The Lancet December 02, 2017

Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial

Yoon-Koo Kang et al.

Bottom Line

In patients with heavily pretreated advanced gastric or gastroesophageal junction cancer, third-line or later treatment with the PD-1 inhibitor nivolumab significantly improved overall survival compared to placebo.

Key Findings

1. Nivolumab significantly prolonged median overall survival compared to placebo (5.26 months vs. 4.14 months; HR 0.63, 95% CI 0.51-0.78, p<0.0001).
2. The 12-month overall survival rate was substantially higher in the nivolumab arm at 26.2%, compared to 10.9% in the placebo arm.
3. The objective response rate (ORR) was 11.2% in the nivolumab group, compared to 0% in the placebo group.
4. Grade 3 or 4 treatment-related adverse events occurred in 10% of patients receiving nivolumab and 4% of those receiving placebo, indicating a manageable safety profile.

Study Design

Design
Phase 3 RCT
Double-Blind
Sample
493
Patients
Duration
8.9 mo
Median
Setting
Multicenter, Asia
Population Patients with unresectable advanced or recurrent gastric or gastroesophageal junction adenocarcinoma refractory to, or intolerant of, at least two previous chemotherapy regimens
Intervention Nivolumab (3 mg/kg IV every 2 weeks)
Comparator Placebo (IV every 2 weeks)
Outcome Overall survival

Study Limitations

The trial was exclusively conducted in Asian countries (Japan, South Korea, and Taiwan), which limits the direct extrapolation of the findings to Western populations given known differences in gastric cancer epidemiology and biology.
Tumor tissue for biomarker analysis was not mandatory, resulting in PD-L1 expression data being available for only a small fraction of participants. This precluded definitive conclusions regarding the predictive value of PD-L1.
The absolute median survival benefit was relatively modest (slightly over one month) in the unselected overall population, highlighting the need for better biomarkers to identify the subset of patients achieving long-term durable responses.

Clinical Significance

The ATTRACTION-2 trial was practice-changing, establishing nivolumab as a standard-of-care option for patients with advanced gastric and gastroesophageal junction cancers whose disease has progressed on two or more prior lines of chemotherapy. It provided the definitive phase 3 evidence needed to integrate immune checkpoint inhibitors into the treatment paradigm for advanced gastric cancer.

Historical Context

Historically, patients with advanced gastric or gastroesophageal junction cancer who exhausted first- and second-line systemic therapies had a dismal prognosis with median survival times around 3 to 4 months. Before ATTRACTION-2, no treatments had consistently demonstrated a survival benefit in the third-line setting. This landmark trial was the first phase 3 study to successfully show an overall survival advantage for a PD-1 inhibitor in advanced gastric cancer. Its success led to the initial regulatory approvals for nivolumab in Asia and laid the groundwork for subsequent trials (like CheckMate-649) that successfully moved immunotherapy into the first-line setting.

Guided Discussion

High-yield insights from every perspective

Med Student
Medical Student

What is the mechanism of action of nivolumab, and why is advanced gastric cancer a rational target for immune checkpoint blockade therapy?

Key Response

Nivolumab is a monoclonal antibody that blocks the PD-1 receptor on T-cells, preventing its interaction with PD-L1 and PD-L2 on tumor cells and thereby restoring T-cell-mediated anti-tumor immunity. Gastric cancers often possess features that make them immunogenic, such as high mutational burdens, microsatellite instability (MSI-H), or Epstein-Barr virus (EBV) positivity, which create neoantigens that can be recognized by a disinhibited immune system.

Resident
Resident

A patient with metastatic gastric cancer who progressed on fluoropyrimidine, platinum, and taxane-based therapies is started on nivolumab based on the ATTRACTION-2 trial. What specific immune-related adverse events (irAEs) should be monitored, and how does their management fundamentally differ from standard chemotherapy toxicities?

Key Response

Physicians must monitor for irAEs such as pneumonitis, colitis, hepatitis, endocrinopathies, and dermatitis. Unlike standard chemotherapy toxicities which are typically managed with dose delays, reductions, or supportive care like growth factors, severe irAEs require holding the immunotherapy and initiating high-dose systemic corticosteroids with a slow taper to suppress the autoimmune response.

Fellow
Fellow

The ATTRACTION-2 trial demonstrated an overall survival benefit with nivolumab regardless of PD-L1 expression, which contrasts with several Western trials where PD-L1 heavily influences checkpoint inhibitor efficacy in gastroesophageal cancers. How do regional differences in gastric cancer biology and the methodology of evaluating PD-L1 explain these discrepancies?

Key Response

Asian gastric cancers have different clinical and molecular profiles, such as higher rates of distal tumors and H. pylori infection, compared to Western cohorts which have more proximal GEJ tumors. Furthermore, ATTRACTION-2 evaluated PD-L1 expression solely on tumor cells using the Tumor Proportion Score (TPS), whereas later studies demonstrated that the Combined Positive Score (CPS), which includes lymphocytes and macrophages, is a far more accurate predictive biomarker for PD-1 inhibitor efficacy in upper GI malignancies.

Attending
Attending

In the ATTRACTION-2 trial, nivolumab was compared to placebo in the third-line setting. How do you counsel a heavily pretreated patient about the absolute versus relative survival benefits of this therapy, particularly regarding the 'tail of the survival curve' phenomenon?

Key Response

While the trial showed a statistically significant relative reduction in the risk of death, the absolute median overall survival improvement was modest (5.26 months vs 4.14 months). Counseling requires explaining that while average gains are small, immunotherapy is characterized by a 'tail on the curve' where a subset of patients achieves durable, long-term survival (e.g., 12-month OS was 26.2% for nivolumab vs 10.9% for placebo), which must be weighed against potential toxicities in the palliative setting.

Scholarly Review

Critical appraisal through the lens of expert reviewers and guideline development

PhD
PhD

The ATTRACTION-2 study was conducted exclusively in Asian countries. From a methodological and epidemiological standpoint, how does this geographical restriction impact the external validity of the trial, and what study design strategies are necessary to establish global applicability?

Key Response

Genetic, environmental, and standard-of-care differences between Asian and Western gastric cancer populations severely threaten the external validity of this study. To establish global generalizability, researchers must employ multi-regional clinical trials (MRCTs) with pre-planned stratification and adequately powered subgroup analyses by geographic region, alongside harmonization of biomarker assays and subsequent-line treatment protocols.

Journal Editor
Journal Editor

Given that tissue availability in the third-line setting is often limited to archival primary tumor biopsies, how does temporal and spatial tumor heterogeneity threaten the validity of the PD-L1 subgroup analyses presented in the ATTRACTION-2 manuscript?

Key Response

Using archival tissue from initial diagnosis to assess PD-L1 status in the third-line setting ignores the dynamic nature of the tumor immune microenvironment, which frequently evolves after multiple lines of cytotoxic chemotherapy. A rigorous reviewer would flag that the lack of fresh pre-treatment biopsies severely limits the reliability of the PD-L1 subgroup findings, potentially masking the true predictive value of the biomarker at the exact time of study entry.

Guideline Committee
Guideline Committee

Based on the ATTRACTION-2 data and subsequent global trials, should nivolumab be universally recommended as a category 1 option for all patients with advanced gastric cancer in the third-line setting, or should guidelines mandate restriction based on PD-L1 CPS and MSI-H status?

Key Response

While ATTRACTION-2 initially supported a broad approval in Asia, global guidelines like NCCN and ESMO have evolved to heavily prioritize biomarkers. Current guidelines strongly prioritize the use of checkpoint inhibitors for patients with MSI-H/dMMR tumors or high PD-L1 CPS expression, reflecting the nuanced integration of ATTRACTION-2 with trials like CheckMate-649 and KEYNOTE-059, emphasizing biomarker-directed stewardship rather than universal unselected application in later lines.

Clinical Landscape

Noteworthy Related Trials

2018

KEYNOTE-061 Trial

n = 592 · Lancet

Tested

Pembrolizumab

Population

Advanced gastric or GEJ cancer progressing on first-line chemotherapy

Comparator

Paclitaxel

Endpoint

Overall survival in patients with PD-L1 CPS >= 1

Key result: Pembrolizumab did not significantly improve overall survival compared to paclitaxel as a second-line therapy in this patient population.
2018

TAGS Trial

n = 507 · Lancet Oncol

Tested

Trifluridine/tipiracil (TAS-102)

Population

Heavily pretreated metastatic gastric or GEJ cancer (>= 2 prior regimens)

Comparator

Placebo

Endpoint

Overall survival

Key result: Trifluridine/tipiracil significantly prolonged overall survival compared to placebo, establishing it as an effective late-line treatment option.
2021

CheckMate 649 Trial

n = 1,581 · Lancet

Tested

Nivolumab plus chemotherapy

Population

Previously untreated advanced gastric, GEJ, or esophageal adenocarcinoma

Comparator

Chemotherapy alone

Endpoint

OS and PFS in PD-L1 CPS >= 5

Key result: Nivolumab plus chemotherapy significantly improved overall survival compared to chemotherapy alone in patients with PD-L1 CPS of 5 or greater.

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