March 30 - April 2, 2014 Sheraton Sonoma County Petaluma, California Liu et al ENGOT-OV24 Avanova NRG-GY004 NRG-GY005 SOLO3 ARIEL4 NEO Status Reported Ongoing Ongoing Ongoing Ongoing Ongoing Ongoing Population Platinum sensitive Platinum sensitive Platinum sensitive Platinum resistant Platinum sensitive; BRCAmut Platinum sensitive; BRCAmut Pre-op Design Phase II at relapse Phase II at relapse Phase III at relapse Phase III at relapse Phase III at relapse Phase III at relapse Randomized phase II Regimen Olaparib Cediranib + Olaparib Bevacizumab Bev + Nir Olaparib Cediranib + Olaparib Platinumcombo Cediranib Olaparib Cediranib+ olaparib Nonplatinum chemo Olaparib Standard of care monotherapy Rucaparib Standard of care Olaparib Endpoint PFS PFS PFS OS PFS PFS Translational research n
21 OReO Study: Olaparib Retreatment in Platinum-Sensitive Ovarian Cancer OC in RELAPSE Previous treatment with consecutive PARPi 6 months and 12 months if 1 st line Whatever the line and the PARPi Stratification factors Prior bevacizumab Platinum-based chemotherapy RP/RC R A N D O M I Z A T I O N 2:1 PD according to investigator *300 mg bid or last tolerable dose <3 3 chemo lines
22 Side Effects: How To Manage?
23 Olaparib: Safety Profile in STUDY 19 (BRCAm) Profile Consistent With Overall Population BRCAm [N = 96] Preferred Term (%) Olaparib N = 74 All Grades N = 62 Nausea 54 (73%) 20 (32%) Fatigue 40 (54%) 23 (37%) Vomiting 27 (36%) 5 (8%) Diarrhea 22 (30%) 12 (19%) Anemia 19 (26%) 3 (5%) * * * Olaparib N = 74 Grade 3 N = 62 1 (1%) 0 5 (7%) 1 (2%) 2 (3%) 0 2 (3%) 1 (2%) 4 (5%) 1 (2%) Any Serious AE 25 (18.4%) 11 (8.6%) 16 (21.6%) 6 (9.7%) AEs leading to dose reductions Any AE leading to discontinuation 34 (25%) 6 (4.7%) 19 (25.7%) 2 (3.2%) 6 (4.4%) 2 (1.6%) 5 (6.8%) 0 Ledermann J, et al. Lancet Oncol. 2014;15(8):
24 : Treatment-Emergent Grade 3/4 Adverse Events Occurring in 5% of Patients Event no. (%) N = 367 N = 179 Thrombocytopenia a 124 (33.8) 1 (0.6) Anemia b 93 (25.3) 0 Neutropenia c 72 (19.6) 3 (1.7) Fatigue d 30 (8.2) 1 (0.6) Hypertension 30 (8.2) 4 (2.2) MDS/AML occurred in 5 of 367 (1.4%) in patients who received niraparib and 2 of 179 (1.1%) in patients who received placebo. *There were no Grade 5 events. a Thrombocytopenia = thrombocytopenia and decreased platelet count. No grade 3 or 4 bleeding events were associated with thrombocytopenia; b Anemia = anemia and decreased hemoglobin counts; c Neutropenia = neutropenia, decreased neutrophil count, and febrile neutropenia; d Fatigue = fatigue, asthenia, malaise, and lethargy. Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
25 Dose Adjustments Due to Treatment Emergent Adverse Events Event no. (%) Any Grade Grade 3/4 Any Grade Dose Reductions N = 367 Events That Occurred After Cycle 3 N = 296 Dose Discontinuations N = 367 Thrombocytopenia a 148 (40.3) 7 (2.4) 12 (3.3) Anemia b 68 (18.5) 50 (16.9) 5 (1.4) Neutropenia c 32 (8.7) 8 (2.7) 7 (1.9) Fatigue d 20 (5.4) 9 (3.0) 12 (3.3) Hypertension 5 (1.4) - 1 Mandatory dose reductions for hematology laboratory abnormalities were required for thrombocytopenia, anemia, and neutropenia a Thrombocytopenia = thrombocytopenia and decreased platelet count. No grade 3 or 4 bleeding events were associated with thrombocytopenia; b Anemia = anemia and decreased hemoglobin counts; c Neutropenia = neutropenia, decreased neutrophil count, and febrile neutropenia; d Fatigue = fatigue, asthenia, malaise, and lethargy. Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
26 : Patient-Reported Outcomes (PROs) gbrcamut: FOSI Non-gBRCAmut: FOSI Measured using the Functional Assessment of Cancer Therapy Ovarian Symptom Index (FOSI) and the EQ-5D-5L PRO surveys were collected at: Screening visit Every other cycle through cycle 14 Post progression Compliance rates were high, and similar between the two treatment arms : FOSI completion rate ranged from 75.0% to 97.1% : FOSI completion rate ranged from 77.6% to 97.4% PROs were similar for niraparib compared with placebo gbrcamut: EQ-5D-5L Non-gBRCAmut: EQ-5D-5L Mirza MR, et al. N Engl J Med. 2016;375(22): Mirza MR, et al. Ann Oncol. 2016;27(Suppl 6): Abstract LBA3_PR.
27 Combination Approach: Which Partner?
28 Antiangiogenesis and PARP-i Chronic hypoxia induces down-regulation of BRCA1 and RAD51, and decreases homologous recombination in cancer cells Cediranib/olaparib significantly increased PFS compared to olaparib alone in DDP-sensitive recurrent ovarian cancer Anti-VEGF induces hypoxia in tumor microenvironment, which contributes to genomic instability and increased sensitivity of cells to PARP-i Randomized phase III trial of bevacizumab and olaparib in first line ongoing (PAOLA-1) Randomized phase III trials of cediranib and olaparib in DDP-resistant and -sensitive (including maintenance) recurrent ovarian cancer ongoing (NRG-GY , ICON 9) Randomized phase II study of niraparib+bevacizumab in DDP-sensitive ongoing (AVANOVA) Proportion progression-free Olaparib Ced/Olap PFS events Median PFS 9.0 mo 17.7 mo p=0.005 HR 0.42 (95% CI: ) Tentori L, et al. Eur J Cancer. 2007;43(14): Liu J, et al. Lancet Oncol. 2014;15(11):
29 Immune Checkpoint Inhibitors and PARP-i: Ongoing Trials EOCs in gbrcam pts: higher mutational load and number of neoantigens that favor recruitment of increased TILs EOCs in gbrcam: increased CD8+ TILs and high PD-1/PD-L1; favorable subset for immune checkpoint inhibitors alone or combined with PARP-i or chemotherapy McAlpine JN,Mod Pathol. 2012;25(5): Strickland KC, et al. Oncotarget. 2016;7(12): Treatment Sponsor Study Condition Primary Outcome + pembrolizumab Durvalumab + cediranib or olaparib Olaparib + tremelimumab Tremelimumab ± olaparib TESARO NCT Adv TNBC or recurrent EOC NCI NCT Adv solid tumors or recurrent EOC New Mexico Center Care Alliance Sydney Kimmel Comprehensive Cancer Center NCT NCT Recurrent BRCAm EOC Recurrent/ persistent EOC DLT RR Recommended dose ORR Recommended dose, ORR Safety
30 PARP Inhibitor Plus PI3K Inhibitor Preclinical data in TNBC cells demonstrate that P13K inhibition suppresses BRCA 1/2 expression and enhances sensitivity to PARP inhibition, partly through activation of ERK and transcription factor ETS1 Control BKM 120 Olaparib BKM plus olaparib Phase I trial of olaparib / AZD5363 confirms tolerability with multiple responses in gbrca and nonbrca patients ERK, extracellular signal-regulated kinase; TNBC, triple-negative breast cancer Ibrahim YH, et al. Cancer Discov. 2012;2(11): Juvekar A, et al. Cancer Discov. 2012;2(11): Rehman FL, et al. Cancer Discov. 2012;2(11): Michalarea V, et al. Presented at: 2016 American Association of Cancer Research Annual Meeting; April 16-20, 2016: New Orleans, Louisiana; Abstract CT011.
31 Impact On Clinical Practice: How To Integrate?
32 March 30 - April 2, 2014 Sheraton Sonoma County Petaluma, California GOG3005 First-Line SOLO 1 GOG3004 PRIMA PAOLA 1 Status Ongoing Ongoing Ongoing Ongoing Population Design Regimen Stage 1C, II, III, IV Phase III Chemo +/- Veliparib/placebo Stage 3-4 BRCAmut Stage 3-4 HRD Stage 3b-4 HGSC/endomet on bevacizumab Phase III Phase III Phase III Olaparib. placebo NED/CR/PR Maintenance after chemotherapy. Olaparib + bevacizumab + bevacizumab Primary endpoint PFS PFS PFS PFS N Randomization (1:1:1) (2:1) (2:1) (2:1)
33 Ovarian Cancer Treatment Algorithm First line Carboplatin/ Paclitaxel bevacizumab Relapse Chemo followed by PARP-i Chemo + bevacizumab Patient selection DDP-sensitive gbrcam sbrcam DDP-sensitive All comers? Not yet
34 Ovarian Cancer Treatment Algorithm First line Carboplatin/ Paclitaxel bevacizumab Relapse Chemo followed by PARP-i Chemo + bevacizumab Patient selection DDP-sensitive gbrcam sbrcam DDP-sensitive All comers? Not yet
35 Ovarian Cancer Treatment Algorithm First line Carboplatin/ Paclitaxel Relapse Chemo followed by PARP-i Chemo + bevacizumab Patient selection DDP-sensitive Any relapse gbrcam sbrcam DDP-sensitive Any relapse All comers? Not yet DDP sensitive (1 relapse) All comers DDP resistant (1 and 2 relapse) All comers Subsequent relapse Chemo + bevacizumab if DDP resistant Chemo followed by PARP inhibitors if DDP sensitive
36 Ovarian Cancer Treatment Algorithm First line Carboplatin/ Paclitaxel Relapse Chemo followed by PARP-i Chemo + bevacizumab Patient selection DDP-sensitive Any relapse gbrcam sbrcam DDP-sensitive Any relapse All comers? Not yet DDP sensitive (1 relapse) All comers DDP resistant (1 and 2 relapse) All comers Subsequent relapse Chemo + bevacizumab if DDP resistant Chemo followed by PARP inhibitors if DDP sensitive
37 For Our Patients.. More Choices Better Than No Choices!!!
38 Histotype Patient preference and expectation Treatment-free interval p = platinum np = nonplatin b = biological Treatment of relapse: much more than DDPfree interval Previous agents used: PARPi, bevacizumab Symptoms Urgent response needed? DDP, cisplatin; PARPi, poly ADP-ribose polymerase inhibitors BRCA status Toxicities N of prior lines
39 Take-Home Messages PARP inhibitors demonstrated a highly significant clinical benefit in ovarian cancer Maintenance therapy with either olaparib or niraparib leads to significant prolongation of disease control NOVA is the first phase III trial demonstrating a significant activity also in BRCAwt patients Olaparib and rucaparib are active as single agents in BRCA-mutated recurrent ovarian cancer patients Toxicity is manageable, and prolonged administration is feasible after appropriate dose adjustment Combining PARP inhibitors with antiangiogenic drugs or immune checkpoint inhibitors represents a promising approach, and several randomized trials are ongoing to explore further indication for PARP inhibitors in ovarian cancer
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