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VALOR

Trial of Antisense Oligonucleotide Tofersen for SOD1 ALS

Year of Publication: 2022

Authors: Timothy M. Miller, Merit E. Cudkowicz, Angela Genge, ..., for the VALOR and OLE Working Group

Journal: New England Journal of Medicine

Citation: N Engl J Med 2022;387:1099-1110

Link: https://doi.org/10.1056/NEJMoa2204705


Clinical Question

Does the intrathecally administered antisense oligonucleotide tofersen, which reduces SOD1 protein synthesis, improve clinical outcomes in patients with ALS associated with SOD1 mutations?

Bottom Line

Tofersen demonstrated clear target engagement with significant reductions in CSF SOD1 protein and plasma neurofilament light chains, but did not significantly improve clinical endpoints at 28 weeks. Combined analysis at 52 weeks comparing early-start vs delayed-start cohorts suggested potential clinical benefit with earlier treatment initiation, though these results require cautious interpretation due to lack of multiplicity adjustment.

Major Points

  • Primary endpoint not met: ALSFRS-R change at 28 weeks was -6.98 with tofersen vs -8.14 with placebo (difference 1.2 points, p=0.97)
  • Clear target engagement demonstrated: CSF SOD1 reduced by 29% with tofersen vs 16% increase with placebo
  • Plasma neurofilament light chains reduced by 60% with tofersen vs 20% increase with placebo
  • 88% of participants entered the open-label extension (95 of 108)
  • At 52 weeks, early-start cohort showed -6.0 point ALSFRS-R change vs -9.5 in delayed-start cohort (difference 3.5 points, 95% CI 0.4-6.7)
  • Neurologic serious adverse events occurred in 7% of tofersen recipients (myelitis, aseptic meningitis, lumbar radiculopathy, increased intracranial pressure, papilledema)
  • 42 SOD1 mutations represented across 108 participants
  • Trial included 16 participants with p.Ala5Val mutation (aggressive phenotype)
  • Baseline imbalances existed: neurofilament light chains 15-25% higher and ALSFRS-R decline faster in tofersen group
  • Study may have been underpowered due to slower-than-projected disease progression in placebo group

Design

Study Type: Phase 3, multicenter, randomized, double-blind, placebo-controlled trial with open-label extension

Randomization: 1

Blinding: Double-blind. Participants, investigators, and site staff remained blinded during extension phase to original VALOR assignments. Tofersen and placebo (artificial CSF) administered via identical intrathecal injection.

Enrollment Period: March 2019 to July 2021

Follow-up Duration: 28 weeks (randomized phase); 52 weeks (combined analysis); ongoing extension up to 236 weeks

Centers: 32

Countries: United States, Canada, United Kingdom, Germany, Italy, Belgium, Japan, France, Netherlands, Australia

Sample Size: 108

Analysis: Joint rank test for primary endpoint accounting for functional decline and survival. ANCOVA with multiple imputation for missing data. Randomization stratified by edaravone/riluzole use and faster/slower progression criteria. Sequential closed testing procedure for secondary endpoints. 84% power to detect treatment difference assuming ALSFRS-R change of -4.8 (tofersen) vs -24.7 (placebo). Combined analysis at 52 weeks adjusted for baseline neurofilament light chain concentration as covariate.


Inclusion Criteria

  • Adults with weakness attributable to ALS
  • Confirmed SOD1 mutation
  • Faster-progression subgroup criteria based on SOD1 mutation type and prerandomization ALSFRS-R slope (for primary analysis population)

Exclusion Criteria

  • Not specified in detail in the primary publication

Arms

FieldTofersenControl
InterventionTofersen 100mg intrathecal bolus injection through lumbar puncture (15-mL solution). Three doses once every 2 weeks, followed by five doses once every 4 weeks (8 doses total over 24 weeks).Artificial cerebrospinal fluid, equivalent 15-mL volume, administered via intrathecal injection on same schedule as tofersen
Duration24 weeks treatment; 28 weeks follow-up; ongoing open-label extension up to 236 weeks24 weeks treatment; 28 weeks follow-up; crossover to tofersen in open-label extension

Outcomes

OutcomeTypeControlInterventionHR / OR / RRP-value
Change from baseline to week 28 in ALSFRS-R total score (range 0-48, higher = better function) in faster-progression subgroup, analyzed using joint rank testPrimary-8.14 (adjusted mean change)-6.98 (adjusted mean change)0.97 (joint rank test)
CSF SOD1 protein concentration (faster-progression subgroup)SecondaryGeometric mean ratio to baseline 1.16 (16% increase)Geometric mean ratio to baseline 0.71 (29% reduction)0.62Not formally tested (primary endpoint not met)
Plasma neurofilament light chains (faster-progression subgroup)SecondaryGeometric mean ratio to baseline 1.20 (20% increase)Geometric mean ratio to baseline 0.40 (60% reduction)0.33Not formally tested
Slow vital capacity % predicted (faster-progression subgroup)Secondary-22.2 percentage points-14.3 percentage pointsNot formally tested
Handheld dynamometry megascore (faster-progression subgroup)Secondary-0.37-0.34Not formally tested
Death or permanent ventilation (faster-progression subgroup)Secondary2/21 (10%)4/39 (10%)1.39Not formally tested
ALSFRS-R change at 52 weeks (combined analysis, all participants)Secondary-9.5 (delayed-start cohort)-6.0 (early-start cohort)Not adjusted for multiplicity; difference 3.5 (95% CI 0.4-6.7)
Slow vital capacity at 52 weeks (combined analysis)Secondary-18.6% (delayed-start)-9.4% (early-start)Not adjusted; difference 9.2 (95% CI 1.7-16.6)
Time to death or permanent ventilation (combined analysis)SecondaryReference (delayed-start)HR 0.36 (early-start)0.3695% CI 0.14-0.94
Time to death (combined analysis)SecondaryReference (delayed-start)HR 0.27 (early-start)0.2795% CI 0.08-0.89
Any adverse eventAdverse34 (94%)69 (96%) in VALOR; 102 (98%) combined
Serious adverse eventAdverse5 (14%)13 (18%) in VALOR; 38 (37%) combined
Serious event related to trial agentAdverse0 (0%)4 (6%) in VALOR; 7 (7%) combined
Neurologic serious adverse events (myelitis, aseptic meningitis, radiculopathy, increased ICP, papilledema)Adverse07 (7% of all tofersen recipients)
DeathAdverse0 in VALOR1 (1%) in VALOR; 14 (13%) combined
Procedural painAdverse21 (58%)41 (57%)
HeadacheAdverse16 (44%)33 (46%)
Back painAdverse2 (6%)15 (21%)
Pain in arm or legAdverse6 (17%)19 (26%)
CSF pleocytosis (>10 cells/mm³)Adverse2 (6%)42 (58%)
Elevated CSF proteinAdverse~40% at baseline; median change -15 mg/L~40% at baseline; median change +110 mg/L

Subgroup Analysis

Primary analysis was conducted in the faster-progression subgroup (n=60) defined by SOD1 mutation type and prerandomization ALSFRS-R slope. Slower-progression subgroup (n=48) was enrolled but not included in primary efficacy analysis. Combined analysis at 52 weeks included all 108 participants regardless of progression group. Subgroup analyses by baseline neurofilament light chain concentration (above vs below median) were prespecified. Baseline imbalances were noted with higher neurofilament levels (15-25% higher) and faster ALSFRS-R decline in tofersen group. 16 participants had p.Ala5Val mutation (most aggressive phenotype); median disease duration 1.73 years with 3 still in trial at data cutoff.


Criticisms

  • Primary endpoint not achieved - no significant clinical benefit demonstrated at 28 weeks
  • Baseline imbalances: neurofilament light chains 15-25% higher and ALSFRS-R decline faster in tofersen group
  • Study may have been underpowered due to slower-than-projected disease progression in placebo group (3x slower than anticipated)
  • Prognostic criteria for faster/slower progression using SOD1 mutation type and prerandomization ALSFRS-R slope may not be consistently prognostic over short trial periods
  • Combined analysis at 52 weeks not adjusted for multiplicity - no definitive conclusions can be drawn
  • ~20% missing data requiring imputation in combined analysis
  • VALOR results were known at time of combined analysis, potentially introducing bias
  • Short 28-week duration may be insufficient to detect clinical benefit
  • CSF pleocytosis in 58% of tofersen recipients raises questions about inflammatory response
  • Neurologic serious adverse events (myelitis, meningitis) in 7% of recipients - mechanism unclear
  • Relationship between CSF pleocytosis/elevated protein and myelitis not established
  • Heterogeneous population with 42 different SOD1 mutations makes interpretation difficult
  • Intrathecal administration via repeated lumbar punctures creates burden and procedural complications

Funding

Funded by Biogen

Based on: VALOR (New England Journal of Medicine, 2022)

Authors: Timothy M. Miller, Merit E. Cudkowicz, Angela Genge, ..., for the VALOR and OLE Working Group

Citation: N Engl J Med 2022;387:1099-1110

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