Brain stimulation for patients with multiple sclerosis: an umbrella review of therapeutic efficacy

Cohrs S (2008) Sleep disturbances in patients with schizophrenia. CNS Drugs 22(11):939–62

World Health Organization (2004) Atlas: country resources for neurological disorders 2004: results of a collaborative study of the World Health Organization and the World Federation of Neurology. World Health Organization

Ayache SS, Creange A, Farhat WH, Zouari HG, Lesage C, Palm U et al (2015) Cortical excitability changes over time in progressive multiple sclerosis. Funct Neurol 30(4):257–263

Coles A (2008) Alastair Compston, Alasdair Coles. Lancet 372:1502–1517

Amatya B, Khan F, La Mantia L, Demetrios M, Wade DT (2013) Non pharmacological interventions for spasticity in multiple sclerosis. Cochrane Database Syst Rev 2:CD009974

Patwardhan MB, Matchar DB, Samsa GP, McCrory DC, Williams RG, Li TT (2005) Cost of multiple sclerosis by level of disability: a review of literature. Mult Scler 11(2):232–239

Peterson EW, Cho CC, von Koch L, Finlayson ML (2008) Injurious falls among middle aged and older adults with multiple sclerosis. Arch Phys Med Rehab 89(6):1031–1037

Neva JL, Lakhani B, Brown KE, Wadden KP, Mang CS, Ledwell NH et al (2016) Multiple measures of corticospinal excitability are associated with clinical features of multiple sclerosis. Behav Brain Res 297:187–195

Comabella M, Montalban X (2014) Body fluid biomarkers in multiple sclerosis. Lancet Neurol 13(1):113–126

Ziemssen T, Derfuss T, de Stefano N, Giovannoni G, Palavra F, Tomic D et al (2016) Optimizing treatment success in multiple sclerosis. J Neurol 263(6):1053–1065

Andravizou A, Siokas V, Artemiadis A, Bakirtzis C, Aloizou A-M, Grigoriadis N et al (2020) Clinically reliable cognitive decline in relapsing remitting multiple sclerosis: is it the tip of the iceberg? Neurol Res 42(7):575–586

Chalah MA, Riachi N, Ahdab R, Creange A, Lefaucheur JP, Ayache SS (2015) Fatigue in multiple sclerosis: neural correlates and the role of non-invasive brain stimulation. Front Cell Neurosci 9:460

von Bismarck O, Dankowski T, Ambrosius B, Hessler N, Antony G, Ziegler A et al (2018) Treatment choices and neuropsychological symptoms of a large cohort of early MS. Neurol Neuroimmunol Neuroinflamm 5(3):e446

Leocani L, Chieffo R, Gentile A, Centonze D (2019) Beyond rehabilitation in MS: Insights from non-invasive brain stimulation. Mult Scler 25(10):1363–1371

Wingerchuk DM, Carter JL (2014) Multiple sclerosis: current and emerging disease-modifying therapies and treatment strategies. Mayo Clinic Proceedings 89(2):225–240

Comi G, Radaelli M, Soelberg SP (2017) Evolving concepts in the treatment of relapsing multiple sclerosis. Lancet 389(10076):1347–1356

Bartlett TE, Wang YT (2013) The intersections of NMDAR-dependent synaptic plasticity and cell survival. Neuropharmacology 74:59–68

Sampaio-Baptista C, Johansen-Berg H (2017) White matter plasticity in the adult brain. Neuron 96(6):1239–1251

Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1(8437):1106–1107

Mori F, Codeca C, Kusayanagi H, Monteleone F, Boffa L, Rimano A et al (2010) Effects of intermittent theta burst stimulation on spasticity in patients with multiple sclerosis. Eur J Neurol 17(2):295–300

Rossini PM, Burke D, Chen R, Cohen L, Daskalakis Z, Di Iorio R et al (2015) 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 IFCN Committee. Clin Neurophysiol 126(6):1071–107

Rotenberg A, Horvath JC, Pascual-Leone A (2014) The transcranial magnetic stimulation (TMS) device and foundational techniques. Springer, New York

Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929

Huang Y-Z, Chen R-S, Rothwell JC, Wen H-Y (2007) The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 118(5):1028–1032

Mori F, Koch G, Foti C, Bernardi G, Centonze D (2009) The use of repetitive transcranial magnetic stimulation (rTMS) for the treatment of spasticity. Prog Brain Res 175:429–439

Siebner H, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16

Stagg CJ, Nitsche MA (2011) Physiological basis of transcranial direct current stimulation. Neuroscientist 17(1):37–53

Krause B, Marquez-Ruiz J, Cohen KR (2013) The effect of transcranial direct current stimulation: a role for cortical excitation/inhibition balance? Front Hum Neurosci 7:602

Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 6(3):424–432

Batsikadze G, Moliadze V, Paulus W, Kuo MF, Nitsche MA (2013) Partially non-linear stimulation intensity-dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol 591(7):1987–2000

Woods AJ, Antal A, Bikson M, Boggio PS, Brunoni AR, Celnik P et al (2016) A technical guide to tDCS, and related non-invasive brain stimulation tools. Clin Neurophysiol 127(2):1031–1048

Abdelmoula A, Baudry S, Duchateau J (2016) Anodal transcranial direct current stimulation enhances time to task failure of a submaximal contraction of elbow flexors without changing corticospinal excitability. Neuroscience 322:94–103

Meesen RL, Thijs H, Leenus DJ, Cuypers K (2014) A single session of 1 mA anodal tDCS-supported motor training does not improve motor performance in patients with multiple sclerosis. Restor Neurol Neurosci 32(2):293–300

Iodice R, Dubbioso R, Ruggiero L, Santoro L, Manganelli F (2015) Anodal transcranial direct current stimulation of motor cortex does not ameliorate spasticity in multiple sclerosis. Restor Neurol Neurosci 33(4):487–492

Ayache SS, Palm U, Chalah MA, Al-Ani T, Brignol A, Abdellaoui M et al (2016) Prefrontal tDCS decreases pain in patients with multiple sclerosis. Front Neurosci 10:147

Mori F, Nicoletti CG, Kusayanagi H, Foti C, Restivo DA, Marciani MG, Centonze D (2013) Transcranial direct current stimulation ameliorates tactile sensory deficit in multiple sclerosis. Brain Stimul 6(4):654–659

Tecchio F, Cancelli A, Cottone C, Zito G, Pasqualetti P, Ghazaryan A et al (2014) Multiple sclerosis fatigue relief by bilateral somatosensory cortex neuromodulation. J Neurol 261(8):1552–1558

Mattioli F, Bellomi F, Stampatori C, Capra R, Miniussi C (2016) Neuroenhancement through cognitive training and anodal tDCS in multiple sclerosis. Mult Scler J 22(2):222–230

Kringelbach ML, Jenkinson N, Owen SL, Aziz TZ (2007) Translational principles of deep brain stimulation. Nat Rev Neurosci 8(8):623–635

Roy HA, Aziz TZ (2014) Deep brain stimulation and multiple sclerosis: therapeutic applications. Mult Scler Relat Disord 3(4):431–439

Mohammadipour F, Atashzadeh-Shoorideh F, Parvizy S, Hosseini M (2017) An explanatory study on the concept of nursing presence from the perspective of patients admitted to hospitals. J Clin Nurs 26(23–24):4313–4324

Kan RLD, Xu GXJ, Shu KT, Lai FHY, Kranz G, Kranz GS (2022) Effects of non-invasive brain stimulation in multiple sclerosis: systematic review and meta-analysis. Ther Adv Chronic Dis 13:20406223211069200

Hsu WY, Cheng CH, Zanto TP, Gazzaley A, Bove RM (2021) Effects of transcranial direct current stimulation on cognition, mood, pain, and fatigue in multiple sclerosis: a systematic review and meta-analysis. Front Neurol 12:626113

Hadoush H, Alawneh A, Kassab M, Al-Wardat M, Al-Jarrah M (2022) Effectiveness of non-pharmacological rehabilitation interventions in pain management in patients with multiple sclerosis: systematic review and meta-analysis. NeuroRehabilitation 50(4):347–365

Hiew S, Nguemeni C, Zeller D (2022) Efficacy of transcranial direct current stimulation in people with multiple sclerosis: a review. Eur J Neurol 29(2):648–664

Zucchella C, Mantovani E, De Icco R, Tassorelli C, Sandrini G, Tamburin S (2020) Non-invasive brain and spinal stimulation for pain and related symptoms in multiple sclerosis: a systematic review. Front Neurosci 14:547069

Liu M, Fan S, Xu Y, Cui L (2019) Non-invasive brain stimulation for fatigue in multiple sclerosis patients: a systematic review and meta-analysis. Mult Scler Relat Disord 36:101375

Jaeger S, Paul F, Scheel M, Brandt A, Heine J, Pach D et al (2019) Multiple sclerosis-related fatigue: altered resting-state functional connectivity of the ventral striatum and dorsolateral prefrontal cortex. Mult Scler 25(4):554–564

Chalah MA, Kauv P, Creange A, Hodel J, Lefaucheur JP, Ayache SS (2019) Neurophysiological, radiological and neuropsychological evaluation of fatigue in multiple sclerosis. Mult Scler Relat Disord 28:145–152

Boggio PS, Rigonatti SP, Ribeiro RB, Myczkowski ML, Nitsche MA, Pascual-Leone A, Fregni F (2008) A randomized, double-blind clinical trial on the efficacy of cortical direct current stimulation for the treatment of major depression. Int J Neuropsychopharmacol 11(2):249–254

Chalah MA, Riachi N, Ahdab R, Mhalla A, Abdellaoui M, Creange A et al (2017) Effects of left DLPFC versus right PPC tDCS on multiple sclerosis fatigue. J Neurol Sci 372:131–137

Bakshi R, Shaikh ZA, Miletich RS, Czarnecki D, Dmochowski J, Henschel K et al (2000) Fatigue in multiple sclerosis and its relationship to depression and neurologic disability. Mult Scler 6(3):181–185

Li S, Zhang Q, Zheng S, Li G, Li S, He L, Zeng Y, Chen L, Chen S, Zheng X, Zou J (2023) Efficacy of non-invasive brain stimulation on cognitive and motor functions in multiple sclerosis: A systematic review and meta-analysis. Front Neurol 14:1091252

Li S, Zhang Q, Zheng S, Li G, Li S, He L et al (2023) Efficacy of non-invasive brain stimulation on cognitive and motor functions in multiple sclerosis: a systematic review and meta-analysis. Front Neurol 14:1091252

Filippi M, Riccitelli G, Mattioli F, Capra R, Stampatori C, Pagani E et al (2012) Multiple sclerosis: effects of cognitive rehabilitation on structural and functional MR imaging measures–an explorative study. Radiology 262(3):932–940

Sastre-Garriga J, Alonso J, Renom M, Arevalo MJ, Gonzalez I, Galan I et al (2011) A functional magnetic resonance proof of concept pilot trial of cognitive rehabilitation in multiple sclerosis. Mult Scler 17(4):457–467

Cerasa A, Gioia MC, Valentino P, Nistico R, Chiriaco C, Pirritano D et al (2013) Computer-assisted cognitive rehabilitation of attention deficits for multiple sclerosis: a randomized trial with fMRI correlates. Neurorehabil Neural Repair 27(4):284–295

Leon Ruiz M, Sospedra M, Arce Arce S, Tejeiro-Martinez J, Benito-Leon J (2022) Current evidence on the potential therapeutic applications of transcranial magnetic stimulation in multiple sclerosis: a systematic review of the literature. Neurologia 37(3):199–215

Chen X, Yin L, An Y, Yan H, Zhang T, Lu X, Yan J (2022) Effects of repetitive transcranial magnetic stimulation in multiple sclerosis: a systematic review and meta-analysis. Mult Scler Relat Disord 59:103564

Khan F, Amatya B, Bensmail D, Yelnik A (2019) Non-pharmacological interventions for spasticity in adults: an overview of systematic reviews. Ann Phys Rehabil Med 62(4):265–273

Hughes C, Howard IM (2013) Spasticity management in multiple sclerosis. Phys Med Rehabil Clin N Am 24(4):593–604

Iodice R, Manganelli F, Dubbioso R (2017) The therapeutic use of non-invasive brain stimulation in multiple sclerosis - a review. Restor Neurol Neurosci 35(5):497–509

Fjeldstad C, Pardo G, Bemben D, Bemben M (2011) Decreased postural balance in multiple sclerosis patients with low disability. Int J Rehabil Res 34(1):53–58

Zali A, Khoshnood RJ, Motavaf M, Salimi A, Akhlaghdoust M, Safari S et al (2021) Deep brain stimulation for multiple sclerosis tremor: a systematic review and meta-analysis. Mult Scler Relat Disord 56:103256

Brandmeir NJ, Murray A, Cheyuo C, Ferari C, Rezai AR (2020) Deep brain stimulation for multiple sclerosis tremor: a meta-analysis. Neuromodulation 23(4):463–468

Wishart HA, Roberts DW, Roth RM, McDonald BC, Coffey DJ, Mamourian AC et al (2003) Chronic deep brain stimulation for the treatment of tremor in multiple sclerosis: review and case reports. J Neurol Neurosurg Psychiatry 74(10):1392–1397

Yap L, Kouyialis A, Varma TR (2007) Stereotactic neurosurgery for disabling tremor in multiple sclerosis: thalamotomy or deep brain stimulation? Br J Neurosurg 21(4):349–354

Razza LB, Palumbo P, Moffa AH, Carvalho AF, Solmi M, Loo CK, Brunoni AR (2020) A systematic review and meta-analysis on the effects of transcranial direct current stimulation in depressive episodes. Depress Anxiety 37(7):594–608

Grimm S, Beck J, Schuepbach D, Hell D, Boesiger P, Bermpohl F et al (2008) Imbalance between left and right dorsolateral prefrontal cortex in major depression is linked to negative emotional judgment: an fMRI study in severe major depressive disorder. Biol Psychiatry 63(4):369–376

Vanderhasselt MA, De Raedt R, Leyman L, Baeken C (2009) Acute effects of repetitive transcranial magnetic stimulation on attentional control are related to antidepressant outcomes. J Psychiatry Neurosci 34(2):119–126

Keeser D, Padberg F, Reisinger E, Pogarell O, Kirsch V, Palm U et al (2011) Prefrontal direct current stimulation modulates resting EEG and event-related potentials in healthy subjects: a standardized low resolution tomography (sLORETA) study. Neuroimage 55(2):644–657

Keeser D, Meindl T, Bor J, Palm U, Pogarell O, Mulert C et al (2011) Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J Neurosci 31(43):15284–15293