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EMERGE / ENGAGE

Two Randomized Phase 3 Studies of Aducanumab in Early Alzheimer's Disease

Year of Publication: 2022

Authors: S. Budd Haeberlein, P.S. Aisen, F. Barkhof, ..., A. Sandrock

Journal: Journal of Prevention of Alzheimer's Disease (JPAD)

Citation: J Prev Alz Dis 2022;2(9):197-210

Link: http://dx.doi.org/10.14283/jpad.2022.30


Clinical Question

Does aducanumab, a human monoclonal antibody targeting aggregated amyloid beta, slow clinical decline in patients with early Alzheimer's disease (MCI due to AD or mild AD dementia)?

Bottom Line

Results were discordant between two identically designed trials. EMERGE met its primary endpoint, with high-dose aducanumab reducing CDR-SB decline by 22% vs placebo and showing consistent benefit across all secondary endpoints. ENGAGE did not meet its primary or secondary endpoints. Both trials confirmed dose-dependent amyloid plaque reduction and downstream biomarker changes. The discordance is attributed to differential high-dose exposure resulting from protocol amendment timing. ARIA-E was the most common adverse event (35–36% at high dose).

Major Points

  • EMERGE and ENGAGE were two identically designed phase 3 RCTs of aducanumab in early AD, enrolling 1638 and 1647 patients respectively across 348 sites in 20 countries
  • Both trials were terminated early based on a prespecified futility analysis after ~50% of patients had opportunity to complete week 78; the futility analysis was based on two violated assumptions (similar treatment effect between studies and constancy of effect over time)
  • EMERGE primary endpoint met: high-dose aducanumab reduced CDR-SB decline by 22% vs placebo (−0.39; 95% CI −0.69 to −0.09; P=.012)
  • EMERGE secondary endpoints all met: MMSE −18% (P=.049), ADAS-Cog13 −27% (P=.010), ADCS-ADL-MCI −40% (P<.001)
  • ENGAGE primary endpoint not met: CDR-SB difference 0.03 vs placebo (95% CI −0.26 to 0.33; P=.833); no secondary endpoints were significant
  • Both trials showed significant dose- and time-dependent reduction in amyloid PET SUVR: EMERGE high dose −0.278 (71% reduction on centiloid scale), ENGAGE high dose −0.232 (59% reduction); the 16.5% lower reduction in ENGAGE may partly explain the clinical discordance
  • Dose-dependent reductions in plasma p-tau181 and CSF p-tau/t-tau observed in both studies, confirming downstream target engagement
  • Two protocol amendments (PV3 and PV4) allowed more patients to achieve the 10 mg/kg target dose; due to enrollment differences, these amendments benefited more EMERGE than ENGAGE patients (29% vs 22% received full 14 doses of 10 mg/kg)
  • ARIA-E occurred in 35% (EMERGE) and 36% (ENGAGE) of high-dose patients; incidence was higher in ApoE ε4 carriers (42–43%) and homozygous carriers (65%); 98% resolved on study, most within 12–16 weeks
  • 16 deaths occurred across both studies (5 placebo, 3 low dose, 8 high dose); none attributed to study treatment
  • Low-dose results were generally intermediate between high dose and placebo in both trials but not statistically significant

Design

Study Type: Two identically designed randomized, double-blind, placebo-controlled, global phase 3 trials

Randomization: 1

Blinding: Double-blind. Participants, families, and blinded study team were unaware of treatment assignment. Two independent efficacy raters were blinded to ARIA and medical information. Unblinded pharmacy staff managed treatment preparation. Treating physicians managed ARIA but could not serve as raters and had no access to post-baseline efficacy data.

Enrollment Period: August 2015 (ENGAGE) / September 2015 (EMERGE) to July 2018; terminated March 21, 2019

Follow-up Duration: 78 weeks (76 weeks of dosing + week 78 assessment); mean follow-up ~74–75 weeks

Centers: 348

Countries: USA, Canada, UK, Netherlands, France, Sweden, Japan, and 13 other countries (20 total)

Sample Size: 3285

Analysis: Mixed model for repeated measures (MMRM) with fixed effects for treatment, categorical visit, treatment-by-visit interaction, baseline score, baseline score-by-visit interaction, baseline MMSE, AD medication use, region, and ApoE ε4 status. Randomized and dosed population. Data collected after March 20, 2019 excluded. Sequential multiplicity-adjusted testing procedure for primary and secondary endpoints. Prespecified sensitivity analyses for missing data. Biomarker analyses exploratory. SAS software used.


Inclusion Criteria

  • Age 50–85 years
  • Clinical criteria for MCI due to AD or mild AD dementia
  • Amyloid pathology confirmed by visual assessment of amyloid PET (18F-florbetapir, 18F-flutemetamol, or 18F-florbetaben)
  • MMSE score 24–30
  • CDR global score 0.5
  • Stable use of concomitant medications for chronic conditions permitted
  • If on cholinesterase inhibitors or memantine, must be on stable dose before screening

Exclusion Criteria

  • Confounding brain pathologies on MRI: acute or sub-acute hemorrhage, >4 microhemorrhages, cortical infarcts, >1 lacunar infarct, superficial siderosis, or significant white matter disease
  • Conditions posing risk to patient or preventing MRI monitoring
  • Medical conditions possibly contributing to cognitive impairment
  • Use of medications with anti-platelet or anticoagulant properties (except aspirin ≤325 mg daily)
  • Hepatitis B or C positive
  • Unstable chronic medication doses (<4 weeks stable) or unstable AD medication doses (<8 weeks stable)

Arms

FieldControlLow-dose aducanumabHigh-dose aducanumab
InterventionMatching IV saline infusion every 4 weeks over 76 weeks (20 doses total)Aducanumab IV infusion every 4 weeks, titrated to target dose of 3 mg/kg (ApoE ε4+) or 6 mg/kg (ApoE ε4−), over 76 weeks (20 doses total)Aducanumab IV infusion every 4 weeks, titrated to target dose of 10 mg/kg (initially 6 mg/kg for ApoE ε4+ carriers, increased to 10 mg/kg per PV4 amendment), over 76 weeks (20 doses total)
Duration76 weeks76 weeks76 weeks

Outcomes

OutcomeTypeControlInterventionHR / OR / RRP-value
Change from baseline to week 78 in CDR-SB (Clinical Dementia Rating Sum of Boxes; range 0–18, higher = greater impairment)Primary
MMSE change from baseline at week 78 (range 0–30, lower = greater impairment)Secondary
ADAS-Cog13 change from baseline at week 78 (range 0–85, higher = greater impairment)Secondary
ADCS-ADL-MCI change from baseline at week 78 (range 0–53, lower = greater impairment)Secondary
NPI-10 change from baseline at week 78 (tertiary endpoint)Secondary
Amyloid PET SUVR change from baseline at week 78Secondary
Plasma p-tau181 change from baseline at week 78Secondary
ARIA-E (EMERGE)Adverse2%
ARIA-E (ENGAGE)Adverse3%
ARIA-E in ApoE ε4 homozygous carriers (combined high dose)Adverse
Brain microhemorrhage (EMERGE)Adverse7%
Brain microhemorrhage (ENGAGE)Adverse6%
Localized superficial siderosis (EMERGE)Adverse3%
Localized superficial siderosis (ENGAGE)Adverse2%
Headache (EMERGE)Adverse15%
Headache (ENGAGE)Adverse15%
Fall (EMERGE)Adverse13%
Fall (ENGAGE)Adverse11%
Serious adverse events (EMERGE)Adverse15%
Serious adverse events (ENGAGE)Adverse13%
Deaths (pooled both studies)Adverse
Serious ARIA events (EMERGE high dose)Adverse
Serious ARIA events (ENGAGE high dose)Adverse
Symptomatic ARIA (EMERGE high dose)Adverse
Symptomatic ARIA (ENGAGE high dose)Adverse

Subgroup Analysis

In EMERGE, high-dose aducanumab showed numerical advantage over placebo in all prespecified subgroups for the primary endpoint and 47 of 48 subgroups for secondary endpoints (79 of 80 total subgroup comparisons favored aducanumab). In ENGAGE, low-dose subgroup results were generally consistent, while high-dose subgroup results were more variable. ApoE ε4 carrier status was a key modifier of both efficacy (via dose exposure) and safety (higher ARIA rates in carriers).


Criticisms

  • Discordant results between two identically designed trials fundamentally undermine confidence in efficacy conclusions; a single positive trial (EMERGE) is insufficient to establish clinical benefit
  • Both trials were terminated early based on a futility analysis whose two core assumptions were violated — this raises questions about data completeness and the validity of post-hoc explanations for the discordance
  • The explanation for discordance (differential dosing due to protocol amendments) is post-hoc; 29% vs 22% receiving full 14 doses of 10 mg/kg is a modest difference to explain fully negative vs fully positive results
  • The 22% reduction in CDR-SB decline (0.39 points on an 18-point scale) in EMERGE is of uncertain clinical meaningfulness for individual patients
  • High rates of ARIA-E (35–43% at high dose, 65% in ApoE ε4 homozygotes) raise significant safety concerns and could lead to functional unblinding despite efforts to maintain blinding
  • The trial population lacked racial/ethnic diversity (≤1% Black/African American), limiting generalizability
  • CSF and tau PET biomarker substudies had small sample sizes from non-random subsets of participants
  • Low-dose arms were not statistically significant in either trial on any endpoint, weakening the dose-response argument for clinical outcomes despite biomarker dose-response
  • Increased lateral ventricular volume in all aducanumab groups relative to placebo raises questions about brain volume loss, though authors attribute this to non-neurodegenerative factors
  • The sponsor (Biogen) played a role in study design, conduct, data analysis, and manuscript preparation, introducing potential conflict of interest

Funding

Biogen. Biogen played a role in the design, conduct, data collection, analysis, interpretation, and manuscript preparation. Medical writing support provided by Meditech Media funded by Biogen.

Based on: EMERGE / ENGAGE (Journal of Prevention of Alzheimer's Disease (JPAD), 2022)

Authors: S. Budd Haeberlein, P.S. Aisen, F. Barkhof, ..., A. Sandrock

Citation: J Prev Alz Dis 2022;2(9):197-210

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