A retrospective qualitative report of symptoms and safety from transcranial focused ultrasound for neuromodulation in humans.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
27 03 2020
27 03 2020
Historique:
received:
09
12
2019
accepted:
04
03
2020
entrez:
30
3
2020
pubmed:
30
3
2020
medline:
1
12
2020
Statut:
epublish
Résumé
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
Identifiants
pubmed: 32221350
doi: 10.1038/s41598-020-62265-8
pii: 10.1038/s41598-020-62265-8
pmc: PMC7101402
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5573Références
Tufail, Y. et al. Transcranial pulsed ultrasound stimulates intact brain circuits. Neuron 66, 681–694 (2010).
doi: 10.1016/j.neuron.2010.05.008
pubmed: 20547127
Mehic, E. et al. Increased anatomical specificity of neuromodulation via modulated focused ultrasound. PLoS One 9, e86939 (2014).
doi: 10.1371/journal.pone.0086939
pubmed: 24504255
pmcid: 3913583
King, R. L., Brown, J. R., Newsome, W. T. & Pauly, K. B. Effective parameters for ultrasound-induced in vivo neurostimulation. Ultrasound Med. Biol. 39, 312–331 (2013).
doi: 10.1016/j.ultrasmedbio.2012.09.009
pubmed: 23219040
Kim, H., Chiu, A., Lee, S. D., Fischer, K. & Yoo, S. S. Focused ultrasound-mediated non-invasive brain stimulation: examination of sonication parameters. Brain Stimul. 7, 748–756 (2014).
doi: 10.1016/j.brs.2014.06.011
pubmed: 25088462
pmcid: 4167941
Min, B. K. et al. Focused ultrasound-mediated suppression of chemically-induced acute epileptic EEG activity. BMC Neurosci. 12, 23-2202–12-23 (2011).
doi: 10.1186/1471-2202-12-23
Younan, Y. et al. Influence of the pressure field distribution in transcranial ultrasonic neurostimulation. Med. Phys. 40, 082902 (2013).
doi: 10.1118/1.4812423
pubmed: 23927357
Yang, P. S. et al. Transcranial focused ultrasound to the thalamus is associated with reduced extracellular GABA levels in rats. Neuropsychobiology 65, 153–160 (2012).
doi: 10.1159/000336001
pubmed: 22378299
Yoo, S. S. et al. Focused ultrasound modulates region-specific brain activity. Neuroimage 56, 1267–1275 (2011).
doi: 10.1016/j.neuroimage.2011.02.058
pubmed: 21354315
pmcid: 3342684
Lee, W. et al. Image-Guided Focused Ultrasound-Mediated Regional Brain Stimulation in Sheep. Ultrasound Med. Biol. 42, 459–470 (2016).
doi: 10.1016/j.ultrasmedbio.2015.10.001
pubmed: 26525652
Yoon, K. et al. Effects of sonication parameters on transcranial focused ultrasound brain stimulation in an ovine model. PLoS One 14, e0224311 (2019).
doi: 10.1371/journal.pone.0224311
pubmed: 31648261
pmcid: 6812789
Dallapiazza, R. F. et al. Noninvasive neuromodulation and thalamic mapping with low-intensity focused ultrasound. J. Neurosurg., 1–10 (2017).
Folloni, D. et al. Manipulation of Subcortical and Deep Cortical Activity in the Primate Brain Using Transcranial Focused Ultrasound Stimulation. Neuron 101, 1109–1116.e5 (2019).
doi: 10.1016/j.neuron.2019.01.019
pubmed: 30765166
pmcid: 6520498
Verhagen, L. et al. Offline impact of transcranial focused ultrasound on cortical activation in primates. Elife 8, https://doi.org/10.7554/eLife.40541 (2019).
Deffieux, T. et al. Low-intensity focused ultrasound modulates monkey visuomotor behavior. Curr. Biol. 23, 2430–2433 (2013).
doi: 10.1016/j.cub.2013.10.029
pubmed: 24239121
Wattiez, N. et al. Transcranial ultrasonic stimulation modulates single-neuron discharge in macaques performing an antisaccade task. Brain Stimul. 10, 1024–1031 (2017).
doi: 10.1016/j.brs.2017.07.007
pubmed: 28789857
Legon, W. et al. Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans. Nat. Neurosci. 17, 322–329 (2014).
doi: 10.1038/nn.3620
pubmed: 24413698
Legon, W., Ai, L., Bansal, P. & Mueller, J. K. Neuromodulation with single-element transcranial focused ultrasound in human thalamus. Hum. Brain Mapp. 39, 1995–2006 (2018).
doi: 10.1002/hbm.23981
pubmed: 29380485
Hameroff, S. et al. Transcranial ultrasound (TUS) effects on mental states: a pilot study. Brain Stimul. 6, 409–415 (2013).
doi: 10.1016/j.brs.2012.05.002
pubmed: 22664271
Lee, W. et al. Image-guided transcranial focused ultrasound stimulates human primary somatosensory cortex. Sci. Rep. 5, 8743 (2015).
doi: 10.1038/srep08743
pubmed: 25735418
pmcid: 4348665
Lee, W., Chung, Y. A., Jung, Y., Song, I. U. & Yoo, S. S. Simultaneous acoustic stimulation of human primary and secondary somatosensory cortices using transcranial focused ultrasound. BMC Neurosci. 17, 68 (2016).
doi: 10.1186/s12868-016-0303-6
pubmed: 27784293
pmcid: 5081675
Legon, W., Bansal, P., Tyshynsky, R., Ai, L. & Mueller, J. K. Transcranial focused ultrasound neuromodulation of the human primary motor cortex. Sci. Rep. 8, 10007-018–28320-1 (2018).
doi: 10.1038/s41598-018-28320-1
Lee, W. et al. Transcranial focused ultrasound stimulation of human primary visual cortex. Sci. Rep. 6, 34026 (2016).
doi: 10.1038/srep34026
pubmed: 27658372
pmcid: 5034307
Monti, M. M., Schnakers, C., Korb, A. S., Bystritsky, A. & Vespa, P. M. Non-Invasive Ultrasonic Thalamic Stimulation in Disorders of Consciousness after Severe Brain Injury: A First-in-Man Report. Brain Stimul. 9, 940–941 (2016).
doi: 10.1016/j.brs.2016.07.008
pubmed: 27567470
Mueller, J., Legon, W., Opitz, A., Sato, T. F. & Tyler, W. J. Transcranial focused ultrasound modulates intrinsic and evoked EEG dynamics. Brain Stimul. 7, 900–908 (2014).
doi: 10.1016/j.brs.2014.08.008
pubmed: 25265863
Ai, L., Mueller, J. K., Bansal, P. & Legon, W. Transcranial focused ultrasound for BOLD fMRI signal modulation in humans. EMBC, 1758–1761 (2016).
Ai, L., Bansal, P., Mueller, J. K. & Legon, W. Effects of transcranial focused ultrasound on human primary motor cortex using 7T fMRI: a pilot study. BMC Neurosci. 19, 56-018–0456-6 (2018).
doi: 10.1186/s12868-018-0456-6
White, P. J., Clement, G. T. & Hynynen, K. Longitudinal and shear mode ultrasound propagation in human skull bone. Ultrasound Med. Biol. 32, 1085–1096 (2006).
doi: 10.1016/j.ultrasmedbio.2006.03.015
pubmed: 16829322
pmcid: 1560344
Plaksin, M., Kimmel, E. & Shoham, S. Cell-Type-Selective Effects of Intramembrane Cavitation as a Unifying Theoretical Framework for Ultrasonic Neuromodulation. eNeuro 3, https://doi.org/10.1523/ENEURO.0136-15.2016. eCollection 2016 May-Jun (2016).
Krasovitski, B., Frenkel, V., Shoham, S. & Kimmel, E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc. Natl. Acad. Sci. USA 108, 3258–3263 (2011).
doi: 10.1073/pnas.1015771108
pubmed: 21300891
Tyler, W. J. Noninvasive neuromodulation with ultrasound? A continuum mechanics hypothesis. Neuroscientist 17, 25–36 (2011).
doi: 10.1177/1073858409348066
pubmed: 20103504
Tyler, W. J. The mechanobiology of brain function. Nat. Rev. Neurosci. 13, 867–878 (2012).
doi: 10.1038/nrn3383
pubmed: 23165263
Mueller, J. K., Ai, L., Bansal, P. & Legon, W. Computational exploration of wave propagation and heating from transcranial focused ultrasound for neuromodulation. J. Neural Eng. 13, 056002–2560/13/5/056002. Epub 2016 Jul 28 (2016).
Elias, W. J. et al. A pilot study of focused ultrasound thalamotomy for essential tremor. N. Engl. J. Med. 369, 640–648 (2013).
doi: 10.1056/NEJMoa1300962
pubmed: 23944301
Lipsman, N. et al. MR-guided focused ultrasound thalamotomy for essential tremor: a proof-of-concept study. Lancet Neurol. 12, 462–468 (2013).
doi: 10.1016/S1474-4422(13)70048-6
pubmed: 23523144
Downs, M. E. et al. Long-Term Safety of Repeated Blood-Brain Barrier Opening via Focused Ultrasound with Microbubbles in Non-Human Primates Performing a Cognitive Task. PLoS One 10, e0125911 (2015).
doi: 10.1371/journal.pone.0125911
pubmed: 25945493
pmcid: 4422704
McDannold, N., Vykhodtseva, N. & Hynynen, K. Targeted disruption of the blood-brain barrier with focused ultrasound: association with cavitation activity. Phys. Med. Biol. 51, 793–807 (2006).
doi: 10.1088/0031-9155/51/4/003
pubmed: 16467579
http://www.fda.gov/downloads/MedicalDevices/DeviceRegulationandGuidance/GuidanceDocuments/UCM070911.pdf .
Duck, F. A. Medical and non-medical protection standards for ultrasound and infrasound. Prog. Biophys. Mol. Biol. 93, 176–191 (2007).
doi: 10.1016/j.pbiomolbio.2006.07.008
pubmed: 16965806
Shaw, A., ter Haar, G., Haller, J. & Wilkens, V. Towards a dosimetric framework for therapeutic ultrasound. Int. J. Hyperthermia 31, 182–192 (2015).
doi: 10.3109/02656736.2014.997311
pubmed: 25774889
O’Brien, W. D. Jr. Ultrasound-biophysics mechanisms. Prog. Biophys. Mol. Biol. 93, 212–255 (2007).
doi: 10.1016/j.pbiomolbio.2006.07.010
pubmed: 16934858
Mesiwala, A. H. et al. High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo. Ultrasound Med. Biol. 28, 389–400 (2002).
doi: 10.1016/S0301-5629(01)00521-X
pubmed: 11978420
Vykhodtseva, N. I., Hynynen, K. & Damianou, C. Histologic effects of high intensity pulsed ultrasound exposure with subharmonic emission in rabbit brain in vivo. Ultrasound Med. Biol. 21, 969–979 (1995).
doi: 10.1016/0301-5629(95)00038-S
pubmed: 7491751
Dunn, F. & Fry, F. J. Ultrasonic threshold dosages for the mammalian central nervous system. IEEE Trans. Biomed. Eng. 18, 253–256 (1971).
doi: 10.1109/TBME.1971.4502847
pubmed: 4997992
Ulrich, W. D. Ultrasound dosage for nontherapeutic use on human beings–extrapolations from a literature survey. IEEE Trans. Biomed. Eng. 21, 48–51 (1974).
doi: 10.1109/TBME.1974.324362
pubmed: 4813876
Gillick, B. et al. Transcranial direct current stimulation and constraint-induced therapy in cerebral palsy: A randomized, blinded, sham-controlled clinical trial. Eur. J. Paediatr. Neurol. (2018).
Gillick, B. T. et al. Non-Invasive Brain Stimulation in Children With Unilateral Cerebral Palsy: A Protocol and Risk Mitigation Guide. Frontiers in pediatrics March (2018).
Deng, Z. D., Lisanby, S. H. & Peterchev, A. V. Coil design considerations for deep transcranial magnetic stimulation. Clin. Neurophysiol. 125, 1202–1212 (2014).
doi: 10.1016/j.clinph.2013.11.038
pubmed: 24411523
Levkovitz, Y. et al. A randomized controlled feasibility and safety study of deep transcranial magnetic stimulation. Clinical Neurophysiology 118, 2730–2744 (2007).
doi: 10.1016/j.clinph.2007.09.061
pubmed: 17977787
Lenoir, C. et al. Report of one confirmed generalized seizure and one suspected partial seizure induced by deep continuous theta burst stimulation of the right operculo-insular cortex. 11, 1187 (2018).
Mueller, J. K., Ai, L., Bansal, P. & Legon, W. Numerical evaluation of the skull for human neuromodulation with transcranial focused ultrasound. J. Neural Eng., https://doi.org/10.1088/1741-2552/aa843e (2017).
Karshafian, R., Bevan, P. D., Williams, R., Samac, S. & Burns, P. N. Sonoporation by ultrasound-activated microbubble contrast agents: effect of acoustic exposure parameters on cell membrane permeability and cell viability. Ultrasound Med. Biol. 35, 847–860 (2009).
doi: 10.1016/j.ultrasmedbio.2008.10.013
pubmed: 19110370
Rossi, S., Hallett, M., Rossini, P. M. & Pascual-Leone, A., Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120, 2008–2039 (2009).
doi: 10.1016/j.clinph.2009.08.016
pubmed: 19833552
pmcid: 3260536
Sato, T., Shapiro, M. G. & Tsao, D. Y. Ultrasonic neuromodulation in vivo: discovery of a somato-auditory artifact and its implications. 808.1 (2017).
Guo, H. et al. Ultrasound produces extensive brain activation via a cochlear pathway. Neuron 98, 1020–1030. e4 (2018).
doi: 10.1016/j.neuron.2018.04.036
pubmed: 29804919