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ORIGINAL REPORT
Background: The aim of this study was to investigate the rehabilitation benefit by 69.7%. Self-reported benefits were
integration of motor function and spasticity assessment of cited by 26 participants and included increase in fitness, quality
individuals with spinal cord injury into cycling therapy. of life, confidence and social contact (3).
Methods: Twenty-three participants with incomplete spinal Sport activities that are usually offered for clients in rehabili-
cord injury performed 18 training sessions (standard devia- tation centres mainly address the upper extremities and conse-
tion (SD) 14) on an instrumented tricycle combined with quently do not prevent atrophy and functional changes in leg
functional electrical stimulation. Each therapy session in- muscles and decrease in bone density in the lower extremity.
cluded a power output test to assess the participants’ ability As the muscle mass of the lower body is more than 50% of the
to pedal actively and a spasticity test routine that measures total muscle mass (4), it is important to include the lower limbs
the legs’ resistance to the pedalling motion. In addition, the
to achieve training effective heart rates. Specific training with
required time for the therapy phases was monitored.
functional electrical stimulation (FES) can cause significant
Results: The results of the power output test showed a month-
improvements in the cardiovascular and pulmonary systems
ly increase in power output of 4.4 W (SD 13.7) at 30 rpm and
(5, 6), reduce atrophy of skeletal muscle (7, 8), increase bone
18.2 W (SD 23.9) at 60 rpm. The results of the spasticity as-
sessment indicate a 12.2 W (SD 9.7) reduction in resistance density and lead to psychological benefits (9–13).
at 60 rpm after the functional electrical stimulation training FES cycling is a suitable training method for the lower ex-
for the subject group with spasticity. tremities of individuals with SCI, as, in contrast to walking,
Conclusion: In clinical use over a time-period of 2 years this problems with balance can easily be avoided by appropriate
combined form of therapy and motor function assessment seat design, and muscle force is converted into drive power
was well accepted by participants. The active power output with relatively high efficiency during pedalling. Mobile cy-
test and the spasticity test routine offered a proper tool to cling by means of FES is attractive for individuals with SCI,
monitor participants’ progress in functional rehabilitation as it allows them to move independently with power gener-
and changes in spasticity. ated by their own leg muscles. FES cycling ergometers are
Key words: spasticity; SCI; paraplegia; tetraplegia; FES; cy- commercially available; the first commercialized leg cycling
cling; 10MWT. exercising system was ERGYS (Therapeutic Alliances Inc.)
in 1984. However, cycling training with FES is assumed to be
J Rebahil Med 2012; 44: 444–449
time-consuming and complex and is only applied in clinical
Correspondence address: Werner Reichenfelser, Getreidemarkt routine to a moderate extent.
9/307/3, AT-1060 Wien, Austria. E-mail: werner.reichefelser@ The periodic assessment of the functional abilities of indi-
tuwien.ac.at viduals with SCI is important in order to monitor rehabilitation
Submitted September 12, 2011; accepted January 31, 2012 progress and to evaluate existing and new therapy approaches.
To assess, for example, walking ability, the 6-Minute Walk Test
(6MWT) or the 10-Metre Walk Test (10MWT) are established
Introduction
(14). The Walking Index for Spinal Cord Injury (WISCI II)
One of the major challenges in the rehabilitation of individuals scores the amount of physical assistance, braces or devices
with spinal cord injury (SCI) is to improve functional inde- required for walking over a distance of 10 m. It is an SCI-
pendence and prevent the deterioration of musculoskeletal and specific test and covers the entire range of walking ability
cardiovascular systems. Cardiovascular disease is an increasing (15) with levels 0 (client is unable to stand and/or participate
cause of mortality in chronic SCI (1). O’Neill & Maguire (2) in assisted walking) to 20 (ambulates with no devices, no
reported that the general benefit of sporting activity in clinical braces and no physical assistance over a distance of 10 m).
rehabilitation was recognized by 78.8% of participants and the For the neurological and functional status, the American Spinal
Injury Association Impairment Scale (AIS) is also used. This (AnthroTech Leichtfahrzeugtechnik GmbH, Eckental, Germany) that
is a 5-point ordinal scale that classifies individuals from A was adapted to meet the special requirements to enable measurements
and to perform FES cycling training for persons with SCI.
(complete SCI) to E (normal sensory and motor function) (16).
The drive unit can brake or propel the crank with defined torque,
Nevertheless, van Hedel (17) points out that testing of func- keep it at constant angular velocity or hold the crank in a defined
tional outcome, as provided by these scores, can be improved angular position for isometric measurements. For safety reasons the
by interval-scaled measurements. maximum torque is limited by the motor control. The therapist can
In matters of clinical spasticity assessment the currently used operate different training modes and specified test routines via a laptop.
For an easier transfer the correct steering rod can be swivelled down
scales, e.g. Penn Spasm Frequency Scale (PSFS) or Modified and a transfer board can be hugged onto the frame.
Ashworth Scale (MAS), correlate poorly with each other The power applied to the pedals is measured via the induced drive
(18). Both intra- and inter-tester repeatability of the MAS are current. The angle encoder at the crank axis transmits the actual crank
questionable (19, 20). Biering-Sorenson et al. (20) also point angle to the 10 channel stimulator, which stimulates the involved
out the need of simple instruments, which provide a reliable muscles in predefined crank angle ranges. The system can be used as a
stationary cycle fixed on a rack or as a mobile FES cycle. The drivers’
quantitative measure with a low inter-rater variability. A reli- legs are stabilized on the pedals via orthoses.
able method for the quantification of spasticity could support
the neurologist’s decision on the type and dose of anti-spastic Participants
medication. The study was approved by the ethics review board of Lower Austria.
The aim of this study is to integrate reliable and easy assess- Twenty-six persons with incomplete SCI gave written consent to
participate in the study. Three participants could not continue after
ment of both the participants’ motor function, as an indicator
the first therapy session because of instability of the upper body and
for the progress of rehabilitation, and spasticity into FES lack of time. Twenty-three participants (7 tetraplegic, 16 paraplegic,
cycling training. An instrumented FES cycling and measure- 3 females, 20 males, mean age 40 years (standard deviation (SD) 14),
ment system was used that can be applied as both a stationary lesion height: L1 to C4, AIS Score: B–D, time since injury: 9 (SD 7)
cycling ergometer and a mobile FES cycle, which gives the months) performed training sessions 3 times a week over an average
time-period of 2 months. Table I lists the participants and gives infor-
system high flexibility and allows the training to be adapted to mation on gender, age and SCI status. For the spasticity assessment the
the users’ needs and preferences. Predefined test- and training MAS scale was chosen where the scorer passively moves the tested
routines are thought to combine the positive physiological ef- limb and rates the level of stiffness with 0 (no increase in muscle
fects of the cycling training with the assessment of clinically tone), 1, 1+, 2, 3 or 4 (affected part(s) rigid in flexion or extension)
meaningful parameters within an acceptable expenditure on (22). For this study, the therapist manually moved the lower legs of
the participant and quantified the passive resistance of the knee joints
time and effort for both patient and therapist. according to the MAS scale. The mean MAS stands for the MAS scores
averaged over all performed therapy sessions (1.5 was set for the MAS
score 1+ to allow a mathematical calculation of the mean value). The
Material and Methods participants with a mean MAS < 1 form the non-spastic and those with
a mean MAS ≥ 1 the spastic SCI group (Table I).
Cycling and measurement system
In addition, a control group of 13 able-bodied participants (4
For this study an instrumented FES-cycling system (21) was applied females, 9 males, mean age 35 years (SD 9)) performed the training
(Fig. 1). The system is based on a commercially available tricycle session twice. Their mean results from the spasticity test routine are
compared with the spastic and the non-spastic SCI groups.
J Rehabil Med 44
446 W. Reichenfelser et al.
is shifted 180º. Due to the activation dynamics (24) of the muscles lated by subtracting the passive from the active drive torques multiplied
the stimulator shifts the stimulation start and end points prior to the by the angular velocity. Next, the same test is performed at a cadence
set values. This shift depends on the activation and deactivation time of 60 rpm. The results of active pedalling at the two cadences, 30 and
constants of the muscle and the actual cadence of the crank and satis- 60 rpm, are used to examine both the development of muscular force
fies the equation E2.1 [units in rectangular brackets]. For the applied and the participant’s coordinative progress. The increase in active
stimulation the activation and deactivation time constants were set to muscle force is mainly reflected by the power output test at 30 rpm.
0.12 and 0.08 s, respectively (25). In addition, at 60 rpm the coordinative progress of the participant can
E2.1: shift [º] = (de)activation time constant [s] × 60 × cadence be quantified. Due to muscle activation dynamics the optimal timing
[rpm] of muscle contraction is more difficult at higher velocities and, con-
The applied stimulation signal consists of rectangular biphasic pulses sequently, the better the participants’ coordinative abilities the higher
with a frequency of 50 Hz and pulse duration 600 µs. The amplitude the power output at higher cadences. Healthy individuals without any
is set to a level at which the stimulation is not uncomfortable for the motor disorders can generate higher active power during pedalling at
participant, but a clearly visible contraction of the stimulated muscle 60 rpm than at 30 rpm (26). Periodical active power output tests over a
group occurs. For the reported group the mean amplitude was 39 mA longer time-period allow monitoring the motor rehabilitation progress
(SD 11). of each individual participant.
Subsequently, the participant performs the active power output test, Next a 5-minute training is performed with constant motor torque
which is carried out without stimulation and runs at two isokinetic and FES (constant torque training), where the motor supports or brakes
cadences. First, the participant is propelled passively for 10 revolutions the system with constant torque depending on the physical abilities
at constant 30 rpm to assess the necessary drive torque for passive of the participant. The motor support or motor resistance is set by the
movement. An acoustic signal advises the participant to start active therapist in a current range of ±1000 mA to enable the participant to
pedalling with maximal effort during 10 isokinetic crank revolutions. perform a smooth pedalling motion. Before the concluding spasticity
The mean power output generated by the active muscle forces is calcu- test, the isokinetic training is repeated for 5 min.
Therapy session
J Rehabil Med 44
Monitoring of spasticity in incomplete SCI 447
30
Results
20
at 30 rpm
Time needed for therapy sessions at 60 rpm
10 Linear (at 30 rpm)
The mean time needed for one therapy session was calcu-
Linear (at 60 rpm)
lated from 417 therapy sessions with 23 participants. Each 0
participant attended a mean of 18 therapy sessions (SD 14). 0 7 14 21 28 35 42
The pre-training phase took 10.7 min (SD 4.2) and the post- Days since start of therapy
training phase 7.6 min (SD 3.3). The training phase required Fig. 4. Results of the active power output test at 30 and 60 rpm for a subject
33.6 min (SD 6.1). with incomplete tetraplegia (male, 55 years, lesion height C6, American
Spinal Injury Association Impairment Scale: C) over a therapy time-period
of 1.5 months. The related linear trend lines have been added.
Monitoring of the rehabilitation progress via the active power
output test
As an example, Fig. 3 shows the results of the active power values. The monthly increase in power output averaged over
output test of a 53-year-old man with an incomplete spinal all participants was 4.4 [W] (SD 13.7) at 30 rpm and 18.2 [W]
cord lesion at TH11. The ascending linear trend lines picture (SD 23.9) at 60 rpm. The enhanced power output also encour-
the continuous progress in power output over the therapy aged the participants’ performance in mobile FES cycling at
time-period of 5 months. the end of the study period.
Fig. 4 shows the results of the active power output test for a
participant with incomplete tetraplegia (male, 55 years, lesion Results of the spasticity assessment
height C6, AIS C) over a therapy time-period of 1.5 months The bar chart in Fig. 6 expresses the results of the spasticity test
with progressive linear trend lines. routine for the test participants divided into 3 groups. Group
Fig. 5 shows the results of a participant who had already A includes 8 individuals with SCI and mean MAS > 1 (Table
started FES cycling therapy by 2 months after injury, with I, mean MAS 2.0 (SD 0.4)), group B 15 individuals with SCI
decreasing power output at 30 rpm. and mean MAS < 1 (mean MAS 0.2 (SD 0.2)) and group C
The active power output results of the 20 further participants 13 able-bodied individuals. The decrease in resistance to the
differ only by the dynamic of the progress and by their absolute passive movement is calculated for each test subject at each of
90 180
80 160
70 140
Power output [W]
Power output [W]
60 120
50 100
40 80
30 60
20 at 30 rpm 40 at 30 rpm
at 60 rpm at 60 rpm
10 Linear (at 30 rpm) 20 Linear (at 30 rpm )
Linear (at 60 rpm) Linear (at 60 rpm)
0 0
0 14 28 42 56 70 84 98 112 126 140 0 7 14 21 28 35 42 49 56 63
Days since start of therapy Days since start of therapy
Fig. 3. Results of the active power output test at 30 and 60 rpm for a subject Fig. 5. Results of the active power output test at 30 and 60 rpm of a
with incomplete paraplegia (male, age 53 years, lesion height T11, American subject with incomplete paraplegia (male, 47 years, lesion height L1,
Spinal Injury Association Impairment Scale: C) over a therapy time-period American Spinal Injury Association Impairment Scale: D) over a therapy
of 5 months. The related linear trend lines have been added. time-period of 2 months.
J Rehabil Med 44
448 W. Reichenfelser et al.
Modified Ashworth Scale value using the device as a mobile cycle in the gymnasium of the re-
Mean decrease of passive resistance after cycling
19 >1 (spastic)
habilitation centre the stimulation amplitude and, consequently,
Group B: individuals with
spinal cord injury and a mean the FES induced power output, was limited by the sensibility of
15
Modified Ashworth Scale value the participants. Therefore the driving speed of the participants
<1 (non-spastic)
with AIS B was slow; for the participants with AIS C and D a
Group C: able-bodied
individuals higher speed could be reached due to the additional torque they
11 could produce by active muscle force.
To quantify this contribution the active power output test
proved to be an effective tool that can be also used to document
7
the participants’ progress in motor rehabilitation. Due to the
measurements at two different crank velocities it is possible
3 to analyse the development of the muscle forces as well as the
coordinative status during rehabilitation. The results depicted in
Fig. 3 show that the power output is higher at 60 rpm than at 30
-1 10 20 30 40 50 60 rpm, indicating that the participant’s coordinative abilities are
Cadence of crank [rpm]
good. In Fig. 4 a constant progress in force and coordination is
Fig. 6. The bar chart represents the instantaneous decrease in passive pointed out, but the power output is lower at 60 rpm than at 30
resistance [W] due to the functional electrical stimulation (FES) cycling
rpm. This indicates that the participant has problems coordinat-
training. For each training session the decrease in passive resistance was
calculated by subtracting the resistance values measured with the spasticity ing the leg muscles at higher cadences. The reason for this effect
test routine at the end of the training session from the respective values at may be decreased trunk stability due to the lesion height C6. In
the beginning of the training session. The bars depict the mean values with Fig. 5 the decrease in power output at 30 rpm may be caused by
standard deviations (SD) of these results for the 3 groups of participants the reduction in muscle mass in the first months after the injury.
and for the 6 tested crank cadences. The spastic group A (8 individuals However, the increasing values at 60 rpm highlight progress in
with spinal cord injury and a mean Modified Ashworth Scale (MAS) value the participant’s coordinative abilities. Further investigation
> 1, averaged mean MAS = 2.0, SD 0.4) shows the highest decrease in
could focus on the correlation between cycling and walking
passive resistance after the FES cycling training. The difference from the
non-spastic groups B (15 individuals with spinal cord injury and a mean abilities, e.g. by comparing the described power output test with
MAS value < 1, averaged mean MAS = 0.2, SD 0.2) and C (13 able-bodied the 6MWT, the 10MWT or the WISCI II.
individuals) increases at higher cadences. The results of the spasticity assessment show that the resist-
ance of the legs to the passive pedalling movement is decreased
the selected cadences by subtracting the mean value from the in the spastic group after the FES cycling training. The relaxa-
spasticity test routine at the end of the training session from tion increases with velocity, which indicates that spasticity,
the respective value at the beginning of the training session. which is usually velocity-dependent, may be decreased. These
The resulting values represent the instantaneous decrease in results agree with the findings of Krause et al. (27). The de-
passive resistance due to the FES cycling training. The spastic crease in resistance in the able-bodied group showed slightly
group A clearly shows the greatest reduction in resistance after higher values than in the non-spastic SCI group, which may
the FES training and the difference from the other two groups be caused by difficulty in relaxing completely when being
increases at higher cadences. Groups B and C show very similar pedalled during the assessment. Further research is required
results. The legs’ resistance to the passive pedalling motion in order to quantitatively assess spasticity with the described
is also decreased after the FES cycling training for the non- approach and to find related long-term effects of FES cycling
spastic groups B and C, but the values are much lower than on spasticity.
for the spastic group A.
Limitations of this study
J Rehabil Med 44
Monitoring of spasticity in incomplete SCI 449
It should also be pointed out that the contribution of the FES during exercise of the paralyzed lower limbs. Paraplegia 1995;
cycling therapy to the monthly increase in power output can- 33: 90–93.
11. Malagodi MS, Ferguson-Pell MW, Masiello RD. A functional
not be quantified using this study design, because, on the one
electrical stimulation system designed to increase bone mineral
hand, the healing process of incomplete SCI is still in progress density. IEEE Transactions on Rehabilitation Engineering 1993;
9 months after injury and, on the other hand, the participants 1: 1–7.
also attended numerous other therapies in parallel. 12. Twist DJ, Culpepper-Morgan JA, Ragnarsson KT, Petrillo CR,
In conclusion, these results show that the introduced system Kreck MJ. Neuroendocrine changes during functional electrical
stimulation. Am J Phys Med Rehabil 1992; 71: 156–163.
might be a valuable tool in clinical rehabilitation, allowing the 13. Sipski ML, Delisa JA, Schweer S. Functional electrical stimulation
physiological benefits of FES cycling training to be combined bicycle ergometry: patient perceptions. Am J Phys Med Rehabil
with reliable assessment of clinically significant parameters, 1989; 68: 147–149.
and acceptable expenditure of time and effort for both the 14. van Hedel HJ, Wirz M, Dietz V. Assessing walking ability in sub-
client and the therapist. jects with spinal cord injury: Validity and reliability of 3 walking
tests. Arch Phys Med Rehabil 2005; 86: 190–196.
15. Ditunno PL, Ditunno Jr JF. Walking index for spinal cord injury
(WISCI II): scalerevision. Spinal Cord 2001; 39: 654–656.
Acknowledgements 16. Marino RJ, Barros T, Biering-Sorensen F, Burns SP, Donovan
WH, Graves DE, Haak M, Hudson LM, Priebe MM. International
The authors would like to thank all participants for their active attendance standards for neurological classification of spinal cord injury. J
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Basilio for carrying out the therapy sessions. 17. van Hedel HJA, Wirz M, Curt A. Improving walking assessment
This study was supported by the research fund of the Workers Com- in subjects with incomplete spinal cord injury: responsiveness.
pensation Board (AUVA), Austria. Spinal Cord 2006; 44: 352–356.
18. Priebe MM, Sherwood AM, Thornby JI, Kharas NF, Markowski
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J Rehabil Med 44