Transcranial Direct Current Stimulation (tDCS) in Unilateral Cerebral Palsy: A Pilot Study of Motor Effect

Emanuela Inguaggiato, Nadia Bolognini, Simona Fiori, Giovanni Cioni, Emanuela Inguaggiato, Nadia Bolognini, Simona Fiori, Giovanni Cioni

Abstract

Transcranial Direct Current Stimulation (tDCS) is an emerging tool to improve upper limb motor functions after stroke acquired in adulthood; however, there is a paucity of reports on its efficacy for upper limb motor rehabilitation in congenital or early-acquired stroke. In this pilot study we have explored, for the first time, the immediate effects, and their short-term persistence, of a single application of anodal tDCS on chronic upper limb motor disorders in children and young individuals with Unilateral Cerebral Palsy (UCP). To this aim, in a crossover sham-controlled study, eight subjects aged 10-28 years with UCP underwent two sessions of active and sham tDCS. Anodal tDCS (1.5 mA, 20 min) was delivered over the primary motor cortex (M1) of the ipsilesional hemisphere. Results showed, only following the active stimulation, an immediate improvement in unimanual gross motor dexterity of hemiplegic, but not of nonhemiplegic, hand in Box and Block test (BBT). Such improvement remained stable for at least 90 minutes. Performance of both hands in Hand Grip Strength test was not modified by anodal tDCS. Improvement in BBT was unrelated to participants' age or lesion size, as revealed by MRI data analysis. No serious adverse effects occurred after tDCS; some mild and transient side effects (e.g., headache, tingling, and itchiness) were reported in a limited number of cases. This study provides an innovative contribution to scientific literature on the efficacy and safety of anodal tDCS in UCP. This trial is registered with NCT03137940.

Figures

Figure 1
Figure 1
CONSORT diagram and study flow.
Figure 2
Figure 2
BBT scores (i.e., number of blocks moved in 1 min) for the hemiplegic and nonhemiplegic hands, at each assessment of the active anodal tDCS and sham tDCS sessions. T0 = baseline; T1 = immediately after the end of tDCS; T2 = 90 min after the stimulation session. ∗ = significant change from baseline, p < 0.05.
Figure 3
Figure 3
HGS scores (i.e., mean voluntary isometric strength, in kg) for the hemiplegic and nonhemiplegic hands, at each assessment of the real anodal tDCS and sham tDCS sessions. T0 = baseline; T1 = immediately after the end of tDCS; T2 = 90 min after the stimulation session.

References

    1. Ferrari A., Cioni G., Cioni G., et al. The Spastic Forms of Cerebral Palsy. Milan: Springer; 2010. Forms of hemiplegia; pp. 331–356.
    1. Rich T. L., Menk J. S., Rudser K. D., Feyma T., Gillick B. T. Less-affected hand function in children with hemiparetic unilateral cerebral palsy: a comparison study with typically developing peers. Neurorehabilitation and Neural Repair. 2017;31(10-11):965–976. doi: 10.1177/1545968317739997.
    1. Woods A. J., Antal A., Bikson M., et al. A technical guide to tDCS, and related non-invasive brain stimulation tools. Clinical Neurophysiology. 2016;127(2):1031–1048. doi: 10.1016/j.clinph.2015.11.012.
    1. Fregni F., Nitsche M. A., Loo C. K., et al. Regulatory considerations for the clinical and research use of transcranial direct current stimulation (tDCS): review and recommendations from an expert panel. Clinical Research and Regulatory Affairs. 2015;32(1):22–35. doi: 10.3109/10601333.2015.980944.
    1. Brunoni A. R., Nitsche M. A., Bolognini N., et al. Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimulation. 2012;5(3):175–195. doi: 10.1016/j.brs.2011.03.002.
    1. Stagg C. J., Nitsche M. A. Physiological basis of transcranial direct current stimulation. The Neuroscientist. 2011;17(1):37–53. doi: 10.1177/1073858410386614.
    1. Nitsche M. A., Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. The Journal of Physiology. 2000;527(3):633–639. doi: 10.1111/j.1469-7793.2000.t01-1-00633.x.
    1. Fertonani A., Miniussi C. Transcranial electrical stimulation: what we know and do not know about mechanisms. The Neuroscientist. 2017;23(2):109–123. doi: 10.1177/1073858416631966.
    1. Kirton A. Can noninvasive brain stimulation measure and modulate developmental plasticity to improve function in stroke-induced cerebral palsy? Seminars in Pediatric Neurology. 2013;20(2):116–126. doi: 10.1016/j.spen.2013.06.004.
    1. Lefaucheur J. P., Antal A., Ayache S. S., et al. Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS) Clinical Neurophysiology. 2017;128(1):56–92. doi: 10.1016/j.clinph.2016.10.087.
    1. Nowak D. A., Grefkes C., Ameli M., Fink G. R. Interhemispheric competition after stroke: brain stimulation to enhance recovery of function of the affected hand. Neurorehabilitation and Neural Repair. 2009;23(7):641–656. doi: 10.1177/1545968309336661.
    1. Prichard G., Weiller C., Fritsch B., Reis J. Effects of different electrical brain stimulation protocols on subcomponents of motor skill learning. Brain Stimulation. 2014;7(4):532–540. doi: 10.1016/j.brs.2014.04.005.
    1. O'Brien A. T., Bertolucci F., Torrealba-Acosta G., Huerta R., Fregni F., Thibaut A. Non-invasive brain stimulation for fine motor improvement after stroke: a meta-analysis. European Journal of Neurology. 2018;25(8):1017–1026. doi: 10.1111/ene.13643.
    1. Elsner B., Kugler J., Pohl M., Mehrholz J., Cochrane Stroke Group Transcranial direct current stimulation (tDCS) for improving activities of daily living, and physical and cognitive functioning, in people after stroke. Cochrane Database of Systematic Reviews. 2016;3, article CD009645 doi: 10.1002/14651858.CD009645.pub3.
    1. Gennaro M., Mattiello A., Mazziotti R., et al. Focal stroke in the developing rat motor cortex induces age- and experience-dependent maladaptive plasticity of corticospinal system. Frontiers in Neural Circuits. 2017;11(47) doi: 10.3389/fncir.2017.00047.
    1. Li L. M., Violante I. R., Leech R., et al. Brain state and polarity dependent modulation of brain networks by transcranial direct current stimulation. Human Brain Mapping. 2018 doi: 10.1002/hbm.24420.
    1. Palm U., Segmiller F. M., Epple A. N., et al. Transcranial direct current stimulation in children and adolescents: a comprehensive review. Journal of Neural Transmission. 2016;123(10):1219–1234. doi: 10.1007/s00702-016-1572-z.
    1. Collange Grecco L. A., de Almeida Carvalho Duarte N., Mendonça M. E., Galli M., Fregni F., Oliveira C. S. Effects of anodal transcranial direct current stimulation combined with virtual reality for improving gait in children with spastic diparetic cerebral palsy: a pilot, randomized, controlled, double-blind, clinical trial. Clinical Rehabilitation. 2015;29(12):1212–1223. doi: 10.1177/0269215514566997.
    1. Hameed M. Q., Dhamne S. C., Gersner R., et al. Transcranial magnetic and direct current stimulation in children. Current Neurology and Neuroscience Reports. 2017;17(2):p. 11. doi: 10.1007/s11910-017-0719-0.
    1. di Pino G., Pellegrino G., Assenza G., et al. Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nature Reviews Neurology. 2014;10(10):597–608. doi: 10.1038/nrneurol.2014.162.
    1. das Nair R., Lincoln N. Effectiveness of memory rehabilitation after stroke. Stroke. 2008;39(2):p. 516. doi: 10.1161/STROKEAHA.107.496935.
    1. Bolognini N., Pascual-Leone A., Fregni F. Using non-invasive brain stimulation to augment motor training-induced plasticity. Journal of Neuroengineering and Rehabilitation. 2009;6(1):p. 8. doi: 10.1186/1743-0003-6-8.
    1. Bikson M., Grossman P., Thomas C., et al. Safety of transcranial direct current stimulation: evidence based update 2016. Brain Stimulation. 2016;9(5):641–661. doi: 10.1016/j.brs.2016.06.004.
    1. Bolognini N., Vallar G., Casati C., et al. Neurophysiological and behavioral effects of tDCS combined with constraint-induced movement therapy in poststroke patients. Neurorehabilitation and Neural Repair. 2011;25(9):819–829. doi: 10.1177/1545968311411056.
    1. Kirton A., Ciechanski P., Zewdie E., et al. Transcranial direct current stimulation for children with perinatal stroke and hemiparesis. Neurology. 2017;88(3):259–267. doi: 10.1212/WNL.0000000000003518.
    1. Gillick B., Rich T., Nemanich S., et al. Transcranial direct current stimulation and constraint-induced therapy in cerebral palsy: a randomized, blinded, sham-controlled clinical trial. European Journal of Paediatric Neurology. 2018;22(3):358–368. doi: 10.1016/j.ejpn.2018.02.001.
    1. Nitsche M. A., Paulus W. Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans. Neurology. 2001;57(10):1899–1901. doi: 10.1212/WNL.57.10.1899.
    1. Boggio P. S., Nunes A., Rigonatti S. P., Nitsche M. A., Pascual-Leone A., Fregni F. Repeated sessions of noninvasive brain DC stimulation is associated with motor function improvement in stroke patients. Restorative Neurology and Neuroscience. 2007;25(2):123–129.
    1. Krishnan C., Santos L., Peterson M. D., Ehinger M. Safety of noninvasive brain stimulation in children and adolescents. Brain Stimulation. 2015;8(1):76–87. doi: 10.1016/j.brs.2014.10.012.
    1. Ciechanski P., Kirton A. Transcranial direct-current stimulation can enhance motor learning in children. Cerebral Cortex. 2017;27(5):2758–2767. doi: 10.1093/cercor/bhw114.
    1. Antal A., Alekseichuk I., Bikson M., et al. Low intensity transcranial electric stimulation: safety, ethical, legal regulatory and application guidelines. Clinical Neurophysiology. 2017;128(9):1774–1809. doi: 10.1016/j.clinph.2017.06.001.
    1. Rossini P. M., Burke D., Chen R., et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clinical Neurophysiology. 2015;126(6):1071–1107. doi: 10.1016/j.clinph.2015.02.001.
    1. 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. Clinical Neurophysiology. 2009;120(12):2008–2039. doi: 10.1016/j.clinph.2009.08.016.
    1. Eliasson A.-C., Krumlinde-Sundholm L., Rösblad B., et al. The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability. Developmental Medicine & Child Neurology. 2006;48(7):549–554. doi: 10.1017/S0012162206001162.
    1. Cioni G., Sales B., Paolicelli P., Petacchi E., Scusa M., Canapicchi R. MRI and clinical characteristics of children with hemiplegic cerebral palsy. Neuropediatrics. 1999;30(5):249–255. doi: 10.1055/s-2007-973499.
    1. Fiori S., Cioni G., Klingels K., et al. Reliability of a novel: semi-quantitative scale for classification of structural brain magnetic resonance imaging in children with cerebral palsy. Developmental Medicine & Child Neurology. 2014;56(9):839–845. doi: 10.1111/dmcn.12457.
    1. Fiori S., Guzzetta A., Pannek K., et al. Validity of semi-quantitative scale for brain MRI in unilateral cerebral palsy due to periventricular white matter lesions: relationship with hand sensorimotor function and structural connectivity. NeuroImage: Clinical. 2015;8:104–109. doi: 10.1016/j.nicl.2015.04.005.
    1. Gandiga P. C., Hummel F. C., Cohen L. G. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clinical Neurophysiology. 2006;117(4):845–850. doi: 10.1016/j.clinph.2005.12.003.
    1. Jongbloed-Pereboom M., Nijhuis-van der Sanden M. W. G., Steenbergen B. Norm scores of the box and block test for children ages 3–10 years. The American Journal of Occupational Therapy. 2013;67(3):312–318. doi: 10.5014/ajot.2013.006643.
    1. Mathiowetz V., Volland G., Kashman N., Weber K. Adult norms for the box and block test of manual dexterity. American Journal of Occupational Therapy. 1985;39(6):386–391. doi: 10.5014/ajot.39.6.386.
    1. Bolognini N., Spandri V., Ferraro F., et al. Immediate and sustained effects of 5-day transcranial direct current stimulation of the motor cortex in phantom limb pain. The Journal of Pain. 2015;16(7):657–665. doi: 10.1016/j.jpain.2015.03.013.
    1. Bolognini N., Convento S., Banco E., Mattioli F., Tesio L., Vallar G. Improving ideomotor limb apraxia by electrical stimulation of the left posterior parietal cortex. Brain. 2015;138(2):428–439. doi: 10.1093/brain/awu343.
    1. Mailleux L., Simon-Martinez C., Klingels K., et al. Structural brain damage and upper limb kinematics in children with unilateral cerebral palsy. Frontiers in Human Neuroscience. 2017;11:p. 607. doi: 10.3389/fnhum.2017.00607.
    1. Bolognini N., Souza Carneiro M. I., Russo C., Vallar G. Transcranial direct current stimulation in stroke rehabilitation: ready to move to randomized clinical trials and clinical practice? The issue of safety guidelines. European Journal of Neurology. 2017;24(11):p. e78. doi: 10.1111/ene.13396.
    1. Russo C., Souza Carneiro M. I., Bolognini N., Fregni F. Safety review of transcranial direct current stimulation in stroke. Neuromodulation: Technology at the Neural Interface. 2017;20(3):215–222. doi: 10.1111/ner.12574.
    1. Gillick B. T., Gordon A. M., Feyma T., et al. Non-invasive brain stimulation in children with unilateral cerebral palsy: a protocol and risk mitigation guide. Frontiers in Pediatrics. 2018;6:p. 56. doi: 10.3389/fped.2018.00056.

Source: PubMed

3
Abonnieren