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JULY 1989
73R
Abstrucf-A model of hemiplegic spasticity based on electromyographical and biomechanical parameters measured during passive
muscle stretching is presented. Two components of spasticity can be
distinguished-phasic and tonic. This classification depends on the pattern of stretch reflex activity which can be either phasic or tonic as well
as on the muscle stretchltension characteristic. Stretch reflex, as a control loop, is in phasic spasticity characterized by increased sensitivity
to velocity of stretching. In tonic spasticity, sensitivity to length of
stretching is increased. After the injury, phasic spasticity appears first
and invokes monosynaptic reflex pathways. The intensity of tonic spasticity increases with the duration of disability and hence causes changes
in muscle fiber biomechanical properties.
The model mentioned above has been used to evaluate the effects of
FES on spasticity. Hemiplegic patients with implanted peroneal nerve
stimulator for gait correction were followed up for one year starting a
week before implantation. Long-term use of FES resulted in decrease
of tonic spasticity in both ankle joint antagonistic muscle groups. In
stimulated tibialis anterior muscle, the phasic type of spasticity increased. Tu obtain the correlation between changes in spasticity and
functional abilities of patients, the maximal voluntary isometric contraction of both muscle groups was also measured. An improvement in
voluntary strength was also observed. This can be taken as additional
evidence that tonic spasticity is of greater physiological and clinical
significance than phasic spasticity. It may he concluded that use of FES
can decrease tonic spasticity and, if applied early after the injury, can
prevent the appearance of tonic spasticity.
INTRODUCTION
HERAPEUTIC and carry over effects of functional electrical stimulation (FES) have often been
observed and are still under investigation [I 11, [25], [29],
[41]. The functional aspects of changes caused by longterm FES have been tr_eated in various studies. Merletti
with co-workers [30], StefanCiE, ReberSek, and Merletti
[44] and Vodovnik and ReberPek [46] have reported
changes in voluntary control of paretic muscles in hemiplegic patients following FES. Improvement of motor coordination and gait abilities evaluated by biomechanical
and electromyographical measurements during gait have
also been studied by Carnstam, Larsson, and Prevec [8]
and Maleii? et al. 1261. However, it is still questionable
M;inu\cript recci\cd May 70. 1988; revised Novcmber 12. 1988. This
u o r h \-.a\ ~ u p p o i t c din part by the Slovene Research Coinmunity, Ljuhll:ttici. Yugo\la\ i c i . the National lnatitute for Diwbility and Rehabilitation
K e ~ c a r c l i Warhiiigtoii.
.
I>C. and the Vivian Smith Foundation for R e \ t ~ -
whether long-term use of FES results in direct improvement of motor control or also has a certain impact on spasticity.
At least two reasons can explain the lack of quantitative
results of the effects of either short or long term electrical
stimulation on spasticity. First, since a unique definition
of spasticity is still lacking [21], [22] there are numerous
studies concerned with the different parameters of spasticity [4], [8], [15], [28], [38], [47] which can not be easily compared. Second, there is a lack of a simple and effective method for quantitative measurement of the
different components which characterize spasticity. A
large number of studies reported only qualitatively the effects of electrical stimulation on muscle spasticity [3],
[ 171, [23], [24]. Consequently, different and frequently
contradictory opinions about the effects of electrical stimulation on spasticity appear. In clinical practice, there
even exists a widespread attitude that one should not stimulate an already overstimulated spastic muscle.
In this paper, a model of hemiplegic spasticity is presented which is based on electromyographical and biomechanical parameters measured during passive muscle
stretching. The model was used to analyze the results obtained from measurement of ankle joint spasticity in hemiplegic patients with implanted peroneal nerve stimulator
for gait correction. Data were collected starting one week
before implantation and continuing for a maximum of one
year of FES. To obtain the correlation between changes
in spasticity and functional abilities of the patients, the
maximal voluntary isometric contraction of both antagonistic muscle groups was also measured.
MODELOF SPASTICITY
The definition of spasticity is a subject of diverse opinions. A frequently used definition is that of Landau [22],
which includes: 1) decreased dexterity, 2) loss of strength,
3) increased tendon jerks, 4) increased resistance to slower
passive muscle stretch, and 5 ) hyperactive flexion reflexes
(flexor spasms). On the other hand, Knutsson [ 181 described almost unlimited interindividual variation in patients with spastic paresis. This is the basis for the opinion
that spasticity has to be substituted by a detailed description of each particular patients motor disfunction. In this
paper, we have adopted the definition of Pedersen 13 I ] in
which spasticity is described as a part of the upper motoneurone syndrome. The increased phasic and tonic
stretch reflexes are the central part of this definition. Ac-
STEFANOVSKA
er
739
d.:FES A N D SPASTICITY
cordingly , by applying passive muscle stretching at different velocities one can measure neurophysiological and
biomechanical parameters as an indicator of the degree of
spasticity.
Methods of measuring the ankle joint resistance have
already been described [ l ] , [14], [34], [35]. Agarwal and
Gottlieb applied controlled sinusoidal torques and measured the resulting movement in normal [ l ] and spastic
subjects [14]. Rack [34] and Rack et al. [35] imposed
sinusoidal movement and measured resulting torque in
normal subjects. Our approach differs from ones already
mentioned since we applied frequencies of significantly
lower values (0.1-2 Hz) and constant, high amplitude oscillations. There are both engineering and physiological
reasons for such a decision: a) Due to nonlinearities in a
spastic ankle joint the applied frequencies are enough informative in the sense that changes in frequency imply
changes in peak values of the resistive torque. b) While
testing spasticity, the muscle has to be stretched in all of
its length. The range of ankle joint motion in normal subject is 80-90 and is reduced to 40-50 in spastic patients. c) Triggering and measuring the tonic component
of spasticity depend on the duration of stretching. d) For
the phasic component of spasticity, the velocity of
stretching is of high significance. For example, when a
sinusoidal displacement of 1 Hz and amplitude of 16 is
applied, the maximal velocity of stretching is 100/s
which is enough to trigger phasic reflex in the spastic
muscle. Practically, such high amplitude/low frequency
oscillations mimic clinical testing of spasticity.
Measurement of Spasticity
The spasticity of ankle joint muscles in hemiplegic patients was examined. Passive muscle stretching was obtained by sinusoidal movements of the foot in the sagittal
plane. The joint movements were performed by an electrohydraulic position-controlled servosystem [37]. Fig. 1
shows the experimental setup. The center of rotation was
always aligned with the ankle joint axis. Constant resting
(bias) and displacement angles were used. Velocity
dependence on passive resistance was tested at four different velocities of movements, i.e., frequencies of sinusoidal oscillations. Ten successive periods of oscillations were measured at each frequency, with the start and
stop position always at the same bias angle. Four parameters were recorded:
EMG of the tibialis anterior (TA) muscle,
EMG of the triceps surae (TS) muscle,
angular position of the ankle joint, and
resistive torque at the ankle.
Electromyographic activity was detected by silver chloride disc electrodes of 1 cm in diameter.
In the relaxed and cooperative subject a joint resists
movement as a result of its biomechanical properties (joint
inertia and viscoelastic properties of the muscles and joint)
and the degree of triggered stretch reflex, i.e.,
= f(Mc(cp.
signal
electro-
generator
servosystem
ankle
joint
I li
rorque
A b
computer
tibialis soleus
anterior
conversion
analog
recorder
where
is the angular position of the ankle joint, defined
as cp = cpo A sin 27r ft
(po is the resting angle; 30 < (po < 40 in plantar
flexion,
A is the amplitude of oscillation; A = 16,
f is the frequency of movement; f = 0.1,0.5, 1, and
2 Hz,
(b is the velocity of movement; ,,b,(
= 10, 50, 100,
and 200/s,
Mc-ankle joint muscle biomechanical properties,
cp
and
R,-characteristics
Components of Spasticity
The classification of the components of spasticity is
based on the measurements of resistive torque in more
than 100 hemiplegic patients. We have also made the same
measurements in at least 20 normal subjects. In a normal
subject, there is no electromyographic activity in either
the TS or the TA muscles at peak velocities of 10/s200 / s . The peak to peak value of resistive torque does
not change, depending only on the passive biomechanical
properties of the ankle joint, i.e. M = Mc = const. (see
Fig. 3). In the case of spasticity, both electromyographic
activity and resistive torque are increased, resulting in a
characteristic pattern for each particular patient. However, two general types of spasticity can be distinguished
in the hemiplegic population: tonic and phasic spasticity.
Neurophysiological Differences: The two expressions
are in fact used according to the type of reflex activity
[ 121, [ 191, [20], [45]. The term tonic spasticity is used
when tonic component of the stretch reflex activity is predominant, while phasic spasticity is used when phasic
component is predominant. In phasic spasticity, passive
muscle stretching beyond a certain muscle length threshold triggers reflex activity of phasic type. The EMG re-
740
301
l/-j
25
tonic
..
-=E 2 0 W
15-
10-
ut
200%
[ L N rn
0.1
I
I
0.5
1.0
2.0
Frequency ( i : z )
(b)
Fig. 2. (a) Typical pattern of exclusively phasic stretch reflex activity in
triceps surae muscle during passive ankle joint movement. EMG activity
and resistive torque linearly increased with an increase in the velocity of
niovcment. (b) Tonic reflex activity caused strong resistance during passive muscle stretching [note the different sensitivity of resistive torque
in (a) and (b)]. The increased velocity of movement, with simultaneously
decreased duration of stretching resulted in constant EMG activity and
rcsi9tive torque.
cord consists of brief discharge bursts of high frequencies. The intensity increases linearly with increasing
velocity of stretching. Fig. 2(a) shows a typical pattern of
exclusively phasic reflex activity during passive ankle
joint movement, and Fig. 2(b) shows a typical tonic pattern of reflex activity. In the case of tonic activity, the
EMG exhibits a tonic-maintained, low-frequency discharge pattern. The intensity of tonic activity depends on
the velocity and duration of stretching. Increase in frequency of movement results in increased velocity and decreased duration of stretching. The duration of stretching
for each muscle group-agonistic and antagonistic-at 2
Hz is half that at 1 Hz. Consequently, the tonic reflex
activity does not increase proportionally to the velocity of
movement, as shown in Fig. 2(b).
Biomechanical Differences: Velocityltorque characteristics measured on a large population of patients and normal subjects are clustered into three main groups: phasic,
tonic, and normal (Fig. 3 ) . Each of the measured velocity/torque curves falls within one of the three regions
characterized by the upper and lower boundary limit
curve.
At the frequency of 0.1 Hz, the maximal velocity ($,,,
= 10" / s ) is not high enough to trigger phasic reflex even
in the most hyperactive stretch reflex loop. Hence, in
phasic spasticity, the resistive torque includes only biomechanical properties and takes on the values close to
normal subjects. In tonic spasticity, the resistive torque
at 0.1 Hz is higher and reflects either changed muscle fiber properties or a decreased threshold of tonic discharge.
For normal subjects peak-to-peak value of resistive torque
is constant at all measured frequencies. In the phasic
group, the resistive torque increases roughly linearly with
respect to the applied frequency (in some cases the increase can go slightly faster at higher frequencies). In the
tonic group, there is a considerable increase in resistive
torque at lower frequencies (velocities) while at higher
frequencies the resistive torque remains practically saturated. Furthermore, the absolute values of resistive torque
are also significantly higher in tonic than in phasic spasticity. An analytical expression of the above qualitative
descriptions is developed below. The linearity of velocity
dependence of resistive torque can be represented by the
difference in the linear regression characteristic and measured values (regression error)
C IM; I
where M is the measured value of resistive torque obtained by the averaging of peak-to-peak values at ten successive oscillations, A is the estimated value of resistive
torque by linear regression analysis, and for i = 1 ,
* * * , 4 the frequency of movement ( f ) is 0.1, 0.5, 1 ,
and 2 Hz.
The intensity of resistance can be represented by the
area constrained with the interval (0.1; 2 Hz) on the .x
axis and the measured values of resistive torque on the y
axis. In this way the quantitative measure of spasticity can
be defined bv
P = ep/k
where p is the area below the resistive torque curve and k
is a constant.
STEFANOVSKA
el
By choosing k
P
1
<P
I1
74 1
u l . : FES A N D SPASTICITY
TABLE I
PATIENTS
DATA
10 N2 m2 Hz:
I 10 represents
Duration of
Disability
Before Impl.
Age at
Implant.
Cause of Spasticity
3m
25 Y
3m
11 m
6Y
4m
4m
1Y
50
42
37
54
41
48
50
41
CVI
Brain injury
CVI
CVI
Barotrauma
CVI
CVI
Tumor
and
10 < P
I20
LONG-TERM
EFFECTSOF FES
Methodology
The rationale for using implanted electrical stimulator
is that it enables simpler application and regular utilization for the patient, which is particularly important in
long-term study. Eight hemiplegic patients with implanted peroneal nerve stimulators for gait correction were
studied. Patient data are presented in Table I with respect
to the date of implantation. Additional clinical data are
reported elsewhere [4 11.
Before implantation each patient used surface electrical
stimulation for two to three weeks, 30 min per day. The
decision for implantation was made in cases when satisfactory effects of surface FES on gait pattern correction
during swing phase were obtained. All patients were able
to walk using a crutch, except for patient 6, who was able
to walk for 30 m only when assisted. After implantation
all stimulation was stopped for 11 f 1 days. Within the
following week, patients learned to use the peroneal implant and then continued to use chronic electrical stimulation for up to 2 h per day. Only patient 6 did not use
FES to such an extent, as a consequence of his initial inability to walk independently for long distances. Pulse
width of stimulation impulses was up to 0.5 ms using both
surface and implanted electrodes while the frequency was
30-33 Hz. Details on the implantable stimulator and the
technique of implantation are reported elsewhere [42],
WI.
The experimental schedule with particular phases is
given in Fig. 4. The measurements of spasticity and voluntary isometric contraction were made 8 & 4 days before, 21 & 5 days after, six months after and 12 months
after the implantation. Isometric contraction was measured in dorsal and plantar flexion in the same ankle angle
as the resting angle ( cpo) during measurement of spasticity. Maximal voluntary contraction in the TA and T 3
muscles was performed as selectively as possible and had
a duration of approximately 10 s for each muscle. During
the measurements, the patient was always given the same
instructions by the examiner to contract maximally only
one muscle group.
RESULTS
Spasticity: Measurements of resistive torque values
obtained before and six months after implantation are presented in Fig. 5 . Each point in the torque versus frequency plot is defined by coordinates ( f , % ) where f is
is the average of 10 succesthe applied frequency and
sive peak-to-peak values of resistive torque. Low and
constant resistance to passive movement was character-
1) M . A.
2) H. H.
3) R. H.
4) G. J .
5) P. M.
6) J. R.
7) S . A .
8) C . A .
implontation
regular
meosursment measurement
(71)
(T2)
1 week
u s e of FES
maosurament
(T3 )
6 months
mwsurament
(TI)
6 months
istic of patient 8. Chronic FES did not cause any appearance of spasticity in this case. The other seven patients
studied had velocity-dependent resistance increased with
respect to normal. The compressed data for all patients
are presented in Fig. 6. The ordinate of the diagram represents the average of peak to peak values from all the
patients at four frequencies. Three curves are related to
the measurements before, after, and six months after implantation. The decrease in resistive torque after six
months of FES is evident. One can also recognize tile
tendency of the curves toward linearity. This corresponds
to a change in the pattern of reflex activity in the triceps
surae muscle to a phasic pattern. After six months of FES
the phasic reflex activity slightly increased in the stimulated tibialis anterior muscle. A typical increase can be
742
post
3 wk
- 10
6 mo post
gJ
0 01
05
0 10
50
I
Freourncvinzi
100
Md.,rndI
xi0
"eloClly I D I S )
Fig. 6. The average values of the resistive torque calculated from the re
sults obtained in all patients.
r -
tibialis anterior
*--*-*
-__-
,{~&"c.-c
.----
I
I
triceps surae
i
Fig 7 Record\ obtained during passive movement performed at the frequency of 2 Hz before and after six months of FES in patient 4 Increase
in phasic reflex activity in stimulated tibialis anterior muscle IS evident
QUANTITATIVE
TABLE I1
MEASURE
OF SPASTICITY
(P)
Patients
1 weekpreop
3 weekspostop
6 monthspostop
19.5
16.5
1.6
9.4
13.6
12.4
6.5
5.5
16.1
1.3
14.5
3.3
10.7
6.1
6.2
13.0
2.3
1.0
0.7
0.3
2.2
5.7
seen in Fig. 7 where records obtained from the same patient during passive movement with a frequency of 2 Hz
(patient 4-before and six months after the implantation)
are presented. To summarize, let us consider the values
of factor P representing the type of spasticity presented in
Table 11. The data clearly show that long-term use of FES
decreased the level of spasticity and influenced the
changes in the type of spasticity from tonic to phasic.
Voluntary Isometric Contraction: Results are presented in Fig. 8(a) for plantar flexion, and Fig. 8(b) for
dorsal flexion. Each point in the torque versus time plane
is the average value of isometric torque obtained during
10 s of voluntary contraction. Improvement of voluntary
strength in both plantar and dorsal flexors is evident. This
improvement is of higher extent in TA muscle where electrical stimulation was applied.
DISCUSSION
A model of spasticity is presented which includes two
(b)
Fig. 8. Values of maximal voluntary isometric contraction in plantar flexion (a) and dorsal flexion (b). TI-one week before implantation, 1mpI.time of implantation, T2-three weeks after, T3-six months after and
T4--12 months after implantation.
muscles and an increase in phasic spasticity in the stimulated TA muscle were observed. Those changes resulted
in improved voluntary strength in both ankle joint antagonistic muscle groups. Such results are in agreement with
the opinion that tonic reflex activity is of greater physiological and clinical significance than phasic stretch reflex
activity [ 191. The model is based on the measurements of
hemiplegic spasticity and does not include other manifestations of spasticity characteristics of additional pathologies. For example, flexor spasms are rarely present in
hemiplegic spasticity but are particularly dominant in paraplegic spasticity [40].
The method used in this study is based on the measurements of biomechanical and stretch reflex properties of
the spastic muscles. Such a technique has been used in
various studies of mechanisms of spasticity [5], [6], [ 141,
[16], [28], [37], while it has been used in few studies of
the influence of different therapeutic techniques on spasticity [27] and particularly the effects of electrical stimulation [4], [32], [38]. This measurement method enables
minimization of the influence of the measurement itself
on the variable state of spasticity [36]. However, the complexity of spasticity itself and the changes brought about
STEFANOVSKA
rl
U/.:
FES A N D SPASTICITY
743
200ms
Fig. 9 . I)Twitch contraction of soleus muscle in normal subject. 2) spastic patient three years after the injury who has been using FES for two
years, and 3) spastic patient two years after the injury who has not been
using FES.
BioReduced
spasticity
Neurophysioloqical
Improved
voluntary control
i ...I
Fig. I O . Direct effects of FES (first level) resulted in long-term changes
of neurophysiological and biomechanical properties (second level).
REFERENCES
[ 1 I G . C. Agarwal and G . L . Gottlieb, "Oscillation o f the human ankle
121
131
141
[Si
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P . Ashby. M . Verrier, and E , Lighfoot, "Segnlental reflex pathwny
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o/.
P . \ y ~ h i c i r r ~vol.
.
37. pp. 1352-1360. 1974.
V. Alfieri. "Electrical treatment of spasticity-ReHex tonic activity
eICCtrOSti,nUI~,tiOn,~~
i n hcrniple:ric patients and
S(.cim/. J . Rrlicrh. M d . , vol. 14. pp. 177-182, 1982.
T . Bajd. M . Gregori?, L. Vodovnik. and H. Benko. "Electrical slimulation in treating spasticity due to spinal cord injury." Arc.11. P h ~ s .
T/7rr. R d i d 7 i / . , v o l . 66, pp. 515-517, 1985.
A . Berardelli. M . Hallett. C. Kaufman. E. Fine. W . Berenberg. and
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145