ARTICLE IN PRESS

Effects of Repetitive Facilitative Exercise on Spasticity in the

Upper Paretic Limb After Subacute Stroke

Seiji Etoh, MD, PhD,* Tomokazu Noma, OT, PhD,† Ryuji Miyata, MD, PhD,*
and Megumi Shimodozono, MD, PhD*

Background: Repetitive facilitative exercise is an effective method for recovery of the

affected limb in stroke patients. However, its effects on spasticity are unknown. We
aimed to determine the effects of repetitive facilitative exercise on spasticity using
the Modified Ashworth Scale (MAS) and the F-wave, and to determine the relation-
ship between the changes in spasticity and functional recovery of the hemiplegic
upper limb. Methods: Subacute stroke patients underwent repetitive facilitative
exercise (n = 11) or conventional rehabilitation (n = 8) for 4 weeks. We investigated
spasticity and functional recovery in a hemiplegic upper limb retrospectively. The
MAS, F-wave, Fugl-Meyer Assessment (FMA), and the Action Research Arm Test
(ARAT) were assessed immediately before and after the 4-week session.
Results: Repetitive facilitative exercise did not change the MAS and decreased F per-
sistence and the F amplitude ratio, and improved both the FMA and the ARAT for
the affected upper limb. The reduction of F-wave parameters was not correlated
with the improvements in the FMA and ARAT in the repetitive facilitative exercise
group. Conventional rehabilitation had no effect on the MAS, F-wave parameters,
FMA, or the ARAT. Conclusions: Repetitive facilitative exercise decreases spinal
motoneuron excitability and promotes functional recovery. However, there was no
correlation between the change in spinal motoneuron excitability and the improve-
ment of upper-limb function. The present results suggest that repetitive facilitative
exercise is useful for treating spasticity in the subacute phase of stroke.
Key Words: Repetitive facilitative exercise—spasticity—F-wave—stroke
© 2018 National Stroke Association. Published by Elsevier Inc. All rights reserved.

Introduction physiotherapies have been developed to improve the func-

Stroke is a major cause of disability and leaves about two
thirds of its survivors with long-term impairments. Most
patients with stroke who survive the initial injury experi-
ence limited activity and reduced participation.1 Various
From the *Department of Rehabilitation and Physical Medicine,
Graduate School of Medical and Dental Sciences, Kagoshima Univer-
sity, Kagoshima, Japan; and †Department of Rehabilitation, Kirish-
ima Rehabilitation Center of Kagoshima University Hospital,
Kagoshima, Japan.
Received January 20, 2018; revision received June 1, 2018; accepted
June 14, 2018.
Disclosure statement: We report no conflicts of interest.
Address correspondence to Seiji Etoh, MD, PhD, Department of
Rehabilitation and Physical Medicine, Graduate School of Medical
and Dental Sciences, Kagoshima University, 8-35-1, Sakuragaoka,
Kagoshima City, Kagoshima 890-0075, Japan. Tel.: +81-99-275-5339;
fax: +81-99-275-1273. E-mail: etohs@m2.kufm.kagoshima-u.ac.jp
1052-3057/$ - see front matter
© 2018 National Stroke Association. Published by Elsevier Inc. All
rights reserved.
https://doi.org/10.1016/j.jstrokecerebrovasdis.2018.06.013
tion of a hemiplegic upper limb in patients due to stroke.
Repetitive facilitation exercise (RFE) is a form of physio-
therapy that has been shown to reduce the impairment
after stroke.2,3 In RFE, the therapist provides physical
stimulation, such as by eliciting the stretch reflex or skin-
muscle reflex, immediately before the patient tries to
move their hemiplegic hand or finger, to increase the level
of excitation of the corresponding injured descending
motor tracts; this increased excitation allows the patient to
initiate movements of the hemiplegic hand or finger in
response to their intention.2 The results of a randomized
controlled trial (RCT) study showed that RFE significantly
improved motor function of the affected upper limb.3
In addition to motor deficits, muscle spasticity in the
affected upper limb is another feature of stroke. Spasticity
influences body functions and limits activity in stroke
patients. For example, patients who were nonspastic had
statistically and significantly better motor and activity
scores than spastic patients.4 In addition, spasticity in the
affected limbs often inhibits the efficacy of physiotherapy

Journal of Stroke and Cerebrovascular Diseases, Vol. &&, N0. && (&&), 2018: pp 1-6 1
 ARTICLE IN PRESS
2 S. ETOH ET AL.
for the treatment of stroke.5,6 Therefore, it is important to
control spasticity to improve movements of the upper
limb. Although RFE has been shown to be effective for
improving recovery of the affected limb in stroke patients,
its effects on spasticity are unclear.
Constraint-induced movement therapy (CIMT) is also
effective for promoting motor recovery of a hemiplegic
upper limb.7 Several reports have described the effects of
CIMT on spasticity and motoneuron excitability in the
affected upper extremity.8-10 These studies used the Modi-
fied Ashworth Scale (MAS) or F-wave parameters. The
F-wave is a motor response produced by the backfiring of
alpha motoneurons after the antidromic stimulation of
motor nerve fibers. The amplitude and persistence of the
F-wave have been used as indicators of spasticity in previ-
ous studies.11,12 It has been reported that the F-wave can
be used to reliably detect the inhibition of alpha motoneu-
ron excitability.13 F-wave activity is modified by cortical
activity and influenced by the excitability of the motor
neuron pool.14,15 CIMT produced a significant decrease in
both the MAS score and F-wave parameters in the
affected upper limb in chronic stroke patients.10
It is unclear whether RFE decreases spasticity as well as
promoting functional recovery of an affected upper limb
in subacute stroke patients. We aimed to determine the
effects of RFE on spasticity using MAS and the F-wave
and to determine the relationship between the changes in
spasticity and the improvement of motor function in
hemiplegic upper limbs.
Methods
Patients
Participants were extracted from among the subjects of a
previous RCT study on RFE.3 Eleven of the 27 patients in
the RFE group and 8 of the 25 patients in the conventional
rehabilitation group were subjected to measurements of
MAS and F-waves (evaluation of spasticity) in addition to
the Fugl-Meyer Assessment (FMA) and Action Research
Arm Test (ARAT) (evaluation of motor deficits). Therefore,
in the present study, a total of 19 patients were extracted
from the previous RCT study. The mean age was 60.9 years
(standard deviation = 14.4) and the mean duration after
stroke onset was 50.8 days (standard deviation = 21.0).
Inclusion criteria for the previous RCT study were as fol-
lows3: (1) a new, single, computed tomography-confirmed
stroke within the previous 3-13 weeks; (2) Brunnstrom
proximal upper-limb stage
III16; and (3) the ability to fol-
low simple directions. Subjects were excluded due to (1)
arm contractures/pain; (2) preexisting upper-extremity
impairment; (3) cerebellar lesion; (4) unstable medical sta-
tus; (5) perceptual, apraxic, or cognitive deficits that would
prevent adequate participation in the study; or (6) inability
to provide informed consent. The study was approved
by the ethics committee at Kagoshima University Hospital
(27-183). Written informed consent was obtained from each
patient before inclusion.
Measurement
Patients underwent RFE (n = 11) or conventional reha-
bilitation (n = 8) for 4 weeks. We measured MAS scores
and F-waves in addition to FMA and ARAT in a hemiple-
gic upper limb immediately before and after the 4-week
session. The MAS score was used to evaluate spasticity in
the elbow and wrist of the affected upper limb.17 To facili-
tate data analysis, MAS scores (0, 1, 1+, 2, 3, and 4) were
assigned numerical values (0, 1, 2, 3, 4, and 5, respec-
tively). F-waves were recorded in a supine or sitting posi-
tion. A Nihon-Kohden Neuropack was used with a band-
pass filter of 20 Hz-5 kHz, with the sensitivity set to 5 mV
and 500 mV/division, respectively. Compound muscle
action potentials (CMAPs) and F-waves were recorded
from the abductor pollicis brevis on both sides. The
median nerve was stimulated at the wrist at 1 Hz. Stimuli
were .2 ms in duration and 20% higher than the intensity
that elicited the largest CMAPs. Ninety-six F-waves were
recorded. The F-wave persistence on both sides, the F/M
ratio (trial average of the F-wave amplitude [which aver-
ages trials with no response]/CMAP amplitude) of the
affected side and the F-wave amplitude ratio (trial aver-
age of the F-wave amplitude on the affected side/that on
the unaffected side) were used for evaluation. FMA was
used to evaluate motor function.18 The motor score for the
upper extremity includes 33 items and ranges from 0 to
66. The ARAT was used to assess the ability of the subject
to manipulate objects. The ARAT is a validated and reli-
able measure of upper-extremity function with 4 subsec-
tions (grip, grasp, pinch, and gross movement) and
ranges from 0 to 57.19
Intervention
The 11 patients underwent RFE in 40-minute sessions
on a 4-week, 5 sessions/week schedule. RFE involves the
use of rapid passive stretching of the muscles in conjunc-
tion with tapping and rubbing of the skin to assist in
inducing contraction of the targeted muscles. Participants
were directed to concentrate on generating movement of
the joint being treated while avoiding the contraction of
nontargeted muscles. Therapists helped the subjects to
achieve a full range of motion. The target movements
(shoulder flexion, elbow extension, wrist extension, and
finger extension) can be repeated many times during a rel-
atively short time period.
The remaining 8 patients in the subacute group
received conventional rehabilitation for the hemiplegic
upper limb in 40-minute sessions on a 4-week, 5 sessions/-
week schedule. Sessions consisted of (1) ROM exercises;
(2) passive, assistive, active, and progressive resistive
exercise; (3) the use of skateboards or weighted sanders;
and (4) pinching or grasping blocks of various sizes.
 ARTICLE IN PRESS

Statistical Analysis improved after RFE. In contrast, there were no changes in

Nonparametric statistics were used for the analysis.
Baseline characteristics were compared using the Mann-
Whitney U test or the chi-square test for observed fre-
quencies for continuous and ordinal variables, and P val-
ues <.05 were considered to be statistically significant.
The Mann-Whitney U test was used as a test of improve-
ment at 4 weeks after baseline and between group differ-
ences in gain. The Spearman rank correlation coefficient
was used to analyze the relationship between the change
of spasticity and functional recovery. The results are
shown as the median and range. SPSS (version 24 for Win-
dows) was used for the statistical analysis.
Results
We examined the effects of RFE on spasticity and func-
tional recovery. There were no adverse effects. Table 1
shows the demographic data. There were no significant
differences in demographic data between the RFE group
and the conventional rehabilitation group. Table 2 shows
the changes in MAS scores, F-wave parameters, and
motor function after 4 weeks. While there were no
changes in MAS scores, F wave persistence on the affected
side and F-wave amplitude ratios were significantly
reduced after RFE. FMA and ARAT were significantly
MAS score, F-wave parameters, FMA, or ARAT after con-
ventional rehabilitation. The decrease in F-wave persis-
tence, the decrease in the F-wave amplitude ratio, and the
increase in ARAT in the RFE group were significantly
greater than those in the conventional rehabilitation
group. Table 3 shows the results of correlation tests
between the change in spasticity and that in motor func-
tion in the RFE group. Although the patients in the RFE
group showed significant changes in F-wave persistence,
F amplitude ratio, FMA, and ARAT, no significant corre-
lations were observed. We confirmed that the scatter-
grams for the change in spasticity and motor function in
the RFE group did not have a nonlinear relationship. We
show the 4 scattergrams for the relationships between
changes in F-wave persistence on the affected side or the
F-wave amplitude ratio (affected/unaffected side) and
changes in FMA or ARAT (Fig 1), because these parame-
ters significantly improved after 4 weeks (Table 2).
Discussion
RFE did not change MAS scores and reduced both the
F-wave persistence and the F amplitude ratio. RFE
improved the FMA and ARAT scores. In contrast, conven-
tional rehabilitation did not change MAS scores, F-wave

Table 1. Baseline characteristics of the participants (n = 19)*

RFE group (n = 11) Conventional group (n = 8) P values

Age, years 65 (41-73) 64 (39-89) .84y
Sex, male 8 6 .66z
Time since stroke, days 39 (25-75) 61 (24-92) .55y
Side of motor deficit, right 7 2 .12z
Type of stroke
Infarction 6 4 .61z
Hemorrhage 5 4
Stroke location
Basal ganglia 4 2 .51z
Thalamus 1 1
Internal capsule/corona radiata 3 1
Territory of middle cerebral artery 0 3
Cortex 1 1
Brainstem 2 0
FMA 29 (4-60) 8 (4-63) .44y
ARAT 19 (0-48) 0 (0-57) .60y
MAS
Elbow flexors 1 (0-3) .5 (0-3) .90y
Wrist flexors 0 (0-4) .5 (0-3) 1.00y
F-wave persistence (%)
Affected side 85 (0-99) 71 (2-94) .31y
Unaffected side 51 (1-85) 64 (51-78) .44y
F/M (affected side) 2.1 (0-5.3) 2.1 (.1-4.0) .97y
F-wave amplitude ratio (affected side/unaffected side) 1.6 (0-4.6) .6 (0-2.4) .051y
FMA, Fugl-Meyer Assessment; ARAT, Action Research Arm Test; MAS, Modified Ashworth Scale.
* Values are median (range in parentheses) or number.
† Mann-Whitney U test.
‡ Chi-square test.
 ARTICLE IN PRESS
4 S. ETOH ET AL.

parameters, FMA, or ARAT scores. These results mean

P valuesy

.005***

.008***
.012**
that, while RFE does not change the clinical score of spas-

.051

.75
.15

.41
.12
ticity, it does reduce spinal motoneuron excitability. In
contrast, conventional rehabilitation does not affect either
spasticity or motoneuron excitability in subacute stroke

.6 (¡2.5 to 4.6)
.5 (¡2.1 to 1.4)
patients. The reduction of F-wave parameters was not cor-

11 (¡13 to 22)
3 (¡24 to 18)
1.5 (¡5 to 8)

0 (¡2 to 3)
related with the improvements in FMA and ARAT in the

P < .01 (Mann-Whitney U test).

Gain

RFE group. This result indicates that there is no correla-

0 (0-4)

.5 (0-2)
Conventional rehabilitation (n = 8)

tion between the change in motoneuron excitability and

the improvement of upper-limb function during RFE.
While the lack of a change in the clinical score of
spasticity after physiotherapy in this study is inconsistent
84 (19-93)
68 (30-82)
2.5 (.5-7.3)
1.1 (.1-2.3)
with previous reports,8-10,20 the decrease in spinal moto-
13 (5-64)
0 (0-57)
4 weeks

1.5 (0-3)
2 (0-4)

neuron excitability is consistent with previous reports.10

A previous before-after study reported that CIMT
reduced MAS scores, F persistence, and the mean F/M
***
ratio in chronic stroke patients.10 Another before-after
Table 2. Changes in outcome measures at the end of treatment (n = 19)*

64 (51-78)
2.1 (.1-4.0)

study reported that repetitive transcranial magnetic stim-

.6 (0-2.4)

† P values indicate the significance level of between-group differences in gain according to Mann-Whitney U test. **P < .05
8 (4-63)
0 (0-57)

71 (2-94)
.5 (0-3)
.5 (0-3)
Baseline

ulation (rTMS) + intensive occupational therapy reduced

both MAS scores and the mean F/M ratio in chronic
patients.20 There are two possible explanations for this dif-
ference regarding the clinical scores of spasticity. First, the
patients in our study were in the subacute phase (<3
¡.4 (¡1.9 to 2.9)
¡.22 (¡3.7 to .4)
3 (¡17 to 42)
¡3 (¡50 to 5)

* Values are median (range in parentheses). **P < .05 ***P < .01 versus baseline (Mann-Whitney U test).

months) and patients in previous reports were in the

0 (¡2 to 2)
0 (¡1 to 3)

chronic phase (>6 months). A study of 95 stroke patients

8 (0-18)
9 (0-26)
Gain

revealed that spasticity was present in only 19% of

patients investigated 3 months after stroke.4 MAS scores
FMA, Fugl-Meyer Assessment; ARAT, Action Research Arm Test; MAS, Modified Ashworth Scale.

might not have changed in the subacute phase of stroke

RFE group (n = 11)

because of the small number of patients with spasticity.

The other possible explanation is the difference between
***

24 (0-57)***

.5 (.1-4.4)**
73 (3-98)**

1.6 (.1-8.2)

MAS and F-wave parameters. A study of motoneuron

59 (20-95)
4 weeks
47 (8-65)

excitability in stroke patients reported that there was no

1 (0-3)
0 (0-4)

difference in F persistence between spastic (MAS = 1-2)

and nonspastic (MAS = 0) patients.21 Thus, an increase in
spinal motoneuron excitability does not necessarily lead
to spasticity, which suggests that motoneuron excitability
2.1 (0-5.3)
1.6 (0-4.6)
Baseline
29 (4-60)
19 (0-48)

85 (0-99)
51 (1-85)

and spasticity may be related but different phenomena.

1 (0-3)
0 (0-4)

We compared the effect of RFE on spasticity to that of

conventional therapy. We revealed that RFE decreased
motoneuron excitability, but conventional rehabilitation
did not. To the best of our knowledge, this is the first
F-wave amplitude ratio (affected/unaffected side)

study to show that different rehabilitation methods have

different effects on motoneuron excitability in subacute
stroke patients. RFE facilitates the repeated voluntary
movement of an affected upper limb. Repeated voluntary
movement of an affected upper limb might enhance the
corticomotor drive from the motor cortex to spinal moto-
neurons, which might influence motoneuron excitability.
F/M (%) (affected side)
F-wave persistence (%)

All subjects in the present study were extracted from

the previous RCT study.3 These patients had allowed us
to measure F wave and MAS data. We extracted 11
Unaffected side
Elbow flexors

patients (41%) from 27 patients in the RFE group in the

Affected side
Wrist flexors

previous RCT study, and 8 patients (32%) from 25 patients

in the conventional group in the previous RCT study. The
ARAT
FMA

MAS

subjects in the present study cooperated with our meas-

urements and seemed to be interested in the effect of
 ARTICLE IN PRESS

Table 3. Correlations between changes in MAS and F-wave parameters and changes in FMA and ARAT in the RFE group (n = 11)*

⊿FMA ⊿ARAT
RFE group (n = 11)
⊿MAS (elbow) .30 (.37) .26 (.45)
⊿MAS (wrist) .35 (.29) .22 (.53)
⊿F-wave persistence (affected side) ¡.28 (.40) .40 (.23)
⊿F/M (%) (affected side) ¡.28 (.41) .08 (.81)
⊿F-wave amplitude ratio (affected/unaffected side) ¡.20 (.54) .36 (.28)
FMA, Fugl-Meyer Assessment; ARAT, Action Research Arm Test; MAS, Modified Ashworth Scale.
* Coefficient (P value).

Figure 1. Scattergrams of changes in F-wave parameters and changes in FMA and ARAT in the RFE group (n = 11). FMA, Fugl-Meyer Assessment; ARAT,
Action Research Arm Test. (A) Change in F-wave persistence of affected side and changes in FMA or ARAT. (B) Change in F-wave amplitude ratio (affected/
unaffected side) and changes in FMA or ARAT.

rehabilitation. This may have influenced the effect of
rehabilitation on spasticity or upper-limb function.
Although there were no significant differences between
the parameters in the RFE group and those in the con-
ventional group (Table 1), we cannot exclude the possi-
bility of a selection bias.
RFE reduced motoneuron excitability and improved
FMA and ARAT scores, but the reduction in motoneuron
excitability was not correlated with the improvement in
affected upper-limb function in the RFE group. Our result
is consistent with previous reports. A before-after study
showed that CIMT over 2 weeks produced a significant
decrease in F-wave persistence, F/M ratio, and MAS, as
well as the recovery of motor function in the affected limb.
However, there was no correlation between the decrease in
F-wave persistence and the improvement of upper-limb
function.10 These data indicate that motor function and
motoneuron excitability are related but different
phenomena. To further improve rehabilitation, it may be
important to reveal the relationship between motoneuron
excitability and functional recovery in stroke patients.
Limitation
This study has some limitations. First, it included only a
small number of patients. The small size of the study
group prevented us from examining the correlation
between motoneuron excitability and functional recovery
of an affected upper limb. Future studies with a large
number of participants will be needed to reveal the rela-
tionship between motoneuron excitability and functional
recovery. Second, it was difficult to compare the effects of
the two rehabilitation methods precisely because this
study was retrospective and the participants were part of
another RCT study. Third, this study considered only a
limited follow-up period. The long-term effects of RFE on
 ARTICLE IN PRESS
6 S. ETOH ET AL.
excitability should be studied, since this issue is important
in rehabilitation.
Conclusion
In conclusion, this study suggests that RFE decreases
motoneuron excitability, does not change the clinical score
of spasticity, and improves functional recovery of an
affected upper limb in subacute stroke patients. However,
the reduction in motoneuron excitability is not correlated
with the improvement of upper-limb function. Conven-
tional rehabilitation has no effect on motoneuron excit-
ability, clinical scores of spasticity or the functional
recovery of an affected upper limb. Repeated voluntary
movement of an affected hand might influence motoneu-
ron excitability and functional recovery.
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