Archives of Physical Medicine and Rehabilitation

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Archives of Physical Medicine and Rehabilitation 2013;94:822-8

ORIGINAL ARTICLE

Effects of Continuous Passive Motion on Reversing the Adapted

Spinal Circuit in Humans With Chronic Spinal Cord Injury
Ya-Ju Chang, PhDa,b,* Jing-Nong Liang, MSa,* Miao-Ju Hsu, PhDc,d Hen-Yu Lien, PhDa,b
Chia-Ying Fang, MSa,e Cheng-Hsiang Lin, PhDf
From the aDepartment of Physical Therapy and Graduate Institute of Rehabilitation Science, College of Medicine, Chang Gung University,
Taoyuan; bHealthy Aging Research Center, Chang Gung University, Taoyuan; cDepartment of Physical Therapy, College of Health Science,
Kaohsiung Medical University, Kaohsiung; dDepartment of Physical Medicine and Rehabilitation, Kaohsiung Medical University Hospital,
Kaohsiung; eDepartment of Rehabilitation Technology, Tzu Hui Institute of Technology, Pingtung; and fDepartment of Statistics, Tunghai
University, Taichung, Taiwan.

Abstract
Objective: To investigate the possibility of restoring the adapted spinal circuit after spinal cord injury (SCI) by means of long-term continuous
passive motion (CPM) of the ankle joint.
Design: Randomized controlled trial with repeated measures.
Setting: Research laboratory in a general hospital.
Participants: Individuals with motor complete SCI (NZ14) were recruited from a community.
Intervention: CPM of the ankle joint for 1 hour a day, 5 days a week for 4 weeks.
Main Outcome Measures: Modified Ashworth Scale (MAS) scores for evaluation of spasticity and postactivation depression (PAD) were
documented prior to and after intervention.
Results: MAS scores improved after 4 weeks of CPM intervention, indicating a reduction in spasticity of the ankle joint. PAD was restored after
4 weeks of training.
Conclusions: Passive motion of the ankle joint alone was sufficient in reversing the adapted spinal circuit, and therefore indicates that spasticity
after SCI could possibly be managed by CPM intervention. The results of this study support the use of the passive mode of robot-assisted therapy
for humans with complete SCI who cannot exercise actively.
Archives of Physical Medicine and Rehabilitation 2013;94:822-8
ª 2013 by the American Congress of Rehabilitation Medicine

After injury to the spinal cord, the spinal circuitry undergoes
various adaptations, which are paralleled by the progressive onset
of the syndromes of spasticity.1-3 Alterations of the spinal circuitry
function, such as the reduction of postactivation depression (PAD)
at the Ia-motoneuron synapse, could be one of the main spinal
mechanisms underlying spasticity.
The Hoffmann reflex (H-reflex) is a compound muscle action
potential elicited by electric stimulation of afferent Ia fibers in
the mixed muscle nerve with subsequent recruitments of motor
)
Chang and Liang contributed equally to this article.
Presented to the Society for Neuroscience, November 3e7, 2007, San Diego, CA.
Supported by the National Science Council, Taiwan (grant nos. NSC 94-2314-B-182-003 and
95-2314-B-182-044-MY2), the Chang Gung Medical Research Program, Taiwan (grant no.
CMRPD180101), and the Healthy Aging Research Center, Chang Gung University.
No commercial party having a direct financial interest in the results of the research supporting
this article has or will confer a benefit on the authors or on any organization with which the authors
are associated.
neurons through monosynaptic connections in the spinal cord.3
The H-reflex is evoked by direct activation of Ia afferents and
can reflect the excitability of the alpha motor neuron pool.4
Several studies showed that the soleus H-reflex increased in
spastic patients, but there are controversial reports.5-9
PAD is a frequency-related depression of the H-reflex and has
been documented in both humans3,10-16 and cats.2,17 PAD of the
reflex discharge has been described for stimulus intervals as long
as 10 to 20 seconds.18 PAD has been suggested to hold the
synaptic efficacy of the Ia fiber at a relatively low level during
voluntary movements and is of functional significance because it
would keep the stretch reflex at a relatively low gain, and thus
contributes to the prevention of clonus development.14
PAD can evaluate the integrity of adapted spinal circuitry. PAD
has been shown to be impaired in spinal cord-lesioned animals19,20
and in humans3,11,21 with spasticity after spinal cord injury (SCI).

0003-9993/13/$36 - see front matter ª 2013 by the American Congress of Rehabilitation Medicine
http://dx.doi.org/10.1016/j.apmr.2012.11.035
Continuous passive motion on spinal circuitry of SCI
Studies also showed that the decrease of PAD rather than the
decrease of the amplitude of the H-reflex was related to the
spasticity after SCI.3,22
The decrease of PAD after SCI is dependent on the time
postinjury. In rats with spinal cord contusion20 and spinal cord
transection,19 the magnitude of PAD was comparable with that of
the control intact animals at acute phases postinjury, but at chronic
phases of injury, the magnitude of PAD was significantly lower.
Individuals with chronic SCI show less PAD compared with acute
and nonimpaired individuals.3,21
Minimizing post-SCI complications, for example immobiliza-
tion, might reverse these adaptations and consequently reduce
spasticity. Decreased muscle tone has several clinical benefits,
such as allowing patients to perform functional activities easier,
wear orthosis, and perform home exercise programs. In order to
remobilize paralyzed muscles after motor complete SCI, the
therapeutic strategies are limited to passive exercise or electric
stimulation. Electric stimulation has shown promising effects on
the restoration of muscle properties.23,24 However, no parallel
restoration of the spinal circuitry function was found. Passive
exercise used to be overlooked clinically because of the uncer-
tainty of the therapeutic effect and its high demand for man power.
The recent development of robot-assisted therapy makes the long-
term passive exercise with high repetition possible, but the ther-
apeutic effect on the restoration of spinal circuitry and clinical
features needs to be clarified.
In transected animal studies, passive exercise can restore PAD.
Four weeks of passive cycling attenuated and reduced the degree
of atrophy in hind-limb muscles of spinal cord transected rats.25,26
Skinner et al19 conducted 3 months of 5 days per week passive
cycling in acute spinal cord transected rats and showed the
restoration of the PAD of the H-reflex to a level similar to the
nonimpaired rats. Statistically significant levels of PAD were
evident by 30 days of passive cycling exercise, although restora-
tion of PAD could be seen starting 15 days postintervention.27
A linear increase in PAD of the H-reflex was observed with
a duration of 90 days of passive cycling implementation.27 In
summary, passive exercise is able to restore PAD in spinal cord
transected animals in 4 weeks.
There are limited studies that document the effect of passive
exercise on the restoration of spinal circuitry in humans with
SCI. A case study reported that 1 patient with SCI who under-
went 13 weeks of daily passive cycling showed gradual resto-
ration of PAD with time. Subjective assessments indicated
a significant reduction in spasticity.28 However, the effect of
passive cycling exercise has never been successfully reproduced
in a controlled group study in order to set up clinical guidelines.
A possible explanation is that passive cycling is a motion
involving multiple joints of the lower extremities. The range of
motion of the involved joints is difficult to control in cycling
training. For example, excessive hip and knee movement might
compensate the movement of a stiff ankle joint. The treatment
effect is not easy to reproduce because of inconsistent range of
joint movements across subjects.
List of abbreviations:
CPM continuous passive motion
H-reflex Hoffmann reflex
MAS Modified Ashworth Scale
PAD postactivation depression
SCI spinal cord injury
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823
The immediate decrease in reflex sensitivity after short-term
intervention of continuous passive range of motion exercises of
the ankle joint has been shown in both nonimpaired individuals
and individuals with SCI.29,30 There was also a decrease in the
Modified Ashworth Scale (MAS) score, indicating a decrease of
spasticity.30 However, the long-term effect has to be established.
The purpose of this study was to investigate if multiple sessions of
continuous passive motion (CPM) of the ankle joint could restore
the spinal circuit functions, PAD, after injury to the spinal cord
once they had undergone adaptations. Because the single joint
CPM will have better control of the range of motion for the joint
to be trained than cycling motions, and animal studies showed
promising restorations of PAD after 4 weeks of passive cycling
training, the treatment duration was set at 4 weeks. One subject
was overtrained for an additional 8 weeks to preliminarily explore
the optimal duration of training. The results of this study could
provide a new concept in clinical rehabilitation for individuals
with chronic SCI and provide evidence for applications of the
passive mode of robot-assisted therapy.
Methods
Fourteen subjects who had sustained a motor complete SCI for at
least 6 months (chronic SCI) prior to testing were randomly allo-
cated into either the 4-week ankle CPM training group or the
control group (no training) (table 1). The randomization was
according to a balanced prerandomized table. All subjects were
recruited from the community. Subjects’ medical conditions were
stable. One subject allocated in the CPM training group volunteered
to be overtrained for an additional 8 weeks after the end of the study
in order to explore the dose response of training. All subjects had
motor complete paralysis, which was corresponding to American
Spinal Injury Association classification grade A or B,31-33 at or
above the T12 level. The sample size was determined by a pilot
study, and the SD was estimated from previous research.3
All subjects gave their written informed consent in accordance
with the Declaration of Helsinki. The study was approved by the
institutional review board.
Experimental procedures
Prior to electrophysiologic testing, each subject underwent muscle
tone evaluation of the ankle joint using the MAS in sitting position
with knee flexion to 90
. This position was chosen to minimize the
influence of gastrocnemius muscle tone. All clinical examinations
were proceeded under identical conditions for each test by
a licensed physical therapist who was blinded to group allocation.
All subjects were seated with back support during electrophysio-
logic tests. The testing leg was determined in a randomized
manner. The testing leg was secured with hook and loop straps on
a forceplate system30 with knee flexion 110
, and the slope of the
forceplate was adjusted such that the ankle was supported in
neutral position (0
dorsiflexion or plantarflexion).
The surface electromyographic recording electrode was posi-
tioned on the soleus muscle.30,33-36 The recording electrode was
positioned in parallel with the soleus muscle, approximately 2cm
lateral to the midline of the distal calf and distal to the lateral head
of the gastrocnemius, about two thirds the distance from the knee
joint line to the lateral malleolus. A ground electrode was placed
over the lateral malleolus. The M-waves and H-reflexes of the
soleus were elicited by transcutaneous electric stimulation of the
824 Y-J Chang et al

Table 1 Subject demographics, injury characteristics, and spasticity measurements

Training
Control Injury Level Age Time Postinjury (mo) ASIA Grade MAS Pre MAS Post P (MAS Post vs Pre)
Training Group
1y C5 28 15 A 4 3 .013*
2 C7 30 16 A 5 4
3 T4 36 30 A 4 4
4 C5 20 18 A 3 3
5 C6 25 40 A 3 2
6 T10 34 18 A 3 2
7 T12 45 6 B 2 1
Control Group
8 C5 30 18 B 5 5 .159
9 C7 30 30 A 4 5
10 T12 35 12 A 3 3
11 T4 40 60 A 3 3
12 T 40 24 A 3 3
13 T 37 42 A 4 4
14 T4 35 18 A 4 4
Abbreviation: ASIA, American Spinal Injury Association.
* Significant difference between pre- and post-MAS score (P<.05).
y
Subject was overtrained for an additional 8 weeks.

tibial nerve at the popliteal fossa with a fixed pulse width of
500ms. The maximal M-wave was determined. Electric stimula-
tions were set at an intensity that could elicit H-reflexes of peak-
to-peak amplitudes of 20% of the maximal M-wave.10
For the PAD recordings, 5 pairs of soleus H-reflexes were
elicited in a randomized order at each of the following frequen-
cies: 0.1Hz, 1Hz, 5Hz, and 10Hz. The paired stimulation para-
digm was chosen to minimize the possible muscle architecture
change to influence the compound muscle action potentials during
muscle tetanic contractions.34,35 The time interval between 2
consecutive pairs was 15 seconds to ensure complete recovery of
the H-reflex.
Ankle CPM training was administered using a custom-made
training system. The axis of rotation was aligned with the anatomical
axis of the ankle joint. The frequency of motion was adjusted to 1.5
cycles per second, and the range of motion was kept at 5

displacement from neutral for a total ankle displacement of 10
.29,30
Subjects in the CPM group received 60 minutes of CPM
training of both legs per day, 5 days per week for 4 weeks at home
or the institute where they were accommodated. Subjects in the
control group received no training; however, they continued to
receive general health consultations. Except for the CPM training,
no other training or rehabilitation was given during the period of
the experiment. The daily log of CPM training was recorded and
verified every week. Subjects in the training group showed good
compliance to the training. In both the training and control groups,
subjects’ daily life activities remained the same as before they
participated in this study. The schedules for testing were the same
for both groups. The MAS score, H-reflex, and PAD were tested
prior to and after the 4 weeks of training. The posttraining test was
performed at least 24 hours apart from the last training session to
prevent an immediate effect.
At the end of the study, 1 of the subjects in the training group
was overtrained for an additional 8 weeks to complete 12 weeks
of training. For this subject, tests were done every 4 weeks
throughout the course of training.
All data were processed and analyzed offline. For the PAD of
the H-reflex, the peak-to-peak amplitude for each H-reflex was
obtained. For each pair of H-reflexes, the peak-to-peak amplitude
of the test H-reflex was normalized to the peak-to-peak amplitude
of the corresponding conditioning H-reflex.
A 2-way (time conditions  frequency) repeated-measures
analysis of variance was used to determine if the dependent
variable (PAD) was different between the time conditions (pretest
and 4wk) at each frequency tested in the 2 groups (training group
and control group). The post hoc Tukey analysis was used
whenever a significant main effect was found. The Wilcoxon
signed-rank test was used to analyze the change of MAS scores
before and after training. Statistical significance was considered to
be present at P<.05 in all the analyses.
Results
All subjects (mean  SD, 31.148.13y for the CPM training
group; 35.294.15y for the control group) completed this study
(fig 1). The time postinjury  SD of subjects in the training and
control groups were 20.411.1 and 29.116.8 months, respec-
tively (see table 1). All subjects had sustained a motor complete
SCI for at least 6 months (chronic SCI) prior to testing (see
table 1). None of them was taking antihypertonia medication
during the period of the study.
Prior to training, the H-reflex was not significantly depressed at
1Hz and 5Hz for both groups (P>.05), suggesting that the PAD
was impaired in these frequencies. The H-reflex was significantly
depressed to 41%45% and 63%62% only at 10Hz for the
training and control groups, respectively (P<.05). There was no
significant difference between the training and the control groups
at pretest conditions when compared statistically (F1Z.52,
PZ.485) (see table 1).
A lower ratio of test H-reflex/conditioning H-reflex represents
a stronger PAD. In the training group (nZ7), after 4 weeks of
CPM training, group data showed a lack of interaction between

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Continuous passive motion on spinal circuitry of SCI
Fig 1 Flowchart of the inclusion process of the SCI subjects.
the time and frequency factors when compared statistically
(F2Z.18, PZ.836). This suggests that the training induced similar
effects in the frequencies. Main effects showed that 4 weeks of
CPM training resulted in a significant increase in the amount of
PAD (F1Z7, PZ.038) when compared with pretest conditions
(fig 2). These results suggest that 4 weeks of CPM training
resulted in a restoration of the adapted PAD in individuals with
chronic SCI. The control group (nZ7) showed no changes in the
adapted PAD when tested 4 weeks apart (see fig 2).
Group data for the training group (nZ7) showed significantly
lowered MAS scores when the pretest (medianZ3, 25th percen-
tileZ3, 75th percentileZ4) and 4 weeks (medianZ3, 25th per-
centileZ2, 75th percentileZ4) conditions were compared
(PZ.013) (fig 3). This result suggests that 4 weeks of CPM
training resulted in a decrease in MAS scores, indicating
decreased hypertonia. Group data of the MAS scores for the
control (nZ7) group showed no change when the pretest
(medianZ4, 25th percentileZ3, 75th percentileZ4) and 4 weeks
(medianZ4, 25th percentileZ3, 75th percentileZ5) conditions
were compared (PZ.159) (see table 1).
The subject from the training group who completed 12 weeks
of CPM training showed that PAD restored prominently over the
first 4 weeks of training (see fig 3). After the fourth week of
training, PAD continued to increase at stimulation frequencies of
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825
1Hz and 5Hz, but to a lesser extent. No further increase in the
amount of PAD was observed for stimulation frequencies of 10Hz
after the fourth week of training.
Discussion
This study showed that 4 weeks of ankle joint CPM training
restored PAD of the soleus in individuals with chronic spastic SCI.
Moreover, the decrease of hypertonus was also observed after
training, which was evident by the decrease of the MAS score of
calf muscles and the clonus of ankle joints. The effects were
maintained in the subject who had been overtrained for 12 weeks.
After 4 weeks of ankle CPM training, we observed an increase
in PAD rather than restoration. Our results supported results from
previous studies in animal models19,27 and a human case report,28
showing that the restoration of adapted PAD is possible by means
of passive movement. To our knowledge, this is the first study that
presented group data with a control group demonstrating
successful restoration of PAD by means of CPM in humans with
chronic SCI.
Previous studies reported that passive cycling could restore
PAD in spinal cord transected animals19,27,37,38 and a human with
SCI. In the present study, we demonstrated successful restoration
826 Y-J Chang et al

1.8
pre test
4 weeks
test H-reflex/conditioning H-reflex

1.6 1.6

1.4 1.4

1.2 1.2

1.0 1.0

0.8 0.8

0.6 0.6

0.4 0.4

0.2 0.2

0.0
0.1 Hz 1 Hz 5 Hz 10 Hz 0.1 Hz 1 Hz 5 Hz 10 Hz

Training group (N=7) Control group (N=7)

Frequency
0.1 Hz
1 Hz
1.2
test H-reflex/conditioning H-reflex

5 Hz
10Hz
1.0

0.8

0.6

0.4

0.2

0.0
week 0 week 4 week 0 week 4

Time

Fig 2 PAD prior to and after training in the training and control groups. A lower ratio of test H-reflex/conditioning H-reflex represents
a stronger PAD. In the upper panel, the bars show mean and SDs of test-H-reflex amplitude normalized to their respective conditioning H-reflexes
in the training (nZ7) and the control (nZ7) groups during pretest (black bars) and 4 weeks (white bars) conditions at stimulation frequencies of
0.1Hz, 1Hz, 5Hz, and 10Hz. The lower panel shows that the ratio of test H-reflex/conditioning H-reflex decreases significantly after 4 weeks in the
training group but not in the control group.

of PAD using only ankle CPM training. Ankle CPM training
involves primarily repetitive motion of the ankle joint with
minimal motion over the knee and hip joints, whereas passive
cycling involves motion over multiple joints of the lower
extremity. From a biomechanical point of view, cycling in a seated
position involves an ankle displacement of approximately 15
,39
which was similar to the ankle joint displacement of 10
used in
the present study. In terms of training frequency, relatively more
cycles of ankle dorsiflexion/plantarflexion are performed per unit
time in ankle CPM training at the frequency of 1.5 cycles per
second compared with passive cycling at 60 rounds per minute
used in previous studies.19,28 Thus, our study suggests that the
adequate range of motion and repetition numbers of motion of
targeted treatment joints should be assured while using passive
cycling or other forms of passive training.
The subject who completed 12 weeks of CPM training showed
that the improvements in PAD mainly occurred in the initial 4
weeks and were maintained in the subsequent 8 weeks of training.
This duration of PAD restoration is comparable with those of
previous studies of passive cycling on spinal cord transected
animals,19,27,37,38 but is shorter than that of a case report by Kiser
et al28 in which PAD restoration began at 8 weeks of passive
cycling. Ankle CPM was selected over passive cycling, because
the movement type of ankle CPM is different from that of passive
cycling on the whole leg. It was easier for the ankle CPM to
control the range of motion of the target joint than whole leg

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Continuous passive motion on spinal circuitry of SCI
1.6
1.4
test H-reflex/conditioning H-reflex
1.2
1.0
0.8
0.6
0.4
0.2
0.0
0.1 1.0 5.0 10.0
HZ
Fig 3 PAD for 1 participant who completed 12 weeks of training.
The y axis showed the amplitude of test H-reflex normalized to their
respective conditioning H-reflexes. A lower ratio of test H-reflex/
conditioning H-reflex represents a stronger PAD. The x axis showed
the testing frequencies. The 4 lines represent the values at prior to, 4,
8, and 12 weeks of CPM training. Note that the prominent PAD pattern
was shown at 4 weeks of training. No significant improvement in PAD
was shown at 8 and 12 weeks of CPM training.
cycling involving multiple joints. However, both the Kiser study28
as well as our overtrained study were case reports. Whether there
will be extra gain in PAD after 4 weeks needs to be evaluated in
future studies with different designs.
The alterations in presynaptic inhibition and interneuronal
activity,19,27 as a result of passive training, may be the mecha-
nisms underlying restored PAD. The loss of supraspinal influence
after injury is thought to cause intrasegmental reorganization,
resulting in a loss of PAD. It has been suggested that there is
sufficient plasticity in the cord to allow restitution of reflex
modulation to occur using exercise training19 and that passive
cycling induces alternating contractions in the agonist and
antagonist muscles, providing recurrent signaling that possibly
modifies the hyperactive inhibition mechanisms in the SCI model,
thereby leading to a restitution of PAD.
After 4 weeks of ankle CPM training, the MAS scores were
improved in individuals with motor complete SCI, indicating
decreased spasticity. The MAS measures both spastic hypertonia
and the mechanical components of muscle stiffness.40 The effects
of neural components as a result of CPM training have been
shown through the successful restoration of PAD in the present
study. Although a direct causal relation between these spinal
circuit functions and spasticity has yet to be established, their
paralleled adaptations after injury to the spinal cord have
been suggested.
Other possible mechanisms underlying the reduction in MAS
scores could be the reduced sensitivity of muscle spindles.30 The
improvement in circulation resulting in the redistribution of the
more mobile tissue constituents, such as polysaccharides, and
water redistributed within the collagen framework more rapidly
during continuous motion41 could also be attributed to the reason
for improvements in MAS scores.
Although functional outcomes and the changes in quality of
life were not measured in this study, subjects participating in this
study did report some positive effects. All the participants in the
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827
CPM group reported that it was easier to perform self and/or
family-assisted passive range of motion exercise after the first
week of training. Four of the subjects in the training group
reported an improved quality of sleep because of fewer episodes of
Pre-test
lower-extremity spasm. Participants’ subjective statements sug-
4 weeks gested that the reduction of spasticity might translate to the
8 weeks
12 weeks
improvement in some aspects of quality of life. However, further
studies are needed for verification.
Study limitations
Limitations of this study should be kept in mind while interpreting
the results. First, the subjects included in this study had chronic
motor complete SCI. The individuals with acute and/or motor
incomplete SCI may not respond similarly to CPM training.
Second, although this study had overtrained a subject to 12 weeks,
the follow-up effects after the training and the best dosage for
setting clinical training guidelines, such as training duration and
number of sessions, should be further studied. Third, training
effects on quality of life and functional outcomes were not
included in this study. These issues are suggested to be addressed
in future studies.
Conclusions
The 4 weeks of CPM training is effective in restoring adapted
PAD and reducing MAS scores in humans with chronic motor
complete SCI. Although a direct link between the restoration of
normative spinal circuit function and the level of spasticity has not
been established, the results of the present study showed a paral-
leled restoration of spinal circuit functions and a reduction in
spasticity in individuals with chronic motor complete SCI.
Keywords
H-reflex; Motion therapy, continuous passive; Muscle spasticity;
Rehabilitation; Spinal cord injuries
Corresponding author
Ya-Ju Chang, PhD, 259 Wen-Hwa 1st Rd, Kwei-Shan Taoyuan,
Taiwan. E-mail address: yjchang@mail.cgu.edu.tw.
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