Advertisement
Original article| Volume 96, ISSUE 1, P69-75, January 2015

Download started.

Ok

Corticospinal Integrity and Motor Impairment Predict Outcomes After Excitatory Repetitive Transcranial Magnetic Stimulation: A Preliminary Study

Published:September 13, 2014DOI:https://doi.org/10.1016/j.apmr.2014.08.014

      Abstract

      Objective

      To identify the effective predictors for therapeutic outcomes based on intermittent theta-burst stimulation (iTBS).

      Design

      A sham-controlled, double-blind parallel study design.

      Setting

      A tertiary hospital.

      Participants

      People with stroke (N=72) who presented with unilateral hemiplegia.

      Interventions

      Ten consecutive sessions of real or sham iTBS were implemented with the aim of enhancing hand function. Patients were categorized into 4 groups according to the presence (MEP+) or absence (MEP−) of motor-evoked potentials (MEPs) and grip strength according to the Medical Research Council (MRC) scale.

      Main Outcome Measures

      Cortical excitability, Wolf Motor Function Test (WMFT), finger-tapping task (FT), and simple reaction time were performed before and after the sessions.

      Results

      MEPs and the MRC scale were predictive of iTBS therapeutic outcomes. Group A (MEP+, MRC>1) exhibited the greatest WMFT change (7.6±2.3, P<.001), followed by group B (MEP−, MRC>1; 5.2±2.2 score change) and group C (MEP−, MRC=0; 2.3±1.5 score change). These improvements were correlated significantly with baseline motor function and ipsilesional maximum MEP amplitude.

      Conclusions

      The effectiveness of iTBS modulation for poststroke motor enhancement depends on baseline hand grip strength and the presence of MEPs. Our findings indicate that establishing neurostimulation strategies based on the proposed electrophysiological and clinical criteria can allow iTBS to be executed with substantial precision. Effective neuromodulatory strategies can be formulated by using electrophysiological features and clinical presentation information as guidelines.

      Keywords

      List of abbreviations:

      aMT (active motor threshold), CST (corticospinal tract), FDI (first dorsal interosseous), fMRI (functional magnetic resonance imaging), FT (finger-tapping task), iTBS (intermittent theta-burst stimulation), MEP (motor-evoked potential), MRC (Medical Research Council), MT (motor threshold), RT (reaction time), rTMS (repetitive transcranial magnetic stimulation), WMFT (Wolf Motor Function Test)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Archives of Physical Medicine and Rehabilitation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Jørgensen H.S.
        • Nakayama H.
        • Raaschou H.O.
        • Vive-Larsen J.
        • Støier M.
        • Olsen T.S.
        Outcome and time course of recovery in stroke. Part II: time course of recovery. The Copenhagen Stroke Study.
        Arch Phys Med Rehabil. 1995; 76: 406-412
        • Cramer S.C.
        • Sur M.
        • Dobkin B.H.
        • et al.
        Harnessing neuroplasticity for clinical applications.
        Brain. 2011; 134: 1591-1609
        • Ward N.S.
        • Brown M.M.
        • Thompson A.J.
        • Frackowiak R.S.
        Neural correlates of motor recovery after stroke: a longitudinal fMRI study.
        Brain. 2003; 126: 2476-2479
        • Khedr E.M.
        • Ahmed M.A.
        • Fathy N.
        • Rothwell J.C.
        Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke.
        Neurology. 2005; 65: 466-468
        • Mansur C.G.
        • Fregni F.
        • Boggio P.S.
        • et al.
        A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients.
        Neurology. 2005; 64: 1802-1804
        • Bolognini N.
        • Pascual-Leone A.
        • Fregni F.
        Using non-invasive brain stimulation to augment motor training-induced plasticity.
        J Neuroeng Rehabil. 2009; 6: 8-20
        • Iezzi E.
        • Suppa A.
        • Conte A.
        • Li Voti P.
        • Bologna M.
        • Berardelli A.
        Short-term and long-term plasticity interaction in human primary motor cortex.
        Eur J Neurosci. 2011; 33: 1908-1915
        • Wang H.
        • Wang X.
        • Wetzel W.
        • Scheich H.
        Rapid-rate transcranial magnetic stimulation in auditory cortex induces LTP and LTD and impairs discrimination learning of frequency-modulated tones.
        Electroencephalogr Clin Neurophysiol Suppl. 1999; 51: 361-367
        • Murase N.
        • Duque J.
        • Mazzocchio R.
        • Cohen L.G.
        Influence of interhemispheric interactions on motor function in chronic stroke.
        Ann Neurol. 2004; 55: 400-409
        • Huang Y.Z.
        • Chen R.S.
        • Rothwell J.C.
        • Wen H.Y.
        The after-effect of human theta burst stimulation is NMDA receptor dependent.
        Clin Neurophysiol. 2007; 118: 1028-1032
        • Ameli M.
        • Grefkes C.
        • Kemper F.
        • et al.
        Differential effects of high-frequency repetitive transcranial magnetic stimulation over ipsilesional primary motor cortex in cortical and subcortical middle cerebral artery stroke.
        Ann Neurol. 2009; 66: 298-309
        • Pennisi G.
        • Rapisarda G.
        • Bella R.
        • Calabrese V.
        • Maertens De Noordhout A.
        • Delwaide P.J.
        Absence of response to early transcranial magnetic stimulation in ischemic stroke patients: prognostic value for hand motor recovery.
        Stroke. 1999; 30: 2666-2670
        • Stinear C.M.
        • Barber P.A.
        • Smale P.R.
        • Coxon J.P.
        • Fleming M.K.
        • Byblow W.D.
        Functional potential in chronic stroke patients depends on corticospinal tract integrity.
        Brain. 2007; 130: 170-180
        • Rapisarda G.
        • Bastings E.
        • de Noordhout A.M.
        • Pennisi G.
        • Delwaide P.J.
        Can motor recovery in stroke patients be predicted by early transcranial magnetic stimulation?.
        Stroke. 1996; 27: 2191-2196
        • Pleger B.
        • Blankenburg F.
        • Bestmann S.
        • et al.
        Repetitive transcranial magnetic stimulation-induced changes in sensorimotor coupling parallel improvements of somatosensation in humans.
        J Neurosci. 2006; 26: 1945-1952
        • Grefles C.
        • Nowak D.A.
        • Wang L.E.
        • Dafotakis M.
        • Eickhoff S.B.
        • Fink G.R.
        Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling.
        Neuroimage. 2010; 50: 233-242
        • Demeurisse G.
        • Demol O.
        • Robaye E.
        Motor evaluation in vascular hemiplegia.
        Eur Neurol. 1980; 19: 382-389
        • Dodds T.A.
        • Martin D.P.
        • Stolov W.C.
        • Deyo R.A.
        A validation of the functional independence measurement and its performance among rehabilitation in patients.
        Arch Phys Med Rehabil. 1993; 74: 531-536
        • Huang Y.Z.
        • Edwards M.J.
        • Rounis E.
        • Bhatia K.P.
        • Rothwell J.C.
        Theta burst stimulation of the human motor cortex.
        Neuron. 2005; 45: 201-206
        • Khedr E.M.
        • Etraby A.E.
        • Heneda M.
        • Nasef A.M.
        • Razek A.A.
        Long-term effect of repetitive transcranial magnetic stimulation on motor function recovery after acute ischemic stroke.
        Acta Neurol Scand. 2010; 121: 30-37
        • Malcolm M.P.
        • Triggs W.J.
        • Light K.E.
        • Gonzalez Rothi L.J.
        • Wu S.
        • Reid K.
        Repetitive transcranial magnetic stimulation as an adjunct to constraint-induced therapy: an exploratory randomized controlled trial.
        Am J Phys Med Rehabil. 2007; 86: 707-715
        • Stinear J.W.
        • Byblow W.D.
        Rhythmic bilateral movement training modulates corticomotor excitability and enhances upper limb motricity poststroke: a pilot study.
        J Clin Neurophysiol. 2004; 21: 124-131
        • Rossini P.M.
        • Barker A.T.
        • Berardelli A.
        • et al.
        Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee.
        Elctroencephalogr Clin Neurophysiol. 1994; 91: 79-92
        • Wolf S.L.
        • Thompson P.A.
        • Morris D.M.
        • et al.
        The EXCITE trial: attributes of the Wolf Motor Function Test in patients with subacute stroke.
        Neurorehabil Neural Repair. 2005; 19: 194-205
        • Sung W.H.
        • Wang C.P.
        • Chou C.L.
        • Chen Y.C.
        • Tsai P.Y.
        Efficacy of coupling inhibitory and facilitatory rTMS to enhance motor recovery in hemiplegic stroke patients.
        Stroke. 2013; 44: 1375-1382
        • Kantak S.S.
        • Stinear J.W.
        • Buch E.R.
        • Cohen L.G.
        Rewiring the brain: potential role of the premotor cortex in motor control, learning, and recovery of function following brain injury.
        Neurorehabil Neural Repair. 2012; 26: 282-292
        • Johansen-Berg H.
        • Rushworth M.F.
        • Bogdanovic M.D.
        • Kischka U.
        • Wimalaratna S.
        • Matthews P.M.
        The role of ipsilateral premotor cortex in hand movement after stroke.
        Proc Natl Acad Sci U S A. 2002; 99: 14518-14523
        • Ward N.S.
        • Newton J.M.
        • Swayne O.B.
        • et al.
        Motor system activation after subcortical stroke depends on corticospinal system integrity.
        Brain. 2006; 129: 809-819
        • Takahashi C.D.
        • Der-Yeghiaian L.
        • Le V.
        • Motiwala R.R.
        • Cramer S.C.
        Robot-based hand motor therapy after stroke.
        Brain. 2008; 131: 425-437
        • Conforto A.B.
        • Ferreiro K.N.
        • Tomasi C.
        • et al.
        Effects of somatosensory stimulation on motor function after subacute stroke.
        Neurorehabil Neural Repair. 2010; 24: 263-272
        • Borich M.R.
        • Wadden K.P.
        • Boyd L.A.
        Establishing the reproducibility of two approaches to quantify white matter tract integrity in stroke.
        Neuroimage. 2012; 59: 2393-2400
        • Sharma N.
        • Baron J.C.
        • Rowe J.B.
        Motor imagery after stroke: relating outcome to motor network connectivity.
        Ann Neurol. 2009; 66: 604-616