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A retrospective qualitative report of symptoms and safety from transcranial focused ultrasound for neuromodulation in humans

Wynn Legon, Sarah Adams, Priya Bansal, Parantap D. Patel, Landon Hobbs, Leo Ai, Jerel K. Mueller, Gregg Meekins, Bernadette T. Gillick

Scientific Reports 2020, 10 · 10.1038/s41598-020-62265-8

human healthyhealthyeeg megfmriemg mepbehaviourother

Abstract

Low intensity transcranial focused ultrasound (LIFU) is a promising method of non-invasive neuromodulation that uses mechanical energy to affect neuronal excitability. LIFU confers high spatial resolution and adjustable focal lengths for precise neuromodulation of discrete regions in the human brain. Before the full potential of low intensity ultrasound for research and clinical application can be investigated, data on the safety of this technique is indicated. Here, we provide an evaluation of the safety of LIFU for human neuromodulation through participant report and neurological assessment with a comparison of symptomology to other forms of non-invasive brain stimulation. Participants (N = 120) that were enrolled in one of seven human ultrasound neuromodulation studies in one laboratory at the University of Minnesota (2015-2017) were queried to complete a follow-up Participant Report of Symptoms questionnaire assessing their self-reported experience and tolerance to participation in LIFU research (I sppa 11.56-17.12 W/cm 2 ) and the perceived relation of symptoms to LIFU. A total of 64/120 participant (53%) responded to follow-up requests to complete the Participant Report of Symptoms questionnaire. None of the participants experienced serious adverse effects. From the post-hoc assessment of safety using the questionnaire, 7/64 reported mild to moderate symptoms, that were perceived as 'possibly' or 'probably' related to participation in LIFU experiments. These reports included neck pain, problems with attention, muscle twitches and anxiety. The most common unrelated symptoms included sleepiness and neck pain. There were initial transient reports of mild neck pain, scalp tingling and headache that were extinguished upon follow-up. No new symptoms were reported upon follow up out to 1 month. The profile and incidence of symptoms looks to be similar to other forms of non-invasive brain stimulation.

Abstract via europepmc.

Specieshuman
Subjects120 participants
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlinactive transducer, active control site
Auditory controlmatched device sound
Readout timingboth
Anaesthesianot applicable
Readoutseeg meg, fmri, emg mep, behaviour, otherParticipant Report of Symptoms questionnaire (safety/tolerability); single- and paired-pulse TMS motor evoked potentials (MEP, SICI/SICF); P14 somatosensory evoked potential; tactile discrimination task
Direction of effectinhibitoryAcross the seven underlying experiments summarized in Table 1, LIFU was associated with decreases: P14 SEP and alpha/beta/gamma EEG power down, tactile discrimination down, BOLD volume down, MEP amplitude down, and SICI/SICF down; this safety report itself does not re-analyze these effects but cites them as background for the seven studies surveyed.
Adverse eventsobserved7/64 reported mild to moderate symptoms perceived as 'possibly' or 'probably' related to LIFU (neck pain, difficulty paying attention, muscle twitches, anxiety); no participant rated any reported symptom as definitely related to the ultrasound intervention, and no serious adverse events occurred.

Exposures

Exposure 1: Thalamus LIFU (Experiments 1-2)

Target: thalamus — “Thalamus
Device: custom-built

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)0.36✓✓
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)36pulse duration × PRF gives 36%✓✓
Sonication duration (s)0.5✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)14.56✓✓
Free-field Ispta (W/cm²)5.24✓✓
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

Channel 1 (PRF) was a 5 Vp-p square wave burst of 1 kHz (N=500) resulting in a 0.5 second total sonication duration, gating a 500 kHz sine wave (channel 2). Experiment 1 used 300 stimulations with a 4 s inter-stimulus interval (ISI); experiment 2 used 90 stimulations with an 8 s ISI.

Exposure 2: Primary motor cortex (M1) LIFU (Experiments 3-7)

Target: primary motor cortex — “primary motor cortex
Device: custom-built

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)0.36✓✓
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)36pulse duration × PRF gives 36%✓✓
Sonication duration (s)0.5✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)11.56, 17.12swept✓✓
Free-field Ispta (W/cm²)4.16, 6.16swept✓✓
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

Same 500 kHz, 1 kHz PRF, 36% duty-cycle waveform as the thalamus experiments (0.5 s total sonication duration per stimulus). Number of stimulations and ISI varied by experiment: Exp.3, 200 stim/4 s ISI; Exp.4, 54 stim/5.5 s ISI; Exp.5, 80 stim/10 s ISI; Exp.6, 150 stim/10 s ISI; Exp.7, 44 stim/4.75 s ISI.

Flags from extraction

  • n_subjects120 participants were enrolled/exposed across the seven experiments, but only 64/120 (53%) completed the retrospective symptom questionnaire that is the basis of this paper's safety analysis.
  • auditory_controlSham and LIFU conditions were designed to produce the 'same audible sound' via identical transducer contact/buzzing, intended to mitigate indirect auditory activation; this does not map cleanly onto the closed auditory_control vocabulary (not masking noise, ramped pulses, or a dedicated sound-only sham), so 'other' was used.
  • direction_of_effectThis paper is a pooled safety/symptom report; the directionality noted here (mostly decreases) is drawn from Table 1's summary of the seven underlying, separately-published experiments rather than from new analysis in this paper.
  • exposures[0].in_situThe Discussion states that ultrasound intensity intracranially is estimated to be attenuated ~3-4 fold from free-water values, but gives no specific computed in-situ number for these experiments, so in_situ is left not_reported rather than computed.
  • exposures[0].device.manufacturerText describes the transducer only as 'custom-designed'; no manufacturer name is given for the specific units used (Table 3 lists geometry, not maker).