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					 Cercetãri Experimentale & Medico-Chirurgicale

 Anul XIV · Nr.2-3/2007 · Pag. 98-103                                                                    Cercetari
                                                                                                         e x p e r i m e n ta le &
                                                                                                         m edico-chirurgicale

Sîrbu Elena1                           SUMMARY:The work hypothesis starts from the idea that neurophysiologic investigations
                                       (motor and somatosensory evoked potentials) early applied in the first days of cerebral
                                       ischemia can bring important and useful information about the recovery potential of the
                                       hemiplegic patient. We studied 100 hemiplegic patients with ischemic stroke which were
                                       admitted in Neurological Department of Brugmanns Hospital in Brussels and a group of 50
                                       healthy subjects. All subjects performed transcranial magnetic stimulation (TMS) and we
                                       recorded the motor evoked responses (MEP) from tibialis anterior muscle. Somatosensory
                                       evoked potentials (SEP) were recorded performing an electrical stimulation of the median
                                       nerve at the radioulnar joint. Clinical evaluation were performed at day 1 (index 1) and after
                                       45 days (index 2) by the motricity index”.We have noticed a significant improvement in the
                                       otricity index at the patients with present MEP responses between the two evaluations
                                       (p<0.001). The presence of a somatosensory evoked potential didn’t influence the motor
                                       recovery of the patients studied here (p>0,05).MEP is a better prognostic indicator for
                                       motor recovery than SEP, with the condition to be present in the first seven days after the
                                       onset of stroke.
                                       Key Words: transcranial magnetic stimulation, motor evoked potentials, somatosensory
                                       evoked potentials, ischemic stroke, recovery, hemiplegia

                                       RECUPERAREA ISCHEMIEI CEREBRALE

                                       REZUMAT: Ipoteza de lucru porneºte de la ideea cã tehnicile de neurofiziologie
                                       (potenþialele evocate motorii ºi somestezice) aplicate timpuriu, în primele zile poststroke,
                                       pot aduce informaþii deosebit de utile privind potenþialul recuperator al bolnavilor
                                       hemiplegici.Am luat în studiu un lot de 100 de pacienþi hemiplegici cu accident vascular
                                       ischemic internaþi pe secþia de neurologie a spitalului Brugmann din Bruxelles ºi un lot
                                       martor ce cuprinde 50 de subiecþi sãnãtoºi. Ambele loturi au fost supuse unui procedeu de
                                       stimulare magneticã transcranianã (TMS) înregistrându-se rãspunsurile motorii evocate
                                       (PEM) la nivelul muºchiului tibial anterior. Potenþialul evocat somestezic (PES) presupune
                                       stimularea nervului median la nivelul articulaþiei radiocarpiene ºi m surarea rãspunsului
                                       electric progresiv ascendent de-a lungul tractului nervos activat. Cu ajutorul „indicelui
                                       motor” pacienþii au fost evaluaþi clinic, iniþial (index 1) ºi final la 45 de zile de la începerea
                                       tratamentului recuperator (index 2). Din studiul comparativ privind evoluþia indicelui motor
                                       la nivelul muºchiului tibial anterior, înainte ºi dupã tratament, se constantã o ameliorare
                                       semnificativã a acestuia în urma recuperãrii neuromotorii (p< 0,001). Evoluþia indicelui
Received for publication: 05.08.2007
                                       motor este semnificativ mai bunã la bolnavii hemiplegici cu rãspuns motor prezent la nivelul
Revised: 11.09.2007
                                       muºchiului tibial anterior. Potenþialul evocat somestezic, nu a influenþat semnificativ
                                       posibilitatea de recuperare motorie a bolnavilor incluºi în studiu (p>0,05).PEM are valoare
                                       prognosticã în recuperarea neuromotorie a bolnavilor hemiplegici, cu condiþia sã fie prezent
                                       în primele 7 zile poststroke. PEM este un indicator mai relevant decât PES în sensul
                                       evoluþiei favorabile.

 1- Laboratory of Clinical Neurophysiology, CHU Brugmann, Belgium

Correspondence to: Elena Sirbu PhD, Department of Physiotherapy , West University of Timiºoara, Romania, Bd. V. Parvan
4, 1900 Timisoara, Phone: +40-727-213034; Fax: +40-256-496092,Laboratory of Clinical Neurophysiology, CHU Brugmann,
Place Van Gehuchten 4, 1020 Brussels, Belgium, Email:

                                                              one patients had a right-sided lesion and fourthy nine a
INTRODUCTION                                                  left-sided lesion.
                                                                 The site of lesion was cortical in 19 patients,
    Ischemic stroke is the most frequent cerebral vascular
                                                              corticosubcortical in 45 patients and subcortical in 36
affection, with the most severe and complex satchels,
affecting the quality of life and the work capacity.
                                                                 The patients were not receiving any drugs interfering
Cerebrovascular accident (CVA) represents nowadays
                                                              with cortical excitability. During their stay in the
the third cause of death after cardiac affections and
                                                              rehabilitation unit, they underwent physiotherapeutic
cancer. It is the first cause of neurological handicap
                                                              treatment performed twice daily by the same
especially in old people (1).
    In the management of stroke patients, it could be
                                                                 The control group consisted of 50 healthy subjects (30
important to obtain an early indication that a significant
                                                              women, 20 men) aged from 25 to 89 years (mean 57).
motor recovery will occur. This would be an advantage
for planning rehabilitation and for patient motivation.         Clinical assessment
    In the past, prediction of motor recovery has been           Two evaluation of the muscle power in the affected
based only on clinical examination. The degree of initial     lower limb were performed during the study using the
motor deficit was found to be the most important              “motricity index” (MI) (2).
determinant of motor and functional recovery. There may          Muscle power was assessed for ankle dorsiflexion,
be other tests which can provide valuable information in      knee extension and hip flexion while patient was sitting.
patients with a moderate deficit. The measurement of          This provided a weighted score ranging from 0 (no
somatosensory and motor evoked potentials, for                muscle power) to 100 (normal muscle power).
example, is a method of assessing the integrity of               Evaluations were performed before starting the
sensory and motor pathways of the nervous system              recovery program at day 1 (index 1), being then
 ( 4,15).                                                     reevaluated after 45 days (index 2). The gain in muscle
    Several studies have examined the value of                strength as recovery rating was calculated as index2 -
somatosensory evoked potentials (SEP) in the prediction       index1
of functional recovery (15,16).
    The recent development of a non-invasive method of
                                                                Neurophysiological examination
transcranial magnetic stimulation (TMS) allows to study    Neurophysiologic assessments were performed
                                                        within the first week from stroke onset.
the excitability of the motor cortex and to investigate the
function of descending motor pathways (7).                 Transcranial magnetic stimulation (TMS) was
    TMS has been proposed to predict motor recovery     performed with a circular coil (90 mm diameter)
after stroke but the results are still contradictory,   connected to a Magstim 200 (2 Tesla).
probably because of the greatest variability of patients   The coil was placed over the vertex, slightly away
included and differences in the methodologies used.     from the midline to activate the motor cortex and laterally
                                                        over the C7 spinal process to activate the ventral roots.
    According to most of the authors clinical signs usually
correlate with electrophysiological findings. They      Stimuli were given on both sides with increasing
observed that persistent responses to TMS in the acute  intensity until potentials of the largest amplitude and
                                                        shortest latency were obtained. The stimulus intensity
phase of stroke are an indicator of good recovery (10,12).
                                                        was set at 100% power to all patients (5).
    The aim of this paper is to determine the relationship
between motor recovery and the degree of motor               Motor responses evoked (MEP) by TMS were
disabilities, as ascertained with motor or somatosensoryrecorded by surface electrodes fixed over the tibialis
evoked potentials.                                      anterior muscle on the affected side. All MEP responses
                                                        from the cortical and cervical stimulation were recorded
PATIENTS AND METHODS                                    and displayed on the screen of the Nicolet Viking IV
                                                        device. The results of MEP responses were later printed
                                                        out on A4 paper so that calculation of the central motor
   We studied 100 hemiplegic patients with ischemic
                                                        time conduction (CMCT) could be performed. The CMCT
stroke which were admitted in Neurological Department
                                                        was provided by subtraction of the longest cervical
of Brugmanns Hospital in Brussels from 2004 to 2006.
                                                        latency from the shortest cortical latency.
The patient’s age was 49-84 years; the mean was 69
years. There were 48 female and 52 male patients. Fifty

   The somatosensory evoked potentials (SEP) were
recorded performing an electrical stimulation of the                   80
median nerve at the radioulnar joint. The stimulus rate                70

was 5 Hz and the stimulus intensity that elicited a visible            60         53,11
twitch of the thumb muscles was used. Electrodes were                  50

placed over Erb’s point, the seventh cervical vertebra and             40

contralateral somatosensory areas. The reference                       30

electrode was placed at Fz (frontal scalp electrode). The              20

evoked potentials were obtained by averaging the                       10

recordings of 500 stimuli (9).                                          0
                                                                                  Index 1                     Index 2
   The absolute latencies for N11-N13 complex obtained
from the cervical channel and N20 obtained from the
                                                              Figure 1. Mean scores of the “motricity index” at day 1 and after
scalp channel were determined. N13 to N20 interpeak           45 days (p < 0.001). Index 1 = first clinical evaluation, Index 2 =
latency is regarded as central conduction time                second clinical evaluation
measuring from the cervical cord to the sensory cortex
                                                             A longer mean CMCT was found in the affected side of
                                                          the stroke patients compared with data recorded from
   Statistical analysis                                   the left or right sides of the healthy subjects (p< 0.05)
   Statistical analysis were performed using the (Figure 4).
Statistical Package for the Social Sciences statistical      MEP in response to magnetic stimulation were
package (SPSS)(6).                                        present in the tibialis anterior muscles in 66 of our 100
   The independent t test (two-tailed) was used to stroke patients. In the other 34 patients we didn noticed
compare two means and in particular when those means
come from different groups of subjects. Student’s t test
for paired data (two-tailed) was used for the comparison
of the mean values in each group of patients.                   16             14,978

   A Levene’s test was done before in order to assess the       14
equality of variances.
   Values of p<0,05 were considered significant.


   All patients included in this study were assessed
before starting the recovery program at day 1. The mean
score of the motricity index (index 1) was 53.11 0.93 .
                                                                                 CMCT left                  CMCT right
   They were reevaluated after 45 days and the mean
value of the motricity index (index 2) was 70.54 7.65.        Figure 2. Differences in means scores of CMCT in the control
The recovery rating calculated as index2 - index1 was            group (p>0.05).
17.43 (Figure 1). These results indicate that a significant
recovery in motor function occurs 45 days after the onset               18                                    16,768
of stroke (p < 0,001).                                                  16
   TMS tests were performed on both sides on 50 healthy
subjects and we measured their CMCT and amplitude of                               11,753

motor response. These data were compared with data of
CMCT and amplitude of motor response recorded from
100 stroke patients.                                                        8

   No significant difference in mean of CMCT was found                      6

between the left and right sides in the group of healthy                    4
subjects (p>0.05). However, we observed for all stroke                             CMCTa                      CMCTu

patients a significant difference in mean of CMCT             Figure 3. Differences in means scores of CMCT in stroke
between the affected and the unaffected side (p<0.05)            patients (p< 0.05)
(Figure 2, 3).

any response in the affected muscles after cortical              present MEP at day 1 (Figure 5). These findings suggest
stimulation.                                                     that MEP is useful as a prognostic indicator of clinical
   We have noticed a significant improvement in the              outome in ischemic stroke patients.
otricity index especially at the patients with present              Median somatosensory evoked potentials (SEP) were
motor responses (p<0.05).                                        investigated in our stroke patients within 7 days of onset.
   According to tibialis anterior recordings, we observed        We recorded present SEP responses in 56 of our 100
a better clinical outcome in patients in whom there was a        stroke patients.

Figure 4. Mean values of CMCT in stroke patients and control group (p< 0.05)

 Figure 5. Mean values of motricity index (MI) according to MEP in the responsive and nonresponsive groups (p<0.05)

    The presence of a somatosensory evoked potential have a high probability of good stroke outcome. Similar
didn’t influence the motor recovery of the patients findings were observed in other studies (11,12).
studied here (p>0.05) .                                          Another finding was the delayed CMCT observed on
                                                              the affected side of the stroke patients which was
DISCUSSION                                                    significant greater compared to data recorded from the
    The results of this study show that there is a close left or right sides of the healthy subjects. Moreover, we
relationship between motor recovery and the degree of observed a significant difference in mean of CMCT
motor disabilities, as ascertained with motor or between the affected and the unaffected side of the
somatosensory evoked potentials. The capacity to stroke patients.
recover motor function is one of the most important              These data confirm that nerve conduction through the
considerations for the stroke patient.                        central motor pathway is severely affected by ischemic
    MEPs in response to magnetic stimulation were stroke.
analysed in this study. The technique of TMS is easy to          The measurement of somatosensory evoked
perform, rapid, safe and painless. It provides objective      potentials (SEP) is an objective and direct method of
and reliable data. A lot of studies have indicated that the assesing the integrity of sensory pathways of the central
persistence of MEP responses in the acute phase is an nervous system and is extremely useful in clinical
indicator of good recovery. However, other studies practice. The prevailing option is that they do contribute
reported no significant predictive value of MEP in the to prediction of functional recovery. Other authors
acute stage of hemiplegia (11,14).                            concluded that SEP have no value in predicting outcome
    We believe that most studies were conducted on of hemiparesis (3).
heterogeneous groups of patients (distinct types of              In our study we recorded a present somatosensory
strokes, various degree of motor deficit), and the first      response in 56 of our 100 stroke patients. The presence
magnetic stimulation was performed at various delays of a somatosensory evoked potential didn’t influence the
after stroke onset. Moreover, the clinical rating scales motor recovery of the patients studied here.
used were different and subjects were assessed at                So, we conclude that somatosensory evoked
various delays after stroke. That is why the conclusions potentials measured in the acute phase of stroke have no
were not always convergent.                                   value in predicting motor recovery. We believe that SEP
    In our study, all the patients presented similar aspects: is useful in predicting the functional recovery but it is not
first ischemic stroke due to middle cerebral artery infarct, a prognostic factor for motor outcome.
electrophysiological testing performed within the first          In support of the prognostic value of this technique it
week from stroke onset, clinical assessments at day 1 would be preferable to introduce functional assessment
were repeated after 45 days.                                  scales which evaluates most activity of daily living.
    After the second evaluation, all patients presented a        However, it has been reported that MEP are more
better clinical outcome (motricity index) and a significant sensitive than SEP in predicting motor recovery (3).
recovery in motor function. This result confirmed the            Finally, our results indicate that in the acute phase, the
importance of a recovery program and the necessity of an combination of the motor score (motricty index) and
early rehabilitation in the management program of any MEPSs were best able to predict motor recovery in stroke
hemiplegic patient. Similar findings were observed by patients. The SEP did not add significant informations.
other authors (8,13).                                         This finding is valuable in rehabilitation planning. It helps
    There is a close relationship between clinical and therapists to set realistic goals for the treatment of each
electro-physiological parameters, and the presence of patient and to determine how much rehabilitation effort
motor responses in the affected muscles predicted better should spent in the group of patiens who show an
recovery than in its absence (10). In our study, MEP in extremly poor prognosis.
response to magnetic stimulation were present in the
tibialis anterior muscle in 66 of our 100 stroke patients.
   We have found a significant improvement in the             According to the obtained results I present some
motricity index at the patients that presented MEP important conclusions about the aspects I found very
responses. Significant values of the t tests indicated that important:
patients with MEP responses in the acute phase of stroke      n The recovery program must obligatory be included

                                                                 in the management program of any patient with

      ischemic stroke, it must be started early and                  n   The rehabilitation activity consists in a team work,
      continued daily with follow-ups at variable periods                in which everybody has a well established role and
      from months to years.                                              by the same importance: neurologists,
  n   We have noticed a significant intervention of an                   physiotherapists, psychotherapists, nurse and
      early kinetic intervention after the onset of stroke.              social assistants, occupational therapists.
  n   MEP represents a prognostic indicator for motor                n   The patients’ active participation to the
      recovery with the condition to be present in the first             neurorecovery programs represents a chance for
      seven days after the onset of stroke. MEP is a better              rehabilitation and in the same time it assures the
      prognostic factor than SEP, meaning that the                       reduction of the recurrent CVA risk.
      evolution is more favorable.
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15. Tzvetanov P., Rousseff R.T., Atanassova P., Prognostic value of median and tibial somatosensory evoked potentials in
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                                               TO WHOM IT MAY CONCERN
                                                   Brussels. 1st Augustus 2007

                                                I, understanding Prof. Paul Deltenre, Head
                        of the Neurology Dept of the Brugmann University Hospital, hereby
                        allows Dr. Elena SIRBU to use the neurophysiological data
                        ( somatosensory and motor evoked potentials ) that she contributed to
                        acquire in our department for a scientific publication under her name.

                                                                                     Prof. Paul Deltenre


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