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TRIVASOSTIM

Evaluation of External Trigeminal Nerve Stimulation to Prevent Cerebral Vasospasm after Subarachnoid Hemorrhage Due to Aneurysmal Rupture: A Randomized, Double-Blind Proof-of-Concept Pilot Trial (TRIVASOSTIM Study)

Year of Publication: 2023

Authors: Philippe Rigoard, Maxime Billot, Maarten Moens, ..., Konstantin V. Slavin

Journal: International Journal of Environmental Research and Public Health

Citation: Int. J. Environ. Res. Public Health 2023, 20, 5836

Link: https://doi.org/10.3390/ijerph20105836


Clinical Question

Does external transcutaneous trigeminal nerve stimulation (TNS) decrease the incidence of cerebral infarction related to vasospasm in patients with aneurysmal subarachnoid hemorrhage compared to sham stimulation when assessed by MRI at 3 months?

Bottom Line

In this single-center, double-blind, randomized pilot trial of 60 patients with aneurysmal SAH, 10 days of transcutaneous trigeminal nerve stimulation did not significantly reduce the rate of vasospasm-related cerebral infarction at 3 months compared to sham stimulation (23% vs 27%, p=0.99). No significant differences were observed in functional outcomes or quality of life at 6 months. Two deaths occurred in the TNS group (2/30, 7%) versus none in the sham group; both were reported as severe adverse events considered unrelated to the intervention (no formal p-value reported for mortality). While the pathophysiological rationale based on animal studies and the trigeminovascular system's role in cerebral blood flow regulation was compelling, this proof-of-concept pilot trial was unable to demonstrate that TNS can decrease cerebral infarction secondary to vasospasm. The negative results may be attributed to maintaining stimulation intensity below the paresthesia threshold to preserve double-blinding, potentially underestimating a dose-effect relationship. It would be premature to promote trigeminal system neurostimulation in this context, and further research is needed before clinical application can be recommended.

Major Points

  • Single-center, double-blind, randomized controlled pilot trial with 1:1 randomization
  • 60 patients with aneurysmal SAH enrolled from single French institution (Poitiers University Hospital)
  • 60 patients assessed for eligibility and randomized (30 TNS, 30 sham); all 60 analyzed on intention-to-treat basis; 8 patients left the study during follow-up including 2 unrelated deaths in TNS group
  • Inclusion criteria: age 18-75 years, aSAH within 48 hours, WFNS grade I-IV, ruptured aneurysm confirmed by CTA/angiography, candidate for endovascular occlusion or microsurgical exclusion
  • 30 patients randomized to active TNS, 30 to sham stimulation
  • Intervention: bilateral transcutaneous electrical stimulation of supratrochlear and supraorbital nerves (ophthalmic division of trigeminal nerve)
  • Stimulation parameters: 20 Hz frequency, intensity adjusted to sub-paresthesia threshold to maintain blinding
  • Non-sedated patients: mean intensity 9.6±2.7 mA (TNS) vs 11.4±1.5 mA (sham), p=0.16
  • Sedated patients: mean intensity 4.9±2.9 mA (TNS) vs 4.3±2.2 mA (sham), p=0.49
  • Treatment duration: 10 days continuous stimulation (days 1-10 after SAH), mean 9.5 days TNS vs 9.9 days sham (p=0.2)
  • Primary endpoint: cerebral infarction on MRI FLAIR at 3 months (or last CT/MRI before death)
  • Primary outcome negative: 23% (7/30) TNS vs 27% (8/30) sham, p=0.99
  • Late infarction (not observed at D6): 10% (3/30) TNS vs 20% (6/30) sham, p=0.47
  • Modified Rankin Scale ≥3 at 6 months: 10% TNS vs 3% sham, p=0.65
  • Glasgow Outcome Scale moderate disability at 6 months: 18% TNS vs 27% sham, p=0.53
  • EQ5D-3L quality of life index at 6 months: 0.79±0.23 TNS vs 0.79±0.22 sham, p=0.99
  • Mortality at 6 months: 2/30 (7%) TNS vs 0/30 sham; both TNS deaths reported as severe adverse events unrelated to the intervention; no p-value reported
  • Perfusion CT abnormality at D6: 40% (12/30) TNS vs 17% (5/30) sham, p=0.084 (trend but not significant)
  • Vasospasm on CT angiography at D6: 47% (14/30) TNS vs 33% (10/30) sham, p=0.43
  • Moderate-severe vasospasm: TNS 43% (13/30) vs sham 27% (8/30)
  • 50% (7/14) of TNS patients and 80% (8/10) of sham patients with vasospasm were asymptomatic
  • No significant difference in secondary complications during hospitalization (37% TNS vs 33% sham, p=0.99); serious adverse events not separately quantified — only the two TNS deaths were reported as severe adverse events
  • Hydrocephalus occurred in 33% TNS vs 30% sham patients during hospitalization (no separate p-value reported for this subrow)
  • Strong correlation found between vasospasm severity and PCT abnormalities (p<0.0001)
  • 100% of severe vasospasm patients had PCT abnormalities, 53.8% of moderate vasospasm, 5.1% of no/mild vasospasm
  • Significant relationship between WFNS grade and vasospasm occurrence (p=0.016)
  • Study hypothesis based on trigeminovascular system pathophysiology and vasodilator peptide (CGRP) release
  • Stimulation maintained below paresthesia threshold to preserve double-blinding may have limited efficacy

Design

Study Type: Single-center, randomized, double-blind, placebo-controlled, parallel-group, proof-of-concept pilot trial

Randomization: 1

Blinding: Double-blind. Randomization performed using a predefined list from the study methodologist provided to the clinical trial personnel of Poitiers University Hospital, with 1:1 allocation. Both patients and evaluators were blinded to allocation. Sham device identical in appearance to active device and displayed current intensity but delivered no electrical stimulation. Stimulation intensity was kept below the paresthesia threshold (determined with a separate reference TENS device before the blinded device was applied) so neither patient nor clinician could perceive whether stimulation was active

Follow-up Duration: 6 months

Centers: 1

Countries: France

Sample Size: 60

Analysis: Intention-to-treat (ITT) analysis on all 60 randomized patients; 8 patients left the study during follow-up (including 2 deaths unrelated to intervention) but all were analyzed on ITT basis. Sample size: minimum 30 patients per group (60 total) to detect a 30% estimated difference (65% vs 35%) with 80% power using one-tailed Fisher test at 5% risk. Primary endpoint compared using Fisher's exact test. Quantitative outcomes compared using Student's t-test after Shapiro-Wilk normality testing, or Wilcoxon-Mann-Whitney test if non-normal. Qualitative outcomes analyzed using chi-squared or Fisher's exact test. All tests performed at α=5%. No missing data reported for the primary endpoint; secondary endpoints analyzed on available cases without imputation. All analyses performed using SAS software version 9.4


Inclusion Criteria

  • Age 18-75 years
  • Admitted within 48 hours after onset of SAH
  • Ruptured cerebral aneurysm confirmed by CTA or cerebral angiography
  • No progressive psychosis or serious psychotic history requiring hospitalization
  • No progressive cancerous pathology
  • Candidate for aneurysm management by endovascular occlusion or microsurgical exclusion
  • WFNS grade I-IV (1-4)
  • Affiliated with health insurance plan
  • Patient or trusted person able to understand and accept study constraints
  • Written informed consent from patient or legally authorized representative

Exclusion Criteria

  • Receiving reinforced protection (minors, pregnant/breastfeeding women, persons deprived of liberty, persons in health/social institutions, adults under legal protection)
  • Proven dementia or neurological/psychiatric history affecting cognitive or motor skills
  • Clinical severity WFNS grade V (very high mortality risk)
  • Intracerebral or intraventricular hemorrhage without subarachnoid component
  • SAH without evidence of aneurysm
  • Unruptured brain aneurysm
  • Contraindication for TENS device placement (electronic pacemaker)
  • Dermatological problems in stimulation area contraindicating TENS patches

Baseline Characteristics

CharacteristicTNS GroupSham Group
Number3030
Mean age (range), years55.3 ± 9.3 (36-73)59.6 ± 11.5 (27-79)
Female22 (73%)17 (57%)
Male8 (27%)13 (43%)
Height, m165.4 ± 9.5 (145-180)168.8 ± 7.7 (153-185)
Weight, kg72.0 ± 19.8 (45-130)68.8 ± 11.8 (46-92)
BMI, kg/m²26.1 ± 5.9 (18.4-45.0)24.2 ± 4.0 (18.1-36.9)
Median admission time, hours6 (1-32)7 (1-25)
Alcohol abuse5 (17%)4 (13%)
Smoking18 (60%)13 (43%)
Hypertension8 (27%)11 (37%)
WFNS grade at admission - I14 (47%)16 (54%)
WFNS grade at admission - II7 (23%)9 (30%)
WFNS grade at admission - III01 (3%)
WFNS grade at admission - IV9 (30%)4 (13%)
Fisher Grade 11 (3%)0
Fisher Grade 24 (13%)2 (7%)
Fisher Grade 36 (20%)6 (20%)
Fisher Grade 419 (63%)22 (73%)
Hydrocephalus8 (27%)9 (30%)
Aneurysm treated with surgery2 (7%)3 (10%)
Aneurysm treated with coiling28 (93%)27 (90%)
Complete aneurysm obliteration24 (80%)22 (73%)

Arms

FieldTrigeminal Nerve Stimulation (TNS)Control
InterventionBilateral transcutaneous electrical nerve stimulation applied to the innervation territory of the supratrochlear and supraorbital nerves (terminal branches of ophthalmic division V1 of trigeminal nerve). Stimulation frequency 20 Hz. Intensity adjusted to sub-paresthesia threshold for non-sedated patients (determined using a regular TENS device before the blinded device was applied). For sedated patients, intensity maintained at 20 mA unless scheduled to stop sedation before day 10, in which case lower thresholds were used to maintain blinding after awakening. Continuous stimulation 24 hours per day for 10 days (days 1-10 after SAH). Electrodes positioned bilaterally over the supraorbital area. Both TNS and sham groups received standardized and comparable aneurysmal SAH treatment. Perfusion CT scan (PCT) performed at day 6 (D6); MRI with FLAIR at month 3 (M3 ± 3 weeks); clinical evaluation at month 6 (M6 ± 4 weeks). Daily clinical surveillance with Glasgow Coma Scale; additional CT scans when clinically indicated.Identical bilateral electrode placement over the supratrochlear and supraorbital nerve territories. Sham device identical in appearance to the active TNS device and displayed current intensity but delivered no electrical stimulation. Same intensity determination protocol used to maintain blinding. Applied continuously 24 hours per day for 10 days (days 1-10 after SAH). Both TNS and sham groups received standardized and comparable aneurysmal SAH treatment. Same imaging and follow-up schedule as TNS group: perfusion CT scan (PCT) at day 6, MRI with FLAIR at month 3 (M3 ± 3 weeks), clinical evaluation at month 6 (M6 ± 4 weeks).
Duration10 days continuous stimulation, 6 months total follow-up10 days sham stimulation, 6 months total follow-up

Outcomes

OutcomeTypeControlInterventionHR / OR / RRP-value
Presence of cerebral infarction related to vasospasm on MRI FLAIR at 3 months (or on last CT/MRI scan before death), after exclusion of infarcts from other causes (procedure-related, hematoma-related) as primary or relevant cause, or considered not exclusively due to causes other than vasospasm. Both patients and evaluators were blinded to allocation.Primary27% (8/30), 95% CI not reported23% (7/30), 95% CI not reported3.33%0.99 (Fisher's exact test)
Late cerebral infarction (not observed at day 6 but present at 3 months)Secondary20% (6/30)10% (3/30)0.47
Modified Rankin Scale (MRS) ≥3 at 6 months (unfavorable outcome)Secondary3% (1/30) - one patient with MRS 310% (3/30) - one patient MRS 3, two patients deceased (MRS 6)0.65
Glasgow Outcome Scale (GOS) - moderate disability (GOS II) at 6 monthsSecondary27% (8/30)18% (5/28)0.53
EQ5D-3L Index (quality of life) at 6 monthsSecondaryMean 0.79 ± 0.22 [0.27-1.00] (n=30)Mean 0.79 ± 0.23 [0.25-1.00] (n=28)0.99
EQ5D Visual Analog Scale at 6 monthsSecondaryMean 86 ± 11 [65-100] (n=30)Mean 82 ± 12 [50-100] (n=28)0.26
Mortality at 6 monthsSecondary0% (0/30)7% (2/30) - both deaths reported as severe adverse events unrelated to the interventionNot reported
Perfusion abnormality on CT perfusion at day 6Secondary17% (5/30)40% (12/30)0.084 (trend but not significant)
Vasospasm presence on CT angiography at day 6Secondary33% (10/30)47% (14/30)0.43
Moderate-severe vasospasm (26-100% arterial diameter reduction)Secondary27% (8/30) moderate-severe combined43% (13/30) moderate-severe combinedNot separately reported
Symptomatic vasospasm (of vasospasm-positive patients, per Table 5)Secondary20% (2/10 with vasospasm)50% (7/14 with vasospasm)Not reported
Infarct-related hypodensity on head CT at day 6Secondary13% (4/30)10% (3/30)0.99
Hydrocephalus requiring cerebrospinal fluid drainage (at D6)Secondary27% (8/30)27% (8/30)0.99
Secondary complications during hospitalizationAdverse33% (10/30)37% (11/30)0.99
Hydrocephalus during hospitalizationAdverse30% (9/30)33% (10/30)Not separately reported (overall secondary-complications p=0.99)
Serious adverse eventsAdverseNot reported2 deaths reported as severe adverse events unrelated to the study (hemorrhagic stroke at 119 days; postoperative empyema at 70 days)Not reported
Deaths during study (unrelated to intervention)Adverse02 (1 from hemorrhagic stroke at 119 days, 1 from postoperative empyema at 70 days)Not reported

Subgroup Analysis

Strong correlation between vasospasm severity and PCT abnormalities: no/mild vasospasm 5.1% (2/39) had PCT abnormality, moderate vasospasm 53.8% (7/13) had PCT abnormality, severe vasospasm 100% (8/8) had PCT abnormality (p<0.0001). Significant relationship between WFNS grade and vasospasm occurrence (p=0.016): WFNS grade 4 patients had highest vasospasm rate (10/14, 71% of grade 4 patients with vasospasm)


Criticisms

  • Single-center study limits generalizability
  • Small sample size (60 patients) - pilot study not powered for definitive efficacy conclusions
  • One patient (79 years old) exceeded age inclusion criterion of 75 years (protocol deviation)
  • Primary endpoint based solely on radiological criteria (MRI FLAIR at 3 months), not clinical examination
  • TNS intensity maintained below paresthesia threshold to preserve blinding may have limited therapeutic effect - potential dose-effect relationship underestimated
  • Stimulation parameters (frequency 20 Hz, intensity) chosen empirically based on previous works without dose-optimization studies
  • No assessment of whether effective dose reached target - no measurement of CGRP levels or other mechanistic biomarkers
  • Sex imbalance despite randomization (males 27% TNS vs 43% sham, p=0.18) — not statistically significant but potential confounder
  • CT perfusion performed only once at day 6 - single timepoint assessment
  • Unexpectedly high perfusion abnormalities in TNS group (40% vs 17%, p=0.084) raises questions about potential adverse effects
  • External TENS targets peripheral nervous system through autonomic ganglia, may not adequately reach central trigemino-cervical complex compared to direct neuraxis stimulation
  • 57.1% of patients with moderate-severe vasospasm were asymptomatic - disconnect between radiological and clinical vasospasm
  • Only radiological definition of DCI used, which may underestimate clinical impact
  • No stratification for baseline characteristics in randomization
  • Follow-up limited to 6 months - longer-term outcomes unknown
  • Two deaths in TNS group (none in sham) though reported as unrelated to intervention raises safety questions and no formal p-value was provided for mortality
  • Lower DCI incidence than predicted (23-27% vs expected 50-70%) may indicate early screening effect
  • Pathophysiological mechanism assumes vasodilation via neuropeptide release, but DCI pathophysiology involves multiple factors beyond vessel caliber
  • No measurement of cerebral autoregulation which may be impaired during vasospasm
  • Distinction between clinical and radiological vasospasm difficult - complex neurological symptoms hard to attribute solely to vasospasm
  • Almost half of severe vasospasm patients did not develop DCI - other factors involved beyond vessel narrowing
  • Internal inconsistency in paper: Table 5 reports 7 (50%) symptomatic vasospasm in TNS and 2 (20%) in sham, whereas Section 3.5 text states 2 (7%) TNS and 3 (10%) sham

Funding

No external funding. Study conducted at Poitiers University Hospital. Approved by the French Agency for the Safety of Health Products (ANSM) number 2016-A01144-47 and Ethics Committee CPP West III. Registered at ClinicalTrials.gov (NCT02482883) on 26 June 2015

Based on: TRIVASOSTIM (International Journal of Environmental Research and Public Health, 2023)

Authors: Philippe Rigoard, Maxime Billot, Maarten Moens, ..., Konstantin V. Slavin

Citation: Int. J. Environ. Res. Public Health 2023, 20, 5836

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