Correlates of disability in multiple sclerosis detected by transcranial magnetic stimulation

Objective To study the usefulness of corticospinally mediated excitatory responses and transcallosal inhibition (TI) elicited by transcranial magnetic stimulation (TMS) as a surrogate marker of disability in patients with different courses of MS. Methods Focal TMS of the motor cortex was performed in 118 patients with MS (96 with relapsing-remitting, 19 with primary progressive, and three with secondary progressive disease) who had an Expanded Disability Status Scale (EDSS) score between 0 and 6.5 and in 35 normal subjects. Central motor latencies (CML) and TI (onset latency, duration) were investigated. The Spearman rank correlation was used for statistical analysis. Results TMS disclosed prolonged CML in 52.5% and abnormal TI in 61% of the patients. In all patients the EDSS correlated with the frequency of abnormal TI (r = 0.58, p < 0.01) and abnormal CML (r = 0.51, p < 0.01). In patients with primary progressive MS (EDSS 1.5 to 6.5) the frequency of TI abnormalities correlated with EDSS (r = 0.65, p < 0.01) whereas CML did not. Delayed corticospinal responses in hand muscles always led to abnormal TI. Conclusions The combination of central motor latencies and transcallosal inhibition evoked by transcranial magnetic stimulation yields objective data to estimate disease progression in MS as assessed by the EDSS.

[1]  L. Kappos,et al.  Evoked potentials for evaluation of multiple sclerosis , 2001, Clinical Neurophysiology.

[2]  L. Kappos,et al.  Visual and motor evoked potentials in the course of multiple sclerosis. , 2001, Brain : a journal of neurology.

[3]  A. Compston,et al.  Recommended diagnostic criteria for multiple sclerosis: Guidelines from the international panel on the diagnosis of multiple sclerosis , 2001, Annals of neurology.

[4]  M. Kean,et al.  Clinical and neuroradiologic features of acute disseminated encephalomyelitis in children , 2001, Neurology.

[5]  R. Grossman,et al.  ADEM , 2001, Neurology.

[6]  M. Tsai,et al.  The spectrum of postinfectious encephalomyelitis , 2001, Brain and Development.

[7]  E. Wijdicks,et al.  Full recovery after acute hemorrhagic leukoencephalitis (Hurst's disease) , 2000, Journal of Neurology.

[8]  B. Harding,et al.  Acute disseminated encephalomyelitis, multiphasic disseminated encephalomyelitis and multiple sclerosis in children. , 2000, Brain : a journal of neurology.

[9]  J. Saint-Cyr,et al.  Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson's disease. , 2000, Brain : a journal of neurology.

[10]  J. Saint-Cyr,et al.  Neuropsychologic assessment of patients for movement disorder surgery , 2000, Movement disorders : official journal of the Movement Disorder Society.

[11]  A J Thompson,et al.  Diagnostic criteria for primary progressive multiple sclerosis: A position paper , 2000, Annals of neurology.

[12]  L. Leocani,et al.  Neurophysiological investigations in multiple sclerosis. , 2000, Current opinion in neurology.

[13]  Shoshana Revel-Vilk,et al.  Recurrent Acute Disseminated Encephalomyelitis Associated With Acute Cytomegalovirus and Epstein-Barr Virus Infection , 2000, Journal of child neurology.

[14]  R. Rust Multiple sclerosis, acute disseminated encephalomyelitis, and related conditions. , 2000, Seminars in pediatric neurology.

[15]  J. Rothwell,et al.  The impact of deep brain stimulation on executive function in Parkinson's disease. , 2000, Brain : a journal of neurology.

[16]  S. Röricht,et al.  Conduction deficits of callosal fibres in early multiple sclerosis , 2000, Journal of neurology, neurosurgery, and psychiatry.

[17]  L. Lacritz,et al.  Neuropsychological Outcome Following Unilateral Stereotactic Pallidotomy in Intractable Parkinson's Disease , 2000, Brain and Cognition.

[18]  Anthony E. Lang,et al.  Neuropsychological Outcome of GPi Pallidotomy and GPi or STN Deep Brain Stimulation in Parkinson's Disease , 2000, Brain and Cognition.

[19]  B. Schmand,et al.  Unilateral pallidotomy in PD , 2000, Neurology.

[20]  Kenneth Hugdahl,et al.  Neurocognitive Correlates of Stereotactic Thalamotomy and Thalamic Stimulation in Parkinsonian Patients , 2000, Brain and Cognition.

[21]  Mark D. Johnson,et al.  The Role of the Human Thalamus in Language and Memory: Evidence from Electrophysiological Studies , 2000, Brain and Cognition.

[22]  P. Strick,et al.  Basal Ganglia Output and Cognition: Evidence from Anatomical, Behavioral, and Clinical Studies , 2000, Brain and Cognition.

[23]  K. R. Mills,et al.  Magnetic Stimulation of the Human Nervous System , 2000 .

[24]  P. Bossuyt,et al.  A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. , 2000, The New England journal of medicine.

[25]  Marco Rovaris,et al.  The role of magnetic resonance in the assessment of multiple sclerosis , 2000, Journal of the Neurological Sciences.

[26]  W Lang,et al.  Bilateral subthalamic nucleus stimulation improves frontal cortex function in Parkinson's disease. An electrophysiological study of the contingent negative variation. , 1999, Brain : a journal of neurology.

[27]  R. Grossman,et al.  Neuropsychological outcome following unilateral pallidotomy. , 1999, Brain : a journal of neurology.

[28]  M. Miyao,et al.  Acute relapsing encephalopathy mimicking acute necrotizing encephalopathy in a 4-year-old boy , 1999, Brain and Development.

[29]  A. Tröster,et al.  Neuropsychological and quality of life outcome after thalamic stimulation for essential tremor , 1999, Neurology.

[30]  E. Tolosa,et al.  Cognitive and behavioral changes after unilateral posteroventral pallidotomy: Relationship with lesional data from MRI , 1999, Movement disorders : official journal of the Movement Disorder Society.

[31]  I. Saatci,et al.  A case of relapsing acute disseminated encephalomyelitis with high dose corticosteroid treatment , 1999, Brain and Development.

[32]  E. Kunesch,et al.  Demyelination and axonal degeneration in corpus callosum assessed by analysis of transcallosally mediated inhibition in multiple sclerosis , 1999, Clinical Neurophysiology.

[33]  Ludwig Kappos,et al.  Predictive value of gadolinium-enhanced magnetic resonance imaging for relapse rate and changes in disability or impairment in multiple sclerosis: a meta-analysis , 1999, The Lancet.

[34]  Guy Vingerhoets,et al.  Cognitive outcome after unilateral pallidal stimulation in Parkinson’s disease , 1999, Journal of neurology, neurosurgery, and psychiatry.

[35]  R. Baloh,et al.  Motor, cognitive, and behavioral performance following unilateral ventroposterior pallidotomy for Parkinson disease. , 1998, Archives of neurology.

[36]  O. Devinsky,et al.  Cognitive functioning after pallidotomy for refractory Parkinson’s disease , 1998, Journal of neurology, neurosurgery, and psychiatry.

[37]  J. Saint-Cyr,et al.  Neuropsychological consequences of posteroventral pallidotomy for the treatment of Parkinson's disease , 1998, Neurology.

[38]  M Hallett,et al.  Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract , 1998, The Journal of physiology.

[39]  B. Day,et al.  Central motor conduction time in progressive multiple sclerosis. Correlations with MRI and disease activity. , 1998, Brain : a journal of neurology.

[40]  F. Barkhof,et al.  Brain and spinal cord abnormalities in multiple sclerosis. Correlation between MRI parameters, clinical subtypes and symptoms. , 1998, Brain : a journal of neurology.

[41]  T. Aziz,et al.  Neuropsychological, neurological and functional outcome following pallidotomy for Parkinson's disease. A consecutive series of eight simultaneous bilateral and twelve unilateral procedures. , 1998, Brain : a journal of neurology.

[42]  S. Röricht,et al.  Topography of fibers in the human corpus callosum mediating interhemispheric inhibition between the motor cortices , 1998, Annals of neurology.

[43]  J. Lindeboom,et al.  Reading ability as an estimator of premorbid intelligence: does it remain stable in emergent dementia? , 1998, Journal of clinical and experimental neuropsychology.

[44]  A. Polizzi,et al.  Thalamic Syndrome in Children With Measles Infection and Selective, Reversible Thalamic Involvement , 1998, Pediatrics.

[45]  N. Rosman,et al.  Acute Hemorrhagic Leukoencephalitis: Recovery and Reversal of Magnetic Resonance Imaging Findings in a Child , 1997, Journal of child neurology.

[46]  C. Adler,et al.  Unilateral pallidotomy for Parkinson's disease: Comparison of outcome in younger versus elderly patients , 1997, Neurology.

[47]  A. Tröster,et al.  Unilateral pallidal stimulation for Parkinson's disease: Neurobehavioral functioning before and 3 months after electrode implantation , 1997, Neurology.

[48]  J. Delavelle,et al.  Early high-dose intravenous methylprednisolone in acute disseminated encephalomyelitis: A successful recovery , 1997, Neurology.

[49]  Richard S. J. Frackowiak,et al.  Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson's disease , 1997, Annals of neurology.

[50]  N. Fejerman,et al.  4-13-12 Multiphasic disseminated encephalomyelitis and multiple sclerosis in children: Diagnostic clues , 1997, Journal of Neurological Sciences.

[51]  H. Nauta,et al.  Cognitive sequelae of unilateral posteroventral pallidotomy. , 1997, Archives of neurology.

[52]  A J Thompson,et al.  PRIMARY PROGRESSIVE MULTIPLE SCLEROSIS , 1997 .

[53]  M. Mizuguchi Acute necrotizing encephalopathy of childhood: a novel form of acute encephalopathy prevalent in Japan and Taiwan , 1997, Brain and Development.

[54]  H. Lüders,et al.  Empirical methods for assessing meaningful neuropsychological change following epilepsy surgery , 1996, Journal of the International Neuropsychological Society.

[55]  M. Tsai,et al.  Multiphasic disseminated encephalomyelitis mimicking multiple sclerosis , 1996, Brain and Development.

[56]  R. Turner,et al.  Treatment of advanced Parkinson's disease by posterior GPi pallidotomy: 1‐year results of a pilot study , 1996, Annals of neurology.

[57]  A. Thompson,et al.  Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. , 1996, Brain : a journal of neurology.

[58]  K. Hugdahl,et al.  Cognitive function in patients with Parkinson's disease undergoing stereotaxic thalamotomy. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[59]  S. Reingold,et al.  Defining the clinical course of multiple sclerosis , 1996, Neurology.

[60]  D. Enzmann,et al.  Intravenous gammaglobulin therapy in recurrent acute disseminated encephalomyelitis , 1996, Neurology.

[61]  S. Beer,et al.  Diagnostic value of paraclinical tests in multiple sclerosis: relative sensitivities and specificities for reclassification according to the Poser committee criteria. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[62]  M. Mizuguchi,et al.  Acute necrotising encephalopathy of childhood: a new syndrome presenting with multifocal, symmetric brain lesions. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[63]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

[64]  B. Yaqub,et al.  Multiphasic disseminated encephalomyelitis presenting as alternating hemiplegia. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[65]  M. Freedman,et al.  Heat shock protein immunoreactivity in CSF , 1994, Neurology.

[66]  R. R. Smith,et al.  MRI in acute disseminated encephalomyelitis , 1994, Neuroradiology.

[67]  E. Bertini,et al.  Bilateral, Reversible, Selective Thalamic Involvement Demonstrated by Brain MR and Acute Severe Neurological Dysfunction with Favorable Outcome* , 1994, Neuropediatrics.

[68]  G. Francis Large focal tumor‐like demyelinating lesions of the brain , 1993, Annals of neurology.

[69]  D. Kömpf,et al.  Long-latency reflexes, somatosensory evoked potentials and transcranial magnetic stimulation: relation of the three methods in multiple sclerosis. , 1993, Electroencephalography and clinical neurophysiology.

[70]  E. Thompson,et al.  The significance of serum oligoclonal bands in neurological diseases. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[71]  P. Sørensen,et al.  The diagnostic reliability of magnetically evoked motor potentials in multiple sclerosis , 1992, Neurology.

[72]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[73]  G. Davies-Jones,et al.  The role of magnetic stimulation as a quantifier of motor disability in patients with multiple sclerosis , 1991, Journal of the Neurological Sciences.

[74]  D. Seales,et al.  Acute hemorrhagic leukoencephalitis. A successful recovery. , 1991, Archives of neurology.

[75]  B. Shahani,et al.  Hemispheric threshold differences for motor evoked potentials produced by magnetic coil stimulation , 1991, Neurology.

[76]  R. Knobler,et al.  Lower extremity motor evoked potentials in multiple sclerosis. , 1991, Archives of neurology.

[77]  L. Deecke,et al.  The sensitivity of transcranial cortical magnetic stimulation in detecting pyramidal tract lesions in clinically definite multiple sclerosis , 1991, Neurology.

[78]  K J Rothman,et al.  No Adjustments Are Needed for Multiple Comparisons , 1990, Epidemiology.

[79]  M. Lana-Peixoto,et al.  Schilder's myelinoclastic diffuse sclerosis. , 1989, Journal of clinical neuro-ophthalmology.

[80]  C. Marsden,et al.  Internal versus external cues and the control of attention in Parkinson's disease. , 1988, Brain : a journal of neurology.

[81]  M. Swash,et al.  Central motor conduction in multiple sclerosis: evaluation of abnormalities revealed by transcutaneous magnetic stimulation of the brain. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[82]  J. Whitaker,et al.  Cranial MRI in acute disseminated encephalomyelitis , 1988, Neurology.

[83]  K. Mills,et al.  Magnetic brain stimulation: Central motor conduction studies in multiple sclerosis , 1987, Annals of neurology.

[84]  J. Wolinsky,et al.  Measles encephalomyelitis--clinical and immunologic studies. , 1984, The New England journal of medicine.

[85]  J. Kurtzke Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[86]  D. Silberberg,et al.  New diagnostic criteria for multiple sclerosis: Guidelines for research protocols , 1983, Annals of neurology.

[87]  E K Warrington,et al.  Testing for nominal dysphasia. , 1980, Journal of neurology, neurosurgery, and psychiatry.

[88]  D. D. De Vivo,et al.  Steroid‐responsive encephalomyelitis in childhood , 1980, Neurology.

[89]  H. Hacker,et al.  Bilateral reversible thalamic lesions on computed tomography , 1979, Neuroradiology.

[90]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[91]  R O Barnard,et al.  Corpus callosum in multiple sclerosis , 1974, Journal of neurology, neurosurgery, and psychiatry.

[92]  E. Hurst Acute Haemorrhagic Leucoencephalitis: a previously Undefined Entity. , 1941 .

[93]  T. Abe,et al.  Relapsing acute disseminated encephalomyelitis associated with chronic Epstein-Barr virus infection: MRI findings , 2004, Neuroradiology.

[94]  J. Ridley Studies of Interference in Serial Verbal Reactions , 2001 .

[95]  C R Guttmann,et al.  A longitudinal study of callosal atrophy and interhemispheric dysfunction in relapsing-remitting multiple sclerosis. , 2001, Archives of neurology.

[96]  W. Weiner Parkinson’s Disease and Movement Disorders , 2000, Current Clinical Practice.

[97]  P M Matthews,et al.  Axonal injury or loss in the internal capsule and motor impairment in multiple sclerosis. , 2000, Archives of neurology.

[98]  L. Leocani,et al.  Evoked potentials in diagnosis and monitoring of multiple sclerosis. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[99]  B. Meyer,et al.  First diagnostic applications of transcallosal inhibition in diseases affecting callosal neurones (multiple sclerosis, hydrocephalus, Huntington's disease). , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[100]  S. Reingold,et al.  The role of magnetic resonance techniques in understanding and managing multiple sclerosis. , 1998, Brain : a journal of neurology.

[101]  K. Hugdahl,et al.  Thalamotomy and thalamic stimulation: effects on cognition. , 1997, Stereotactic and functional neurosurgery.

[102]  R. Reitan Trail Making Test: Manual for Administration and Scoring , 1992 .

[103]  J. Valk,et al.  Acute Disseminated Encephalomyelitis and Acute Hemorrhagic Encephalomyelitis , 1989 .

[104]  C. Marsden,et al.  Recent Developments in Parkinson's Disease , 1986 .

[105]  F. Roncaroli,et al.  Neuropathology of multiple sclerosis , 2012 .

[106]  M. Lorr,et al.  Manual for the Profile of Mood States , 1971 .