INTRODUCTION
Impaired walking is one of the main functional problems
that the physiotherapist encounters in caring for neurologically impaired
patient. Many factors could affect the ability to walk such as range of motion
(ROM), posture, bony alignment, muscle power, motor control, coordination,
sensation and balance1. The temporal aspects of the hemiplegics gait
are characterized by increased cycle time, reduced walking velocity, and
reduced cadence and altered stance and swing phase periods2,3. The
results of stroke vary widely depending on the size and location of the lesion.
Synaptic wisdom in neural networks with
homeostatic processes appears to prevent over- and under-excitability4.
The two cerebral hemispheres are functionally coupled and balanced as
the motor cortex trans-callosal interactions are mainly inhibitory5.
After stroke, the unaffected hemisphere is dis-inhibited. This in turn may
increase inhibition of the affected hemisphere and could impair functional
recovery6.
Modulation
of motor cortex activity -as the changes of cortical excitability of one
hemisphere- is known to be accompanied by a modulation of excitability of
homonymous regions of the contralateral hemisphere. The modulation of the
corticospinal excitability caused by rTMS depends on the frequency, as high
frequency rTMS is reported to increase the corticospinal excitability while low
frequency rTMS lead to decrease its excitability7-10.
Low frequency rTMS to the unaffected hemisphere showed significant
decrease in simple and choice reaction time of the affected hand in stroke
patients11. Low intensity rTMS reduces inter-hemispheric inhibition
in both directions but is predominantly from the stimulated to the unstimulated
hemisphere12. Spasticity could be modified by the stimulation of
either the affected or the unaffected hemisphere, but the induction of movement
could be achieved only by the stimulation of an intact motor pathway and its
surrounding area, also the improvement in paretic extremities can be achieved
with rTMS even after years of stroke when traditional rehabilitation has failed13.
High frequency rTMS of 10 Hz on the affected hemisphere resulted in significant
large increase in motor evoked potential amplitude and enhanced motor performance
accuracy14. The combination between rTMS and maximal movement effort
of the hemiplegic hand was noticed to improve manual performance and to reduce
wrist flexor spasticity15.
Aim of work: Low
rate rTMS assumed to help gait rehabilitation as well as EEG synchronization
after stroke. Are these two variables correlated?
MATERIAL AND METHODS
This
study was carried out on forty-five adult stroke patients of both sexes (16
males and 14 females) ranging in age from 40 to 60 years. Selection of the patients
was based on careful history taking and clinical examinations. The diagnosis
was confirmed by CT or MRI of the brain. Stroke diagnosis was made by the
treating physician according to the WHO definition of stroke "to exclude
TIAs"16.
Patients
were selected to have left sided hemiplegia due to cerebrovascular accident
(CVA) affecting frontal and/or parietal lobes, medically stable with
mini-mental test score17 not less than 24, mild degree of spasticity
(grade 1 to 1+ according to modified Ashworth scale)18.
Their duration of illness was not more than three months.
Patients
with other neurological (Parkinsonism) or severe orthopedic disorders (unstable
fractures), joints deformities or contractures, balance disturbance and
recurrent stroke were excluded from the study.
Subject's eligibility to participate in the study was based
on screening by the principal investigator or by the treating physical
therapist at the participating location. The therapy protocol was fully
clarified to the patient before his or her consent to participate in the study.
This study has the approval of the ethical committee of the Faculty of
Medicine, Cairo University.
Those
patients were classified into two groups; study group formed of thirty patients
(Group A) receiving physical therapy and rTMS and control group formed of
fifteen patients (Group B) receiving physical therapy only.
The
treatment policy was applied three times per week for six successive weeks
(total of 18 sessions). Physical therapy program was including the following:
prolonged stretch (Bobath approach)19, strengthening exercises for
the hip20, for the back and abdominal muscles21, balance
training and gait training exercises22. This program took
approximately one hour (not less than thirty minutes).
For
group (A) immediately after physiotherapy the patient lies on a motorized bed
and the cranial solenoid of the rTMS was positioned to the left hemisphere
while the whole head of the patient was centered inside in the middle area (Figure
1). The intensity was set to 2 G,
the frequency was 1 Hz for 20 minutes. The machine used was ASA Magnetic Field
for rTMS. It consists of an appliance, motorized bed and solenoids. Frequency
of the output impulse ranged from 0.5 to 1 Hz, and its intensity is displayed
in percentage form, from 5% to 100% of the maximum layout of the solenoid used;
the maximum intensity in G depending on the solenoid used "cranial
solenoid maximum intensity is 80
G.
The
following evaluation tests were done for each patient at the entry of the study
and after the end of the treatment program: Muscle tone assessment to estimate
the amount of resistance that is felt according to modified Ashworth's scale.
Cadence can be measured calculating the number of steps per minutes (through
dividing number of steps in a designated distance on time)23. Timed
“up and go” test (TUG) in which the patient was asked to get up from a chair,
walk three meters, turn, walk back and sit down again. A stopwatch was used to
calculate the time of each trial and record it in seconds. The subjects
received no score if they were unable to complete the test or required
assistance to refrain from falling during the test24,25. Fugl-Meyer
assessment scale (FMA) was used to measure the sensorimotor recovery after
stroke26. Quantitative Electroencephalogram (QEEG) was used – in
group A only- to measure the electrical activity of both hemispheres in the
form of relative power spectrum represented by the percentage of each band’s
amplitude compared to the total amplitude of all frequency bands. Schwarzer
Brain lab4 GmbH machine was used for recording 20 minutes of artifact free
digital EEG. Full cap (19 electrodes) was applied according to the
international 10/20 electrode placement system to record the following
frequency bands; delta (1-3 Hz), theta (4-7 Hz), alpha (8-12 Hz) and beta waves
(13-16Hz). 5 epochs; 10 seconds each were selected for Fast Fourier Transform
(FFT) analysis. The relative posterior alpha power at O1 and O2 as well as the
relative theta/beta ratio at C3 and C4 were calculated before and after the
treatment.
Statistical Analysis
Data
are summarized and analyzed using the arithmetic mean and the standard
deviation. The student's t-test was used for comparison of means of two
independent groups. The alpha point of 0.05 was used as a level of statistical
significance. Minitb_V13 was the used
statistical program.
RESULTS
The
mean value of age was (44.06±3.71 and 45.66±4.271 years; P-value = 0.2828),
while the mean value of duration of illness was (2.53±0.52 and 2.533±0.516 months;
P-value = 0.999) for the study and the control groups; respectively.
The study group showed
significant improvement in the TUG time, cadence value, speed value and FMS
score in the post- treatment evaluation compared to that of the pre-treatment
one. The P-value was 0.0001 for all evaluation tests.
The control group showed also
significant improvement in the post-treatment evaluation tests in comparison to
that of the pre- treatment one in terms of TUG time (P=0.0314), cadence value
(P=0.024), speed value (P=0.0046) and FMS score (P=0.005).
When comparing the two groups
together; the pre-treatment evaluation tests showed insignificant values
(P>0.05); while the post-treatment one was significant (Table 1) for TUG
time (P=0.005), cadence value (P=0.0011), speed value (P=0.0002) as well as for
FMS score (P=0.005).
The study group showed significant improvement in the theta/beta
ratio over the treated unaffected hemisphere at
C3 (P-value 0.01) as well as the untreated affected hemisphere at C4 (P-value
0.006). The relative power spectrum of the posterior alpha rhythm at O1
(P-value 0.03) and O2 (P-value 0.03) also showed significant improvement in the
post treatment evaluation compared to the pre- treatment one (Table 2).
There were no significant correlations
between the changes in the alpha power spectrum or that of the theta /beta
ratio at any of the examined positions of either hemispheres and the changes of
the evaluation tests (TUG, Cadence, Speed and FMS) at the post treatment
evaluation (Table 3).
DISCUSSION
The selection of patients in
this study was aimed to exclude aphasic patients to concentrate on the effect
of rTMS on the motion ability mainly. The degree of spasticity was
also selected to be mild according to the modified Ashworth scale so its effect
on gait deviations and post treatment evaluation is minimized. The duration of
illness was chosen to be less than 3 months as the improvement in the absolute values
of the distance and temporal measures of walking have been observed with
increasing time from the onset of the stroke27,28, with respect to
the time from the onset of the infarct, the most rapid improvements have been
observed over the first six weeks to three months, with slower changes being
evident up to one year29,30. Quantitative electroencephalography (QEEG) is a non-invasive technique that allows a highly
precise measurement of brain function and connectivity. QEEG features are sensitive to modification
in neuronal regulation dysfunction, which may therefore help in detecting
regions of altered brain function and connectivity abnormalities31.
In a resting state, (lower frequency) theta band
activity can reflect drowsiness or “cortical slowing.” Alpha band activity is
typically observed during eyes closed at rest, particularly in posterior
regions, and it is negatively associated with central nervous system arousal.
Beta band activity, by contrast, generally accompanies mental activity and concentration.
A theta-to-beta power ratio measured at the vertex (Cz) during eyes-open or
eyes-closed resting condition has been proposed to capture the relative
contributions of two relevant frequency bands for diagnosing and monitoring
ADHD32; however, the true functional significance of this measure
remains unknown. The affected hemisphere showed high theta/ beta ratio
in the pre-treatment evaluation, which improved in the post treatment one. The subcortical infarct caused ipsilaterally increased
slow and decreased fast frequency activity accompanied by decreased
synchronization of slow, increased synchronization of fast frequencies. Reduced
reactivity in the ischemic side was particularly apparent for complexity
measures. The decreased synchronization in the slow frequencies in
the infarct side is probably the result of lesioned interneuronal connections
lowering the level of cooperation of neuronal systems involved in this type of
activity33,34.
There was
significant improvement of all post treatment evaluation tests of gait
including the TUG, Cadence, Speed and FMS.
In previous studies; the combination treatment of 20
sessions, 2000 pulses of 10-Hz rTMS delivered over bilateral leg motor areas
using the double cone coil with intensive physiotherapy, significantly
increased walking velocity and decreased Physiological Cost Index and decreased
the performance time for TUG35. Fugl-Meyer
Assessment and the Wolf Motor Function Test were applied before and after rTMS to evaluate motor function in the affected upper
limb. Changes in asymmetry index (AI) in the superior and middle frontal
areas correlated significantly and negatively with changes in FMA score36.
In this study; the gait evaluation tests could not be
correlated to the increased power of
the fast frequency bands (alpha and beta) in relation to the slow band (theta)
in either affected or unaffected hemisphere. The confusion
as to the functional association, significance, or “meaning” of EEG measures
may result from analyzing the data at the level of individual scalp channels
rather than the cortical source level. Channel signals are, in fact, weighted
mixtures of source signals originating from many different cortical regions
supporting distinct cognitive functions (plus signals from non-brain artifact sources).
Thus, any single-channel based measure mixes potentials from several sources,
not all of which contribute to the effect of interest, thereby constituting
noise in the signal of interest37.
Conclusion
Although rTMS for the unaffected
hemisphere after stroke improves the gait ability of the patient as well as the
fast frequency band of the EEG yet they are not correlated to each other.
[Disclosure:
Authors report no conflict of Interest]
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