Annals of Oncology MAY 19, 2023

Olaparib plus bevacizumab first-line maintenance in ovarian cancer: final overall survival results from the PAOLA-1/ENGOT-ov25 trial

Isabelle Ray-Coquard, Alexandra Leary, Sandro Pignata, et al.

Bottom Line

In patients with newly diagnosed advanced ovarian cancer who responded to first-line platinum-based chemotherapy plus bevacizumab, the addition of maintenance olaparib significantly improved overall survival specifically in those with homologous recombination deficiency (HRD)-positive tumors.

Key Findings

1. In the HRD-positive population, maintenance olaparib plus bevacizumab resulted in a statistically significant improvement in overall survival compared with placebo plus bevacizumab (median OS: 56.5 vs 51.6 months; HR 0.62; 95% CI 0.45-0.85).
2. The 5-year overall survival rate for patients with HRD-positive tumors was 65.5% in the olaparib-plus-bevacizumab arm compared to 48.4% in the placebo-plus-bevacizumab arm.
3. For the overall intention-to-treat population, the addition of olaparib did not yield a statistically significant improvement in overall survival (HR 0.92; 95% CI 0.76-1.12; P = 0.4118).
4. In the HRD-negative subgroup, no benefit was observed with the addition of olaparib to bevacizumab maintenance therapy.
5. Safety profiles remained consistent with established data for each agent, with no new safety signals; incidences of myelodysplastic syndrome (MDS) and acute myeloid leukemia (AML) were low and balanced between study arms.

Study Design

Design
RCT
Double-Blind
Sample
806
Patients
Duration
61.8 mo
Median
Setting
Multicenter, International
Population Patients with newly diagnosed, FIGO stage III-IV, high-grade serous or endometrioid ovarian, fallopian tube, or primary peritoneal cancer who were in clinical response after first-line platinum-based chemotherapy plus bevacizumab.
Intervention Olaparib (300 mg twice daily) plus bevacizumab (15 mg/kg every 3 weeks) for up to 24 months.
Comparator Placebo plus bevacizumab (15 mg/kg every 3 weeks) for up to 24 months.
Outcome Progression-free survival (PFS) in the overall intention-to-treat population.

Study Limitations

The study lacked an olaparib monotherapy arm, making it difficult to isolate the individual contribution of olaparib versus the combination of olaparib and bevacizumab.
The subgroup analyses, particularly for HRD-positive patients without a BRCA mutation, were limited by smaller sample sizes.
HRD status was not a stratification factor at the time of randomization, which may introduce imbalances across treatment groups.
A high proportion of patients in the placebo arm received subsequent PARP inhibitor therapy after disease progression, which may have confounded the overall survival results.
Post hoc analyses for certain subgroups were not controlled for Type 1 error and should be considered descriptive.

Clinical Significance

The PAOLA-1 trial establishes the combination of olaparib and bevacizumab as a standard-of-care maintenance regimen for patients with newly diagnosed, advanced HRD-positive ovarian cancer, demonstrating a long-term survival benefit that persists despite subsequent therapy.

Historical Context

The PAOLA-1 trial built upon the success of earlier studies (such as GOG 218 and ICON7) that established the role of bevacizumab in first-line maintenance, and the SOLO-1 trial, which demonstrated the efficacy of olaparib monotherapy in patients with BRCA-mutated ovarian cancer. It aimed to explore whether the addition of a PARP inhibitor could extend the benefit of anti-angiogenic therapy to a broader population, specifically those with HRD-positive status.

Guided Discussion

High-yield insights from every perspective

Med Student
Medical Student

How does the concept of 'synthetic lethality' explain why olaparib is particularly effective in ovarian cancer patients with homologous recombination deficiency (HRD)?

Key Response

Synthetic lethality occurs when the simultaneous loss of two pathways leads to cell death, while the loss of either alone does not. Ovarian cancer cells with HRD (like BRCA mutations) have lost one double-strand break repair mechanism. PARP inhibitors (olaparib) block a different pathway (base excision repair for single-strand breaks). When single-strand breaks persist, they become double-strand breaks during replication; since the HRD cancer cell cannot repair these, it undergoes apoptosis, whereas normal cells with intact HRD pathways survive.

Resident
Resident

Based on the PAOLA-1 final OS data, which specific biomarker subgroup derives the greatest survival benefit from the addition of maintenance olaparib to bevacizumab, and how does this change your initial management plan for a newly diagnosed patient?

Key Response

The greatest OS benefit was seen in the HRD-positive subgroup (including both BRCA-mutated and BRCA wild-type HRD+ patients). In the HRD+ group, the 5-year OS rate was 65.5% with olaparib plus bevacizumab versus 48.4% with bevacizumab alone (HR 0.62). This mandates universal germline/somatic BRCA and HRD testing at diagnosis to identify patients who qualify for this specific combination maintenance therapy, as those who are HRD-negative (HRP) did not show a significant OS benefit from the addition of olaparib.

Fellow
Fellow

Compare the therapeutic implications of the PAOLA-1 final results with the SOLO-1 and PRIMA trials regarding the 'tail of the survival curve.' How should we interpret the lack of OS benefit in the HRD-negative (proficient) population in PAOLA-1 compared to the PFS benefits seen in other trials?

Key Response

While PAOLA-1 showed a massive OS benefit for HRD+ patients (confirming the curative potential seen in SOLO-1 for BRCAm), it showed no OS benefit in HRD-negative patients (HR 1.19). This contrasts with the PRIMA trial (niraparib), which showed a modest PFS benefit in the HRD-negative/HRP group. Fellows must recognize that statistically significant PFS gains do not always translate to OS, especially in HRD-proficient tumors where subsequent therapies and different tumor biology may dilute the effect of first-line PARP inhibition.

Attending
Attending

Given the 5-year OS data from PAOLA-1, how do you approach the 'financial toxicity' and cumulative side-effect profile of combination olaparib and bevacizumab versus olaparib monotherapy for a patient with a BRCA mutation?

Key Response

In BRCA-mutated patients, SOLO-1 established olaparib monotherapy as a standard, while PAOLA-1 showed a 5-year OS of 73.2% for the combination. However, there is no head-to-head trial comparing olaparib alone vs. olaparib + bevacizumab. An attending must weigh the added hypertension and proteinuria risks of bevacizumab against the potential incremental benefit, noting that for patients already receiving bevacizumab with chemotherapy, adding olaparib is the evidence-based path to maximizing OS in the HRD+ population.

Scholarly Review

Critical appraisal through the lens of expert reviewers and guideline development

PhD
PhD

The PAOLA-1 trial encountered significant 'crossover' or subsequent PARP inhibitor use in the control arm (bevacizumab only). Critically evaluate how this subsequent therapy impacts the interpretation of the Hazard Ratio for Overall Survival in the HRD-positive subgroup.

Key Response

In the HRD+ control group, approximately 50% of patients received a PARP inhibitor as a subsequent therapy. This usually leads to an underestimation of the true survival benefit of the experimental arm (dilution of effect). Despite this high crossover rate, the OS benefit remained statistically significant and clinically profound (HR 0.62), suggesting that early introduction of PARPi in the maintenance setting is superior to waiting for recurrence, even in HRD-sensitive tumors.

Journal Editor
Journal Editor

The PAOLA-1 study design lacked an 'olaparib monotherapy' arm. As an editor, how does this omission limit the ability to determine whether the survival benefit is synergistic or merely additive, and does this impact the trial's 'practice-changing' status?

Key Response

A three-arm trial (Bev, Olaparib, and Bev+Olaparib) would have been required to prove synergy. Without it, we cannot definitively say if bevacizumab adds value to olaparib in BRCAm patients. However, because the control arm reflected the then-standard of care (bevacizumab) and the HRD+ OS results were so robust, the study remains practice-changing. A reviewer would flag that we are essentially comparing a 'doublet' to a 'singlet' without knowing if the doublet is better than the alternative singlet (olaparib alone).

Guideline Committee
Guideline Committee

Current NCCN and ASCO guidelines prioritize HRD testing to determine maintenance strategies. How do the PAOLA-1 OS results specifically influence the level of evidence for recommending the combination of Olaparib and Bevacizumab in BRCA wild-type, HRD-positive patients compared to other PARP inhibitors?

Key Response

The PAOLA-1 OS data provides Level 1 evidence specifically for the olaparib+bevacizumab combination in the HRD-positive/BRCA wild-type subgroup, a group where OS benefit had been less certain. While guidelines like NCCN already included this (Category 1), the final OS data strengthens the recommendation from 'based on PFS' to 'confirmed by OS,' distinguishing it from niraparib (PRIMA) which has not yet demonstrated a significant OS advantage in the same first-line maintenance context.

Clinical Landscape

Noteworthy Related Trials

2011

GOG-0218 Trial

n = 1873 · NEJM

Tested

Bevacizumab added to chemotherapy and continued as maintenance

Population

Newly diagnosed stage III or IV ovarian cancer

Comparator

Chemotherapy alone

Endpoint

Progression-free survival

Key result: The addition of bevacizumab to chemotherapy followed by bevacizumab maintenance significantly improved progression-free survival.
2018

SOLO-1 Trial

n = 391 · NEJM

Tested

Olaparib maintenance

Population

Newly diagnosed advanced ovarian cancer with BRCA mutation

Comparator

Placebo

Endpoint

Progression-free survival

Key result: Olaparib maintenance provided a significant progression-free survival benefit over placebo in patients with BRCA-mutated ovarian cancer.
2019

PRIMA Trial

n = 733 · NEJM

Tested

Niraparib maintenance

Population

Newly diagnosed advanced ovarian cancer regardless of biomarker status

Comparator

Placebo

Endpoint

Progression-free survival

Key result: Niraparib maintenance therapy resulted in significantly longer progression-free survival than placebo, particularly in patients with homologous recombination deficiency.

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