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Tocilizumab ALS Safety Trial

Tocilizumab is safe and tolerable and reduces C-reactive protein concentrations in the plasma and cerebrospinal fluid of ALS patients

Year of Publication: 2021

Authors: Carol Milligan, Nazem Atassi, Suma Babu, ..., Shafeeq S. Ladha

Journal: Muscle & Nerve

Citation: Muscle Nerve. 2021 September;64(3):309-320

Link: https://doi.org/10.1002/mus.27339


Clinical Question

Is tocilizumab safe and tolerable in ALS patients with elevated inflammatory markers, and does it demonstrate target engagement by reducing inflammatory biomarkers in plasma and CSF?

Bottom Line

Tocilizumab was safe and well tolerated in ALS patients with high inflammatory gene expression profiles. Treatment significantly reduced plasma CRP by 88% and CSF CRP by 1.8-fold relative to placebo, with CSF effects potentially dependent on IL6R Asp358Ala genotype. PBMC gene expression was not useful as a predictive or pharmacodynamic biomarker. These results warrant further study in ALS patients enriched for IL6R C allele carriers and elevated CRP levels.

Major Points

  • First study to demonstrate tocilizumab safety and tolerability specifically in ALS patients
  • Plasma CRP reduced by 88% in tocilizumab group vs 4% increase in placebo (-3.1-fold relative change, p=0.003)
  • CSF CRP reduction of 1.8-fold relative to placebo (p=0.01 unadjusted), first demonstration of tocilizumab effect on CSF CRP
  • CSF CRP reduction was greater in individuals with more IL6R C allele copies, suggesting genotype-dependent effects
  • Plasma IL-6 increased 2.9-fold and plasma sIL-6R increased 3.4-fold with tocilizumab (expected pharmacodynamic effect)
  • PBMC inflammatory gene expression (IL6, IL8, MMP1) was not a useful pharmacodynamic biomarker
  • No clinical efficacy signal detected, but study was not powered for clinical outcomes
  • IL6R C allele frequency of 0.50 in study population (higher than expected 0.37)
  • Results support IL-6 trans-signaling as potential therapeutic target in ALS subpopulation

Design

Study Type: Phase 2, multicenter, randomized, double-blind, placebo-controlled trial

Randomization: 1

Blinding: Double-blind

Enrollment Period: 2015 to 2019

Follow-up Duration: 16 weeks

Centers: 5

Countries: United States

Sample Size: 22

Analysis: Shared-baseline, repeated-measures mixed model with fixed terms for visits, treatment group × postbaseline visit, and random participant-specific visits with unstructured covariance. Log-transformation for target engagement measures. Linear contrasts for treatment-specific mean change. Fisher exact test for primary biomarker endpoint. Step-down Bonferroni adjustment for multiple comparisons. 80% power to detect treatment-dependent difference if ≤5% placebo and ≥30% tocilizumab participants experienced 2-fold decline in ≥2 of 3 pro-inflammatory genes. SAS version 9.4.


Inclusion Criteria

  • Age 18-75 years
  • Revised El Escorial criteria for possible, laboratory-supported probable, probable, or definite ALS
  • Slow vital capacity ≥60% predicted (later relaxed to ≥40%)
  • ≤36 months of ALS-related weakness (later relaxed to any duration)
  • High-inflammatory PBMC gene expression profile defined as: 3-fold upregulation of IL6 vs healthy controls OR 2-fold upregulation of IL6 with 2-fold upregulation of IL8 or MMP1

Exclusion Criteria

  • Not meeting high-inflammatory PBMC gene expression criteria
  • Other standard exclusion criteria for ALS trials (not fully specified in document)

Arms

FieldTocilizumabControl
InterventionTocilizumab 8 mg/kg intravenous infusion at weeks 0, 4, and 8 (3 treatments total)Placebo intravenous infusion at weeks 0, 4, and 8 (3 treatments total)
Duration8 weeks of treatment, 16 weeks follow-up8 weeks of treatment, 16 weeks follow-up

Outcomes

OutcomeTypeControlInterventionHR / OR / RRP-value
Safety (proportion experiencing treatment-emergent adverse events per MedDRA) and tolerability (completing all infusions and study visits). Secondary primary: proportion with ≥2-fold decline in ≥2 of 3 pro-inflammatory genes (IL6, IL8, MMP1)PrimaryTolerability: 75% (6/8 completed). 1 severe AE (aspiration pneumonia). 2 withdrew consent.Tolerability: 86% (12/14 completed). No severe AEs. 2 discontinued infusions (neutropenia, C. difficile colitis) but completed visits.0.60 (tolerability comparison)
Plasma CRP change (baseline to mean of weeks 4-16)Secondary+4% (95% CI -59% to +259%)-88% (95% CI -94% to -76%)0.003 (adjusted); -3.1-fold relative change
CSF CRP change (baseline to week 8)SecondaryNo significant change-1.8-fold relative change vs placebo (95% CI -3.1 to -0.4)0.01 (unadjusted); 0.22 (adjusted)
Plasma IL-6 changeSecondary-0.09-fold (95% CI -0.6 to +0.4)+2.9-fold (95% CI 2.6 to 3.2)<0.001 (adjusted); 3.0-fold relative change
Plasma sIL-6R changeSecondary-0.02-fold (95% CI -0.44 to +0.40)+3.4-fold (95% CI 3.1 to 3.6)<0.001 (adjusted); 3.4-fold relative change
CSF IL-6 change (baseline to week 8)SecondaryNo significant change+1.1-fold relative change vs placebo (95% CI 0.6 to 1.6)0.002 (adjusted)
CSF sIL-6R change (baseline to week 8)SecondaryNo significant change+0.6-fold relative change vs placebo (95% CI 0.4 to 0.8)<0.001 (adjusted)
PBMC IL6 gene expressionSecondaryNo significant changeNo significant change0.28
PBMC IL8 gene expressionSecondaryNo significant changeNo significant change0.53
PBMC MMP1 gene expressionSecondaryNo significant changeNo significant change0.88
ALSFRS-R total score rate of changeSecondaryNot significantly differentNot significantly differentNot significant (confidence bounds too wide)
CSF CRP change by IL6R genotype - per C alleleSecondaryReference-0.8-fold additional reduction per C allele (95% CI -1.5 to -0.09)0.03 (unadjusted); 0.74 (adjusted)
Serious Adverse EventsAdverse1 (aspiration pneumonia)0
Injection-site infectionAdverse10
Clostridium difficile colitisAdverse01 (resolved, discontinued infusions)
Neutropenia (asymptomatic)Adverse01 (had borderline neutropenia at baseline, resolved by week 16)
DeathsAdverse00

Subgroup Analysis

Participants were genotyped for IL6R Asp358Ala polymorphism (rs2228145). Minor allele frequency was 0.50 for IL6R C allele (6 AA, 10 AC, 6 CC genotypes). Baseline plasma sIL-6R was higher with more C allele copies (p=0.02). CSF CRP reduction was greater in participants with more IL6R C allele copies (-0.8-fold additional reduction per C allele, unadjusted p=0.03), suggesting IL-6 trans-signaling may mediate a distinct CNS response in C allele carriers. Plasma effects on CRP, IL-6, and sIL-6R were consistent across all genotypes. CSF IL-6 and sIL-6R increases were not influenced by genotype.


Criticisms

  • Very small sample size (n=22) limits statistical power for efficacy and subgroup analyses
  • PBMC inflammatory gene expression profile was not useful as predictive or pharmacodynamic biomarker
  • CSF CRP significance not maintained after correction for multiple comparisons (unadjusted p=0.01, adjusted p=0.22)
  • CRP was not prespecified as selection criterion - in retrospect would have been more useful than PBMC gene expression
  • Tocilizumab levels in CSF were not measured
  • Study not powered to detect clinical effects
  • Participants had slower-than-average disease progression (ALSFRS-R decline <3 points), making clinical benefit harder to detect
  • Short treatment duration (8 weeks) and follow-up (16 weeks)
  • Higher than expected IL6R C allele frequency (0.50 vs 0.37) may reflect selection bias from PBMC criteria
  • Increased circulating IL-6 levels with treatment raise theoretical concern, though likely reflects altered catabolism rather than pathway upregulation
  • Genotype-dependent CSF CRP effects were post-hoc and require confirmation

Funding

Clinical and Translational Science Awards grant from National Center for Advancing Translational Sciences (UL1TR002366); The ALS Association; Massachusetts General Hospital Neurology Clinical Research Institute; Genentech, Inc; Barrow Neurological Foundation; ALS ONE; Hope For Tomorrow Foundation; gift in memory of Murray Sherman, MD

Based on: Tocilizumab ALS Safety Trial (Muscle & Nerve, 2021)

Authors: Carol Milligan, Nazem Atassi, Suma Babu, ..., Shafeeq S. Ladha

Citation: Muscle Nerve. 2021 September;64(3):309-320

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