Journal of Clinical Oncology JUNE 11, 2021

Final Overall Survival Analysis of the TOURMALINE-MM1 Phase III Trial of Ixazomib, Lenalidomide, and Dexamethasone in Patients With Relapsed or Refractory Multiple Myeloma

Paul G. Richardson, Shaji K. Kumar, Tamas Masszi, et al.

Bottom Line

The TOURMALINE-MM1 trial found that the addition of the oral proteasome inhibitor ixazomib to lenalidomide and dexamethasone significantly improved progression-free survival, though final analysis showed no statistically significant benefit in overall survival, likely confounded by subsequent therapies.

Key Findings

1. The primary endpoint was met with a significant improvement in progression-free survival (PFS): median 20.6 months for the ixazomib-Rd arm versus 14.7 months for the placebo-Rd arm (HR 0.74; 95% CI, 0.59 to 0.94; P = .01).
2. Final analysis after a median follow-up of 85 months showed median overall survival (OS) of 53.6 months with ixazomib-Rd versus 51.6 months with placebo-Rd (HR 0.939; P = .495), failing to demonstrate a statistically significant difference in the intent-to-treat population.
3. OS interpretation was notably confounded by imbalances in subsequent therapies, with placebo-Rd patients receiving more subsequent proteasome inhibitors and daratumumab, potentially masking survival benefits.
4. Subgroup analyses suggested larger magnitudes of OS benefit in specific populations, such as those refractory to their last treatment line (HR 0.742) or those with ISS stage III disease (HR 0.779).

Study Design

Design
RCT
Double-Blind
Sample
722
Patients
Duration
85 mo
Median
Setting
Multicenter, international
Population Adult patients with relapsed, refractory, or relapsed and refractory multiple myeloma who had received 1-3 prior lines of therapy.
Intervention Ixazomib (4 mg) in combination with lenalidomide and dexamethasone.
Comparator Placebo in combination with lenalidomide and dexamethasone.
Outcome Progression-free survival (PFS) assessed by a blinded independent review committee per 2011 International Myeloma Working Group criteria.

Study Limitations

The study did not achieve a statistically significant improvement in the primary secondary endpoint of overall survival in the intention-to-treat population.
Extensive use of subsequent lines of therapy, including novel agents like daratumumab, significantly confounded the ability to isolate the specific impact of the ixazomib-Rd regimen on long-term survival.
Imbalances in the receipt of salvage treatments between the two study arms complicate the final interpretation of OS data.

Clinical Significance

The study established ixazomib-Rd as an effective all-oral triplet regimen for relapsed or refractory multiple myeloma, providing a convenient alternative to parenteral proteasome inhibitors, though its role in long-term survival remains subject to the complexities of modern salvage therapy sequencing.

Historical Context

TOURMALINE-MM1 was the first global, phase III, double-blind, placebo-controlled trial evaluating an all-oral triplet regimen containing a proteasome inhibitor (ixazomib) for patients with relapsed or refractory multiple myeloma, marking a significant step toward improving treatment convenience and reducing clinical burden.

Guided Discussion

High-yield insights from every perspective

Med Student
Medical Student

Ixazomib is a proteasome inhibitor used in the TOURMALINE-MM1 trial. Can you describe the primary mechanism by which inhibiting the 26S proteasome leads to the death of malignant plasma cells in multiple myeloma?

Key Response

Proteasome inhibitors block the degradation of misfolded proteins and regulatory molecules such as IκB. The accumulation of misfolded proteins triggers the unfolded protein response (ER stress), while the stabilization of IκB prevents the translocation of NF-κB to the nucleus, thereby inhibiting pro-survival signaling and inducing apoptosis in plasma cells, which are particularly sensitive due to their high protein secretory burden.

Resident
Resident

The TOURMALINE-MM1 trial evaluated the triplet of ixazomib, lenalidomide, and dexamethasone (IRd) against lenalidomide and dexamethasone (Rd). In which clinical scenarios would the IRd regimen be preferred over other triplet therapies like daratumumab-Rd or carfilzomib-Rd for a patient with relapsed multiple myeloma?

Key Response

IRd is the first all-oral triplet regimen for RRMM. It is particularly valuable for patients who prioritize convenience, live far from infusion centers, or have significant frailty/comorbidities that make frequent clinic visits for IV/subcutaneous infusions (like daratumumab or carfilzomib) burdensome. However, its lower relative efficacy in terms of depth of response compared to daratumumab-based triplets must be balanced against these logistical benefits.

Fellow
Fellow

The final analysis of TOURMALINE-MM1 showed a significant improvement in progression-free survival (PFS) but failed to reach statistical significance for overall survival (OS). What role does 'post-progression survival' (PPS) and subsequent lines of therapy play in the difficulty of demonstrating OS benefits in modern multiple myeloma trials?

Key Response

As survival for RRMM extends into many years, patients receive multiple subsequent lines of highly effective therapy (e.g., monoclonal antibodies, CAR-T, or BCMA-targeted agents) after progressing on a clinical trial. This 'crossover' effect and the long duration of PPS dilute the initial treatment's impact on OS, making OS a difficult primary endpoint to reach in MM compared to PFS, which more directly reflects the intervention's efficacy.

Attending
Attending

The median OS for the ixazomib arm in TOURMALINE-MM1 was 53.6 months versus 48.1 months for the control. How do these results influence your long-term management strategy for a 'standard-risk' patient at first relapse, particularly regarding the sequencing of oral versus parenteral therapies?

Key Response

The data confirms that even without a statistically significant OS 'win,' the IRd regimen contributes to a prolonged survival trajectory. It reinforces a 'marathon' approach to MM management where preserving quality of life through oral regimens is viable, provided the clinician monitors closely for the need to escalate to more potent parenteral triplets (like those containing carfilzomib or daratumumab) if high-risk features emerge or the response is suboptimal.

Scholarly Review

Critical appraisal through the lens of expert reviewers and guideline development

PhD
PhD

In the TOURMALINE-MM1 OS analysis, the hazard ratio was 0.939 with a p-value of 0.495. Given the high rate of subsequent anti-myeloma therapies in both arms (approx. 70%), what statistical modeling techniques could have been utilized to adjust for treatment switching to better estimate the counterfactual OS benefit?

Key Response

To account for the confounding effects of subsequent therapies, researchers can use Rank Preserving Structural Failure Time (RPSFT) models, Inverse Probability of Censoring Weighting (IPCW), or two-stage estimation methods. These models attempt to estimate what the OS would have been if the control group had not received the active drug or other potent subsequent therapies, providing a more direct measure of the drug's intrinsic survival impact.

Journal Editor
Journal Editor

As a reviewer, if the primary endpoint of PFS was met in the initial 2016 report, what is the scientific and ethical value of publishing this 'negative' final OS analysis five years later, and what specific data points would you look for to ensure the OS data isn't misleading?

Key Response

The value lies in providing a complete long-term safety profile and determining if the early PFS benefit translated into a late survival detriment (which would be a major safety signal). An editor would scrutinize the 'subsequent therapy' table to ensure balance between arms; if the control arm received significantly more potent subsequent therapies (like daratumumab), it explains the lack of OS difference and prevents the drug from being unfairly labeled as ineffective for survival.

Guideline Committee
Guideline Committee

NCCN guidelines currently list IRd as a Category 1 recommendation for RRMM. Does the lack of a statistically significant OS benefit in the final TOURMALINE-MM1 analysis warrant a downgrade of this recommendation, and how does it compare to the OS data seen in the POLLUX (daratumumab-Rd) or ASPIRE (carfilzomib-Rd) trials?

Key Response

While IRd remains Category 1 based on its proven PFS benefit and manageable safety profile, it is often viewed as a 'preferred' option primarily for specific patient populations (e.g., those needing all-oral therapy). In contrast, trials like POLLUX showed much more robust OS hazard ratios. The committee must decide if IRd remains 'preferred' or if it should be relegated to 'other recommended regimens' when OS-positive triplets are accessible and tolerated by the patient.

Clinical Landscape

Noteworthy Related Trials

2013

FIRST Trial

n = 1,623 · NEJM

Tested

Lenalidomide plus dexamethasone (Rd) until progression

Population

Patients with newly diagnosed multiple myeloma ineligible for stem-cell transplantation

Comparator

Melphalan, prednisone, and thalidomide (MPT)

Endpoint

Progression-free survival

Key result: Continuous treatment with Rd significantly improved progression-free survival compared to MPT.
2014

PANORAMA 1 Trial

n = 768 · Lancet Oncol

Tested

Panobinostat, bortezomib, and dexamethasone

Population

Patients with relapsed or refractory multiple myeloma

Comparator

Placebo, bortezomib, and dexamethasone

Endpoint

Progression-free survival

Key result: The addition of the HDAC inhibitor panobinostat significantly improved progression-free survival in patients previously treated with bortezomib and IMiDs.
2015

ASPIRE Trial

n = 792 · NEJM

Tested

Carfilzomib, lenalidomide, and dexamethasone (KRd)

Population

Patients with relapsed or refractory multiple myeloma

Comparator

Lenalidomide and dexamethasone (Rd)

Endpoint

Progression-free survival

Key result: The addition of carfilzomib to Rd significantly improved progression-free survival in patients with relapsed disease.

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