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NURTURE

Nusinersen initiated in infants during the presymptomatic stage of spinal muscular atrophy: Interim efficacy and safety results from the Phase 2 NURTURE study

Year of Publication: 2019

Authors: Darryl C De Vivo, Enrico Bertini, Kathryn J Swoboda, ..., Wildon Farwell; on behalf of the NURTURE Study Group

Journal: Neuromuscular Disorders

Citation: De Vivo DC, et al. Nusinersen initiated in infants during the presymptomatic stage of spinal muscular atrophy: Interim efficacy and safety results from the Phase 2 NURTURE study. Neuromuscul Disord. 2019;29(11):842-856.

Link: https://doi.org/10.1016/j.nmd.2019.09.007


Clinical Question

Can nusinersen, initiated intrathecally in presymptomatic infants with genetically confirmed 5q SMA (2 or 3 SMN2 copies) at age <=6 weeks, prevent or profoundly attenuate the severity of SMA -- including survival, respiratory, and motor outcomes -- compared with the expected natural history?

Bottom Line

Presymptomatic nusinersen in SMA infants with 2 or 3 SMN2 copies resulted in 100% survival without permanent ventilation and near-normal motor milestone achievement at median 2.9 years of follow-up, dramatically exceeding the expected natural history of SMA Types I and II and the outcomes of their untreated siblings, supporting immediate treatment after genetic diagnosis via newborn screening.

Major Points

  • NURTURE is a Phase 2, open-label, single-arm study; no control group was included given the expected fatal or severely disabling natural history of untreated 2- and 3-copy SMN2 SMA.
  • 25 infants enrolled (15 with 2 SMN2 copies, 10 with 3 SMN2 copies); median age at first dose 22 days (range 3-42 days).
  • Interim analysis data cutoff: March 29, 2019; median age at last visit 34.8 months (range 25.7-45.4 months); median follow-up 2.9 years.
  • Primary endpoint: all 25 participants alive; 0 required tracheostomy or permanent ventilation. Only 4/25 (16%, all 2-copy) used temporary respiratory support during acute reversible illness.
  • Motor milestones (WHO criteria): 25/25 (100%) achieved sitting without support; 23/25 (92%) achieved walking with assistance; 22/25 (88%) achieved independent walking -- outcomes inconsistent with expected SMA Type I or II natural history.
  • Most milestones achieved within the WHO normative developmental window: 84% sat without support, 65% walked with assistance, and 73% walked independently by the WHO 99th percentile age.
  • 3-copy participants performed better than 2-copy participants: all 10 (100%) with 3 SMN2 copies achieved independent walking vs. 12/15 (80%) with 2 SMN2 copies.
  • CHOP INTEND scores rose from a mean of 49.0 at baseline to approximately 62-63/64 at last visit for both subgroups. 10/15 (67%) 2-copy and 10/10 (100%) 3-copy participants achieved the maximum score of 64.
  • HINE-2 motor milestone total scores increased from a mean of 2.7-3.2 at baseline to 23.9-26.0 at last observed visit, approaching scale maximum.
  • Sibling comparison: NURTURE participants dramatically exceeded motor outcomes of untreated siblings with identical SMN2 copy numbers; 5/6 siblings (2-copy) with SMA required tracheostomy and/or died by 16 months -- vs. 0 NURTURE participants.
  • pNF-H levels were elevated at baseline in presymptomatic infants (even before symptom onset), significantly higher in 2-copy vs. 3-copy participants (plasma P=0.0050; CSF P=0.0020), declined rapidly with nusinersen loading, and lower Day 64 pNF-H levels predicted earlier achievement of independent walking (rs=0.64, P=0.0025).
  • CMAP amplitudes remained stable over time in both subgroups, contrasting with rapid deterioration in historical untreated SMA cohorts.
  • 8/25 (32%) infants had AEs considered possibly related to nusinersen; no AEs definitively related to study drug; no SAEs related to study drug; no new safety signals identified.
  • Key limitations: open-label, no sham control, small sample size, interim analysis of ongoing study, caregiver-reported milestone timing, variable baseline presentation, CHOP INTEND ceiling effect at 60-64 points.

Design

Study Type: Phase 2, open-label, single-arm, multinational, interventional trial (interim analysis)

Randomization:

Blinding: None (open-label)

Enrollment Period: May 2015 - February 2017

Follow-up Duration: Median 33.9 months (range 25.3-45.1 months) at interim data cutoff; ongoing 5-year treatment period

Centers: 15

Countries: USA, Italy, Taiwan, Germany, Australia, Turkey, Qatar

Sample Size: 25

Analysis: Intent-to-treat population (all infants receiving >=1 dose). Kaplan-Meier for time-to-event and milestone achievement. Descriptive statistics for CHOP INTEND, HINE-2, CMAP, pNF-H. Wilson score CI with continuity correction for proportion with clinically manifested SMA. Spearman correlation for predictors of motor function. SAS version 9.4.


Inclusion Criteria

  • Age <=6 weeks at first dose
  • Genetic documentation of 5q SMA (biallelic deletion or protein-disabling mutation of SMN1 gene)
  • 2 or 3 copies of the SMN2 gene
  • Baseline ulnar CMAP amplitude >=1 mV
  • Absence of hypoxemia
  • No clinical signs or symptoms suggestive of SMA at enrollment
  • On stable medications for >=1 month prior to baseline visit (if applicable)
  • Women of childbearing age required to agree to birth control from consent to 2 months after last dose

Exclusion Criteria

  • Prior medical condition that would prevent safe study participation (investigator judgment)
  • Participation in another interventional clinical study within 30 days prior to baseline
  • Concurrent enrollment in non-interventional research incompatible with NURTURE (investigator judgment)
  • Adverse reaction to nusinersen in a prior study contraindicating further treatment
  • Creatinine clearance <=30 mL/min
  • QTc >450 ms (males) or >480 ms (females)
  • Uncontrolled hypertension
  • History of active alcoholism or drug addiction in the year prior to screening
  • Clinically significant hypersensitivity or allergy to any study drug excipient
  • Study center or sponsor personnel or their immediate family

Arms

FieldNusinersen
InterventionIntrathecal nusinersen 12 mg administered by lumbar puncture: 4 loading doses on Days 1, 15, 29, and 64, followed by maintenance doses every 119 days over 5 years.
Duration5-year treatment period (ongoing at interim analysis; median 33.9 months at data cutoff)

Outcomes

OutcomeTypeControlInterventionHR / OR / RRP-value
Time to death or respiratory intervention (invasive or non-invasive ventilation for >=6 h/day continuously for >=7 days, or tracheostomy)Primary0/25 deaths; 0/25 required tracheostomy or permanent ventilation. 4/25 (16%, all 2-copy) required temporary respiratory support >=6 h/day for >=7 days during acute reversible illness.
WHO motor milestone - Sitting without supportSecondary25/25 (100%); median age 7.9 months (2-copy), 6.4 months (3-copy); 84% within WHO 99th percentile
WHO motor milestone - Walking with assistanceSecondary23/25 (92%); median age 16.1 months (2-copy), 9.6 months (3-copy)
WHO motor milestone - Walking aloneSecondary22/25 (88%); 12/15 (80%) 2-copy, 10/10 (100%) 3-copy; median age 20.4 months (2-copy), 12.3 months (3-copy)
CHOP INTEND total score at last visitSecondaryMean 62.1/64 (2-copy); mean 63.4/64 (3-copy). 67% 2-copy and 100% 3-copy achieved max score of 64.
HINE-2 total motor milestone scoreSecondaryMean increased from 2.7 to 23.9 (2-copy); from 3.2 to 26.0 (3-copy). Scale max = 26.
Plasma pNF-H change over timeSecondaryBaseline 20880.9 pg/mL (2-copy) vs 1870.7 pg/mL (3-copy). Declined rapidly during loading. Day 64 pNF-H predicted walking age (rs=0.64, P=0.0025).
Any AEAdverse25/25 (100%)
Serious AEAdverse12/25 (48%); no SAEs related to study drug
AE possibly related to drugAdverse8/25 (32%); none definitively related
AE related to lumbar punctureAdverse8/25 (32%); hemorrhages near thecal space in 4
Treatment discontinuationAdverse0/25 (0%)
PyrexiaAdverse21/25 (84%)
Upper respiratory infectionAdverse19/25 (76%)
PneumoniaAdverse6/25 (24%); all 2-copy
TremorAdverse7/25 (28%); all 2-copy

Subgroup Analysis

3 SMN2 copies had uniformly better outcomes than 2 copies. Baseline pNF-H was the strongest predictor of HINE-2 at Day 302 (rs=-0.53, P=0.0120) and walking age (rs=0.55, P=0.0147). In 2-copy, Day 64 weight-for-age (rs=0.72, P=0.0027) and CMAP (rs=0.66, P=0.0098) also correlated with HINE-2.


Criticisms

  • Open-label design with no sham or placebo control group
  • Small sample size (n=25); interim analysis of ongoing study
  • Caregiver-reported milestone timing may introduce variability
  • No formal prospective assessments of siblings with SMA
  • CHOP INTEND ceiling effect at ~60/64
  • HINE-2 only assessed until Day 778
  • Variable baseline clinical presentation despite all meeting presymptomatic criteria
  • Cross-study comparisons with ENDEAR/CHERISH limited by population differences
  • Funded by Biogen; several co-authors are Biogen employees
  • Long-term durability through childhood/adolescence remains to be determined

Funding

Biogen (Cambridge, MA, USA); medical writing support funded by Biogen.

Based on: NURTURE (Neuromuscular Disorders, 2019)

Authors: Darryl C De Vivo, Enrico Bertini, Kathryn J Swoboda, ..., Wildon Farwell; on behalf of the NURTURE Study Group

Citation: De Vivo DC, et al. Nusinersen initiated in infants during the presymptomatic stage of spinal muscular atrophy: Interim efficacy and safety results from the Phase 2 NURTURE study. Neuromuscul Disord. 2019;29(11):842-856.

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