Enhancing neuromuscular training effect on balance and gait in autistic children by transcranial direct current stimulation

Document Type : Research Paper

Authors

1 University of Tehran, Faculty of Sport Sciences and Health, Department of Sport injuries and Biomechanic, Tehran, Iran

2 Department of Sport injuries and Biomechanic, Faculty of Sport Sciences and Health, University of Tehran, Tehran, IranNeuroscience phd

3 دانشگاه تهران

Abstract

Background: Both of transcranial direct current electrical stimulation (tDCS) and neuromuscular training (NMT) have used to relive motor deficits in neurological disease.
Aim: We decided to investigate augmenting effect of tDCS and NMT to improve static and dynamic balance and gait parameter in autism spectrum disorder (ASD).
Materials and Methods: 24 children with ASD aged 6-10 years old were randomly assigned to one of three groups: NMT+ sham, anodal tDCS, and NMT + tDCS. NMT consisted of 10 sessions motor training (each for 40 min). tDCS training was performed with 1.5 mA on left primary motor cortex for 20 min. Pre-test and post-test evaluations included static and dynamic balance and gait parameters (length and width of stepping and speed of gait).
Results: Although improvement of variables were seen in all groups, but in post intervention comparison, combined group was better in static and dynamic balance and gait parameters than two other groups. NMT was more effective than tDCS only in dynamic balance.
Conclusion: Our findings were indicated tDCS enhance NMT effect on neuromuscular function in ASD, so regarding the augmented effect in combination of NMT and tDCS, it can be considered in rehabilitation of motor deficits in these children.

Keywords


[1] Bhat AN. "Motor impairment increases in children with ASD as a function of social communication, cognitive and functional impairment, repetitive behavior severity, and comorbid diagnoses: A SPARK study report". Autism Research. 2021; 14(1): 202-19. doi: 10.1002/aur.2453.
[2] Fournier KA, Hass CJ, Naik SK, Lodha N, Cauraugh JH. "Motor coordination in ASDs: a synthesis and meta-analysis". Journal of Autism and Developmental Disorders. 2010; 40: 1227-40. doi: 10.1007/s10803-010-0981-3.
[3] Nobile M, Perego P, Piccinini L, Mani E, Rossi A, Bellina M, Molteni M. "Further evidence of complex motor dysfunction in drug naive children with autism using automatic motion analysis of gait". Autism. 2011; 15(3): 263-83. doi: 10.1177/1362361309356929.
[4] Abdel Ghafar MA, Abdelraouf OR, Abdelgalil AA, Seyam MK, Radwan RE, El-Bagalaty AE. "Quantitative assessment of sensory integration and balance in children with ASDs: Cross-sectional study". Children. 2022; 9(3): 353. doi: 10.3390/children9030353.
[5] Gunderson J, Worthley E, Byiers B, Symons F, Wolff J. "Self and caregiver report measurement of sensory features in ASD: a systematic review of psychometric properties". Journal of Neurodevelopmental Disorders. 2023; 15(1): 5. doi: 0.1186/s11689-022-09473-7.
[6] Chakrabarty B, Gulati S. "ASD: sleep morbidities and sensory impairment; emerging paradigm in research and management". The Indian Journal of Pediatrics. 2019; 86: 1-2. doi: 10.1007%2Fs12098-018-2814-x.
[7] Ben-Sasson A, Hen L, Fluss R, Cermak SA, Engel-Yeger B, Gal E. "A meta-analysis of sensory modulation symptoms in individuals with ASDs". Journal of Autism and Developmental Disorders. 2009; 39: 1-11. doi: 10.1007/s10803-008-0593-3.
[8] Hariri R, Nakhostin-Ansari A, Mohammadi F, Memari AH, Oskouie IM, Haghparast A. "An overview of the available intervention strategies for postural balance control in individuals with autism spectrum disorder". Autism Research and Treatment. 2022: 9. doi: 10.1155/2022/3639352.
[9] Massetti T, Crocetta TB, Silva TDd, Trevizan IL, Arab C, Caromano FA, Monteiro CBdM. "Application and outcomes of therapy combining transcranial direct current stimulation and virtual reality: a systematic review". Disability and Rehabilitation: Assistive Technology. 2017; 12(6): 551-9. doi: 10.1080/17483107.2016.1230152.
[10] Nitsche MA, Cohen LG, Wassermann EM, Priori A, Lang N, Antal A, et al. "Transcranial direct current stimulation: state of the art 2008". Brain Stimulation. 2008; 1(3): 206-23. doi: 10.1016/j.brs.2008.06.004.
[11] Fritsch B, Reis J, Martinowich K, Schambra HM, Ji Y, Cohen LG, Lu B. "Direct current stimulation promotes BDNF-dependent synaptic plasticity: Potential implications for motor learning". Neuron. 2010; 66(2): 198-204. doi: 10.1016/j.neuron.2010.03.035.
[12] Antal A, Alekseichuk I, Bikson M, Brockmöller J, Brunoni AR, Chen R, et al. "Low intensity transcranial electric stimulation: safety, ethical, legal regulatory and application guidelines". Clinical Neurophysiology. 2017; 128(9): 1774-809. doi: 10.1016/j.clinph.2017.06.001.
[13] Pascual-Leone A, Freitas C, Oberman L, Horvath JC, Halko M, Eldaief M, et al. "Characterizing brain cortical plasticity and network dynamics across the age-span in health and disease with TMS-EEG and TMS-fMRI". Brain Topography. 2011; 24: 302-15. doi: 10.1007/s10548-011-0196-8.
[14] Baizer JS. "Functional and neuropathological evidence for a role of the brainstem in autism". Frontiers in Integrative Neuroscience. 2021; 15: 748977. doi: 10.3389/fnint.2021.748977.
[15] Hupfeld K, Ketcham C. "Behavioral effects of transcranial direct current stimulation on motor and language planning in minimally verbal children with autism spectrum disorder (ASD): feasibility, limitations and future directions". J Child Dev Disord. 2016; 2(10.4172): 2472-1786.100029. doi: 10.4172/2472-1786.100029.
[16] Cardinale RC, Shih P, Fishman I, Ford LM, Müller RA. "Pervasive rightward asymmetry shifts of functional networks in autism spectrum disorder". JAMA Psychiatry. 2013; 70(9): 975-82. doi: 10.1001/jamapsychiatry.2013.382.
[17] D’Urso G, Bruzzese D, Ferrucci R, Priori A, Pascotto A, Galderisi S, et al. "Transcranial direct current stimulation for hyperactivity and noncompliance in autistic disorder". The World Journal of Biological Psychiatry. 2015; 16(5): 361-6. doi: 10.3109/15622975.2015.1014411.
[18] Schneider HD, Hopp JP. "The use of the Bilingual Aphasia Test for assessment and transcranial direct current stimulation to modulate language acquisition in minimally verbal children with autism". Clinical Linguistics & Phonetics. 2011; 25(6-7): 640-54. doi: 10.3109/02699206.2011.570852.
[19] Rothärmel M, Moulier V, Vasse M, Isaac C, Faerber M, Bendib B, et al. "A prospective open-label pilot study of transcranial direct current stimulation in high-functioning autistic patients with a dysexecutive syndrome". Neuropsychobiology. 2019; 78(4): 189-99. doi: 10.1159/000501025.
[20] Mahmoodifar E, Sotoodeh MS. "Combined transcranial direct current stimulation and selective motor training enhances balance in children with autism spectrum disorder". Perceptual and Motor Skills. 2020; 127(1): 113-25. doi: 10.1177/0031512519888072.
[21] Raj V. "Importance of neuromuscular training of athletes". IJSS. 2015; 5: 141-5.
[22] Tsauo JY, Cheng PF, Yang RS. "The effects of sensorimotor training on knee proprioception and function for patients with knee osteoarthritis: a preliminary report". Clinical Rehabilitation. 2008; 22(5): 448-57. doi: 10.1177/0269215507084597.
[23] Shavikloo J, Norasteh A. The Effect of Integrative Neuromuscular Training on Postural Control of Children with Autism Spectrum. OA Text. 2018.
[24] Cristian P, Elsayed M. "Effectiveness of neuromuscular training on functional balance forchildren with neurodevelopmental disorders". Ovidius University Annals, Series Physical Education & Sport/Science, Movement & Health. 2019; 19. Romania.
[25] Dehghani M, Jafarnezhadgero AA, Darvishani MA, Aali S, Granacher U. "Effects of an 8-week multimodal exercise program on ground reaction forces and plantar pressure during walking in boys with autism spectrum disorder". Trials. 2023; 24(1): 1-10.
[26] Araujo MO, Tamplain P, Duarte NA, Comodo A, Ferreira GO, Queiróga A, et al. "Transcranial direct current stimulation to facilitate neurofunctional rehabilitation in children with autism spectrum disorder: a protocol for a randomized, sham-controlled, double-blind clinical trial". Frontiers in Neurology. 2023; 14: 1196585. doi: 10.3389/fneur.2023.1196585.
[27] Llorens R, Fuentes MA, Borrego A, Latorre J, Alcañiz M, Colomer C, Noé E. "Effectiveness of a combined transcranial direct current stimulation and virtual reality-based intervention on upper limb function in chronic individuals post-stroke with persistent severe hemiparesis: A randomized controlled trial". Journal of Neuroengineering and Rehabilitation. 2021; 18: 1-13. doi: 0.1186/s12984-021-00896-2.
[28] Teixeira PE, Alawdah L, Alhassan HAA, Guidetti M, Priori A, Papatheodorou S, Fregni F. "The analgesic effect of transcranial direct current stimulation (tdcs) combined with physical therapy on common musculoskeletal conditions: A systematic review and meta-analysis". Principles and Practice of Clinical Research. 2020; 6(1): 23. doi: 10.21801%2Fppcrj.2020.61.5.
[29] Beretta VS, Conceição NR, Nóbrega-Sousa P, Orcioli-Silva D, Dantas LKBF, Gobbi LTB, Vitório R. "Transcranial direct current stimulation combined with physical or cognitive training in people with Parkinson’s disease: A systematic review". Journal of Neuroengineering and Rehabilitation. 2020; 17(1): 1-15. doi: 0.1186/s12984-020-00701-6.
[30] Wang B, Xiao S, Yu C, Zhou J, Fu W. "Effects of transcranial direct current stimulation combined with physical training on the excitability of the motor cortex, physical performance, and motor learning: A systematic review". Frontiers in Neuroscience. 2021; 15: 648354. doi: 10.3389/fnins.2021.648354.
[31] Grooms DR, Kiefer AW, Riley MA, Ellis JD, Thomas S, Kitchen K, et al. "Brain-behavior mechanisms for the transfer of neuromuscular training adaptions to simulated sport: Initial findings from the train the brain project". Journal of Sport Rehabilitation. 2018; 27(5). doi: 10.1123/jsr.2017-0241.
[32] Guha M. "Diagnostic and statistical manual of mental disorders: DSM-5". Reference Reviews. 2014; 28(3): 36-7.
[33] Grahek I, Everaert J, Krebs RM, Koster EH. "Cognitive control in depression: Toward clinical models informed by cognitive neuroscience". Clinical Psychological Science. 2018; 6(4): 464-80. doi: 10.1177/2167702618758969.
[34] Şenol D, Altinoğlu M, Şeyma T, Kisaoğlu A, Özbağ D. "Investigation of the relationship of Q Angle and stork balance stand test with somatotype in healthy young individuals". Medical Records. 2019; 1(3): 60-6.
[35] Hammami R, Granacher U, Makhlouf I, Behm DG, Chaouachi A. "Sequencing effects of balance and plyometric training on physical performance in youth soccer athletes". The Journal of Strength & Conditioning Research. 2016; 30(12): 3278-89. doi: 10.1519/JSC.0000000000001425.
[36] Cohen HS, Stitz J, Sangi‐Haghpeykar H, Williams SP, Mulavara AP, Peters BT, Bloomberg JJ. "Tandem walking as a quick screening test for vestibular disorders". The Laryngoscope. 2018; 128(7): 1687-91. doi: 10.1002/lary.27022.
[37] Mansori MH, Moghadas Tabrizi Y, Mohammadkhani K. "Evaluation of the effectiveness of dynamic neuromuscular stability exercises on balance and walking function in the elderly". Iranian Rehabilitation Journal. 2021; 19(3): 279-88. doi: 10.32598/irj.19.3.1406.3.
[38] Cimolin V, Galli M. "Summary measures for clinical gait analysis: A literature review". Gait & Posture. 2014; 39(4): 1005-10. doi: 10.1016/j.gaitpost.2014.02.001.
[39] de Paz RH, Serrano-Muñoz D, Pérez-Nombela S, Bravo-Esteban E, Avendaño-Coy J, Gómez-Soriano J. "Combining transcranial direct-current stimulation with gait training in patients with neurological disorders: A systematic review". Journal of Neuroengineering and Rehabilitation. 2019; 16(1): 1-8. doi: 0.1186/s12984-019-0591-z.
[40] Navarro-Lopez V, Molina-Rueda F, Jimenez-Jimenez S, Alguacil-Diego IM, Carratala-Tejada M. "Effects of transcranial direct current stimulation combined with physiotherapy on gait pattern, balance, and functionality in stroke patients. A systematic review". Diagnostics. 2021; 11(4): 656. doi: 10.3390/diagnostics11040656.
[41] Duarte NdAC, Grecco LAC, Galli M, Fregni F, Oliveira CS. "Effect of transcranial direct-current stimulation combined with treadmill training on balance and functional performance in children with cerebral palsy: a double-blind randomized controlled trial". PloS one. 2014; 9(8): e105777. doi: 10.1371/journal.pone.0105777.
[42] Kaski D, Dominguez R, Allum J, Islam A, Bronstein A. "Combining physical training with transcranial direct current stimulation to improve gait in Parkinson’s disease: A pilot randomized controlled study". Clinical Rehabilitation. 2014; 28(11): 1115-24. doi: 10.1177/0269215514534277.
[43] Weber MJ, Messing SB, Rao H, Detre JA, Thompson‐Schill SL. "Prefrontal transcranial direct current stimulation alters activation and connectivity in cortical and subcortical reward systems: A tDCS‐fMRI study". Human Brain Mapping. 2014; 35(8): 3673-86. doi: 10.1002/hbm.22429.
[44] Fisher BE, Wu AD, Salem GJ, Song J, Lin CHJ, Yip J, et al. "The effect of exercise training in improving motor performance and corticomotor excitability in people with early Parkinson's disease". Archives of Physical Medicine and Rehabilitation. 2008; 89(7): 1221-9. doi: 10.1016/j.apmr.2008.01.013.
[45] Tanaka S, Takeda K, Otaka Y, Kita K, Osu R, Honda M, et al. "Single session of transcranial direct current stimulation transiently increases knee extensor force in patients with hemiparetic stroke". Neurorehabilitation and Neural Repair. 2011; 25(6): 565-9. doi: 10.1177/1545968311402091.
[46] Jeffery DT, Norton JA, Roy FD, Gorassini MA. "Effects of transcranial direct current stimulation on the excitability of the leg motor cortex". Experimental Brain Research. 2007; 182: 281-7. doi: 10.1007/s00221-007-1093-y.
[47] Talelli P, Rothwell J. "Does brain stimulation after stroke have a future?". Current Opinion in Neurology. 2006; 19(6): 543-50. doi: 10.1097/WCO.0b013e32801080d1.
[48] Angius L, Hopker J, Mauger AR. "The ergogenic effects of transcranial direct current stimulation on exercise performance". Frontiers in Physiology. 2017; 8: 90. doi:10.3389/fphys.2017.00090.
[49] Grecco LAC, Duarte NdAC, Mendonça ME, Cimolin V, Galli M, Fregni F, Oliveira CS. "Transcranial direct current stimulation during treadmill training in children with cerebral palsy: a randomized controlled double-blind clinical trial". Research in Developmental Disabilities. 2014; 35(11): 2840-8. doi: 10.1016/j.ridd.2014.07.030.
[50] Salar S, Daneshmandi H, Karimizadeh Ardakani M, Nazari Sharif H. "The relationship of core strength with static and dynamic balance in children with autism". Annals of Applied Sport Science. 2014; 2(4): 33-42. doi: 10.18869/acadpub.aassjournal.2.4.33.