Volume 87, Issue 2 , Pages 222-228, February 2006
Comparison of Electric Stimulation Methods for Reduction of Triceps Surae Spasticity in Spinal Cord Injury
Article Outline
Abstract
van der Salm A, Veltink PH, IJzerman MJ, Groothuis-Oudshoorn KC, Nene AV, Hermens HJ. Comparison of electric stimulation methods for reduction of triceps surae spasticity in spinal cord injury.
Objectives
To compare the effect of 3 methods of electric stimulation to reduce spasticity of the triceps surae in patients with complete spinal cord injury (SCI) and to investigate the carryover effect.
Design
Placebo-controlled study with repeated measurements after the interventions.
Setting
Research department affiliated with a rehabilitation hospital in the Netherlands.
Participants
Ten patients with a complete SCI were recruited from the outpatient population of the rehabilitation hospital. All subjects had American Spinal Injury Association grade A impairment scores, except for one, who had grade C. The patients had no voluntary triceps surae contractibility.
Interventions
Forty-five minutes of cyclic electric stimulation of the agonist, antagonist, or dermatome of the triceps surae or a placebo approach.
Main Outcome Measures
Outcome measures were the Modified Ashworth Scale (MAS), clonus score, and the H-reflex and M wave (H/M) ratio. The electromyographic response to a stretch of the soleus over the whole range of motion was also determined. The magnitude and ankle angle at which the electromyographic response started were calculated.
Results
Stimulation of the agonist provided a significant reduction in the MAS compared with the placebo approach (P<.001). There was no significant change in the H/M ratio or the electromyographic response amplitude after any of the stimulation methods, whereas stimulation of the antagonist muscle resulted in a significant reduction in the ankle angle at which the electromyographic response started, compared with the placebo approach (P<.037).
Conclusions
Triceps surae stimulation reduces the MAS for that specific muscle, whereas the angle at which the reflex starts changes after antagonist stimulation.
Key Words: Electric stimulation , Muscle spasticity , Neurophysiology , Rehabilitation , Spinal cord injuries
MANY TREATMENT MODALITIES are available to reduce spasticity, such as oral medications, chemodenervation and neurolysis, implanted pumps, physical therapy, and surgery. They are applied to reduce spasticity or to treat contractures that result from spasticity.1, 2 In addition to these treatment modalities, therapeutic electric stimulation is also known to reduce spasticity.3 There are several advantages of electric stimulation compared with the other treatment modalities. It can modulate the intensity of the intervention, and therefore the intensity of the effect. This also implies that the spasticity can be modulated instead of totally eliminated. Thus, patients have the potential ability to use the residual muscle tone for function. A second advantage of electric stimulation is the local application. Oral medication, on the other hand, will influence the tonus in all the muscles in the body. The disadvantages of electric stimulation are discomfort for the patient during stimulation and the limited duration of the effect.
In the past, several studies were performed to determine the effect of electric stimulation on spasticity in patients with a spinal cord injury (SCI),3, 4, 5, 6, 7, 8, 9, 10, 11, 12 including studies with whole-hand stimulation (Mesh glove) and transcutaneous electric stimulation. These studies found a positive effect of stimulation in patients with SCI. Pre- and postintervention assessments were made in all the studies to measure the effect of electric stimulation. However, only 1 placebo-controlled study has been reported.9
The methods used for stimulation in these studies differ greatly. Some studies7, 8, 10, 13 describe stimulation of the antagonistic muscle. Antagonist contraction is known to have an inhibitory effect on the agonist muscle,14 and several studies confirm that this so-called reciprocal inhibition is decreased in spastic patients.15, 16, 17, 18, 19 To enhance the reciprocal inhibition in these patients, antagonistic muscle stimulation may be beneficial. In other studies, the dermatome related to the spastic muscle was stimulated,5, 11 using an inhibitory neurophysiologic pathway that is activated by sensory afferents from the low-threshold sensors in the skin.20 These afferents have an inhibitory effect on the muscles related to the same neurologic segment.5 Stimulation of the spastic muscle itself, which is also a method of treatment,6 is based on recurrent inhibition.3 This is thought to be caused by the Renshaw cell, which has a negative feedback loop to the α-motoneuron,14 and this mechanism is found to be decreased in spastic patients.21, 22, 23, 24 Agonist muscle stimulation can be used to enhance the recurrent inhibition as an inhibitory pathway for the agonist muscle. The parameters used for stimulation also differed among the studies, suggesting that the optimal method of stimulation has not yet been identified.
The goal of this study was to determine the effect, in general, and the carryover effect of electric stimulation to reduce spasticity in the triceps surae in patients with SCI. The effects of 3 different methods of electric stimulation were also compared: agonist, antagonist, and dermatome stimulation. Spastic hypertonia was assessed using the Modified Ashworth Scale (MAS), the clonus score, and the H-reflect and M wave (H/M) ratio. In addition, the electromyographic response to a stretch of the soleus muscle over the whole range of motion (ROM) was assessed and the response magnitude and the threshold angle were determined. These measurements were chosen for their neurophysiologic and clinical relevance, measuring either the reflex sensitivity or the mechanical components of muscle stiffness.
Methods
Participants
Patients with SCI were recruited from the database of a rehabilitation center in the Netherlands (Het Roessingh, Enschede). Inclusion criteria were presence of spasticity (MAS grade of ≥1), absence of voluntary contractibility in the triceps surae, time since injury at least 6 months, ability to contract triceps surae muscles and tibialis anterior muscle with electric stimulation, and over 18 years of age. The patients were allowed to take antispasticity medication, but they were asked not to change the dosage within 2 weeks before and during the study period. Patients with hypersensitive skin on the legs, with equinus deformity, or conditions that could temporally increase tonus (specifically bladder infection) were excluded. All patients gave informed consent to participate in the study, which was approved by the local ethics committee.
The database was screened for information about the presence, level, and chronicity of spasticity in the legs, the age of the patient, and any possible reason for exclusion. This screening was performed by a physical medicine and rehabilitation physician and a researcher. The patients who met the inclusion criteria were invited to participate in the study by letter, and 1 week later they were contacted by telephone. The other inclusion and exclusion criteria were assessed by means of a questionnaire and an intake screening. The presence of spastic hypertonia and passive muscle stiffness were measured with the MAS, and inability to voluntarily contract the triceps surae was confirmed. Excitability of the triceps surae and the tibialis anterior with electric stimulation was also determined.
Design
Each patient received the interventions on 4 separate days, with an average interval of 7 days (range, 3–14d). According to the literature, the washout period of the effect of the electric stimulation may last as long as 24 hours.3 A minimum of 72 hours between 2 subsequent interventions was considered to be long enough to ensure that the effect of the former intervention had disappeared. For each patient, the interventions started with a baseline measurement session at the same time each day. Sequentially, patients received 1 of the 3 methods of stimulation (agonist stimulation, antagonist stimulation, dermatome stimulation) or a placebo approach. A second measurement session followed immediately after the intervention. After this, 2 more measurements were performed at intervals of 1 hour (fig 1). The patients received 2 different sequences of stimulation over the 4 days. Half of them received the sequence shown in figure 1, and the other half received this sequence in reverse.
Fig 1.
Design of the study. The patients came on 3 or 4 days, and on each day another intervention was applied: agonist stimulation, antagonist stimulation, dermatome stimulation, or a placebo approach. Each day started with a baseline measurement session followed by an intervention. The first postmeasurement session took place immediately after the intervention, and the second and third postmeasurement sessions with 1-hour intervals.
Stimulation Methods
Three methods of stimulation were compared in this study: stimulation of the antagonist (ipsilateral tibialis anterior), stimulation of the agonist (ipsilateral triceps surae), and dermatome stimulation (ipsilateral S1 dermatome on the lateral side of the foot) (fig 2). For the muscle stimulation (tibialis anterior, triceps surae), the electrodes were applied on the belly of the muscle, just proximal to and distal of the motor point. For dermatome stimulation, 1 electrode was applied just below the lateral malleolus and the other just proximal to the base of the fifth toe (metatarsophalangeal joint V) (see fig 2). For the dermatome and tibialis anterior, stimulation the size of the electrode was 5×5cm, and for the triceps surae stimulation the size of the electrodes was 5×9cm. We used self-adhesive electrodes.a
Fig 2.
Application of the stimulation electrodes for antagonist (tibialis anterior), agonist (triceps surae), and dermatome (S1) stimulation.
The stimulation parameters are presented in table 1. Absolute maximum of the stimulator was 100mA. In some cases, when a simulation of 3 times the motor threshold evoked spasms, the stimulation amplitude was set just below the level at which the spasms occurred. During the interventions, the ankle joint was fixed on a footplate to prevent movements.
Table 1. Stimulation Parameters
| Parameter | Agonist Stimulation | Antagonist Stimulation | Dermatome Stimulation |
|---|---|---|---|
| Pulse width (μs) | 300 | 300 | 100 |
| Pulse rate (Hz) | 30 | 30 | 30 |
| Burst duration (s) | 4 | 4 | 4 |
| Ramp-up time (s) | 1 | 1 | 1 |
| Pause duration (s) | 4 | 4 | 4 |
| Total duration (min) | 45 | 45 | 45 |
| Intensity | 300% MT | 300%MT | 80%MT |
The placebo approach was performed in the same way as the stimulations. All the electrodes and wires were applied and the stimulation intensity was increased, but the device was not turned on. This was unknown to the patients, and they could not feel whether there was stimulation because they had complete lesions. Moreover, the limb was covered with a towel so that they were not able to see contractions of the muscles.
Modified Ashworth Scale
We used a Dutch translation of the MAS for the measurement of spastic hypertonia.25 During all measurements, the patients were seated upright with the knee flexed at 75° (full extension was defined as 0°). In 2 cases, the knee was kept in extension during the measurement. These patients had insufficient trunk stability to sit in the device, so they were measured in their wheelchairs. The validity and reliability of the MAS has been found to be marginal in the lower limb.26 To increase reliability, only 1 experienced physical therapist performed the MAS measurement during all sessions.27 The observer was blinded for the interventions. For the numerical analysis of the MAS, the 1+ value was ascribed as 2, thus MAS 2 was ascribed as 3, and so forth.
Clonus Score
The same observer assessed whether the patients suffered from clonus of the triceps surae muscle. The clonus was elicited by a rapid perturbation with sustained pressure. The observer determined whether the clonus was maintained for more than 5 seconds or whether the clonus disappeared. Thus, the clonus score was: 0, no clonus; 1, self-limiting clonus; or 2, sustaining clonus.
H-Reflex Measurement
To measure the H/M ratio, a stimulus was applied to the tibial nerve in the popliteal fossa. The optimal location was sought with a handheld probe and, when it was found, an electrodeb was placed on this location. The inactive electrode was a self-adhesive 5×9cm electrode placed directly above the ipsilateral patella. For the H-reflex measurement a rectangular biphasic pulse, with a pulse width of 1000μs, was applied.
For the electromyography, we applied Ag-AgCl gel, self-adhesive electrodesb with a diameter of 12mm, and used a bipolar arrangement with an interelectrode space of 20mm. The ground electrode was applied to the ipsilateral medial malleolus. Before application, the leg was shaved and the skin was abraded and cleaned with alcohol. A strict protocol was followed for placement of the electrodes.28 The sample frequency of the electromyographic activity was 2048Hz, and the data were band-filtered at 20 to 200Hz.
The amplitude of the H-reflex and M wave were determined by calculating the peak-to-peak value from the electromyographic signal at appropriate delays after the stimulus. The stimulation intensity was increased in steps of 5 to 10mA. After saturation of the M wave was achieved, the maximum H-reflex was determined. Approximately 15 stimuli were given, at a rate of less than 0.1 pulses per second, until an appropriate H/M graph was obtained.
The maximum H-reflex (Hmax) and maximum M wave (Mmax) were determined, and the H/M ratio was calculated according to the following formula29, 30:
The validity of the H/M ratio as a value for the reflex excitability may be diffused by muscle fatigue,29 but the reliability of the H/M ratio of the soleus muscle is good.31
Stretch Reflex
SetupThe muscle response was measured during a stretch of the soleus muscle over the whole ROM at several speeds.32 Patients were seated upright with the knee flexed at 75°. In 2 cases, the knee was kept in extension during the measurement. These patients had insufficient trunk stability to sit in the device, so they were measured in their wheelchairs. The foot was strapped on a footplate that rotated around the ankle joint; for the measurement, the footplate was moved in dorsiflexion, thus stretching the triceps surae. In 1 session, 30 to 45 stretches were applied at various different velocities, ranging from 30°/s to 150°/s.
Data recording and analysisElectromyographic activity was recorded in the soleus muscle, similar to the measurement of the H/M ratio. The filtered electromyographic signal was searched for bursts with a threshold value, defined as 3 times the standard deviation (SD) of the noise level. When a burst was found during the stretch movement the root mean square (RMS) value was calculated over a window of 100ms (200 samples), subsequent to the moment at which the threshold was passed. The RMS responses increased exponentially with increasing velocities. An exponential curve fit was estimated, and an average response value at a velocity of 100°/s (EMG100) was determined with this fitted line.32
Another outcome was the reflex-initiating angle, which was defined as the angle at which a reflex was generated, resulting in an actual electromyographic response at an average stretch velocity of 100°/s. The reflex-initiating angle outcome was the angle 45ms before the start of the electromyographic burst.33 The position in which the ankle had no plantar- or dorsiflexion (anatomic position) was defined as 0°. This 45-ms delay was incorporated to include the time between the initiation of the reflex and the actual electromyographic response. This outcome is comparable to scores on the Tardieu scale that is used in clinical practice.34 This scale measures fast, manually applied stretch movements, similar to the stretch of 100°/s we used to determine the reflex-initiating angle.32
Statistical Analysis
The outcomes of the MAS, clonus score, H/M ratio, EMG100, and reflex-initiating angle were analyzed with a linear mixed model.35 The following factors were included in the model as fixed factors: sequence of the interventions, initial (baseline) values, interventions, time, and the interaction between intervention and time. We used this interaction to determine the effect of the intervention on the change in the outcomes over time, that is, the carryover effect. The factor patient was included as a random factor in the linear mixed model. The intervention effect was analyzed with the same linear mixed model after removal of the interaction term.
For both comparisons (carryover effect, intervention effect), post hoc tests were performed in which the interventions were compared with the placebo approach. The level of significance was defined as 5%.
Results
Participants
Thirty-three patients were found to be suitable for inclusion according to the files and were contacted. Sixteen patients were not willing to participate because of other commitments or lack of interest. Seventeen patients were seen for intake, 7 of whom were excluded because of lack of spasticity in the triceps surae muscles. Finally, 10 of the selected patients participated in the study. The demographic data of these patients are presented in table 2. Two patients were unable to attend all 4 measurement days and, therefore, 2 sessions in which the effect of the agonist stimulation was measured were missed.
Table 2. Demographic Data
| Patient | Sex | Age (y) | Injury Level | ASIA Grade | Time Since Injury (mo) | MAS Score | Clonus |
|---|---|---|---|---|---|---|---|
| 1 | M | 36 | T4 | A | 71 | 1+ | Yes |
| 2 | M | 30 | T5 | C | 33 | 1 | No |
| 3 | M | 42 | C6 | A | 211 | 1+ | Yes |
| 4 | M | 30 | C6-7 | A | 28 | 3 | Yes |
| 5 | F | 41 | T8 | A | 208 | 1+ | No |
| 6 | M | 37 | T11 | A | 217 | 1 | Yes |
| 7 | M | 34 | C6 | A | 105 | 3 | Yes |
| 8 | F | 21 | C5 | A | 97 | 1 | Yes |
| 9 | M | 41 | T4-5 | A | 275 | 1 | No |
| 10 | M | 41 | C3-4 | A | 150 | 1 | Yes |
Effect of Electric Stimulation
Clinical scalesNone of the participants reported adverse effects or increased spasms after any of the interventions. On the MAS, a significant intervention effect was found (P<.001; fig 3), but the clonus score showed no significant intervention effect (P<.21). Post hoc tests for the MAS showed that only the agonist stimulation differed significantly from the placebo approach (P<.001). It was found that the group average on the MAS decreased from 1.6 to 0.9 (46% reduction) immediately after stimulation of the agonist. However, given the rather mild grades of spasticity, this reduction may be of limited clinical relevance. No significant carryover effect was found on the MAS or the clonus score (n=10, P<.113; n=10, P<.586; respectively).
Fig 3.
Effect of the stimulations and placebo approach for the (A) MAS, (B) clonus score, (C) H/M ratio, (D) EMG100, and (E) reflex-initiating angle. Presented are baseline, and post 1, 2, and 3 measurement outcomes. Values are average with 1 SD. The SD is mainly due to intersubject variability. Significant differences were found in intervention effect (IE) of the MAS and reflex-initiating angle. For the MAS, post hoc tests indicate significant differences in intervention effect between the placebo approach and agonist stimulation (IE Pl-Ag). For the reflex-initiating angle, a significant difference in intervention effect was found between the placebo approach and antagonist stimulation (IE Pl-Ant). Abbreviation: stim, stimulation. *P<.05; †P<.001.
The H/M ratio showed no significant changes in the intervention effect or carryover effect (n=7, P<.31; n=7, P<.43; respectively) because only minimal changes were present (see fig 3). The EMG100 outcomes showed no significant changes for either the intervention effect (P<.60) or the carryover effect (n=8, P<.79). The reflex-initiating angle showed a significant change for the intervention effect (n=8, P<.015), but the carryover effect was not significant (n=8, P<.14). Post hoc tests for the intervention effect showed that antagonist stimulation resulted in a significant change, compared with the placebo effect (P<.037). The reflex-initiating angle changed from 18.6° to 15.2° of plantarflexion immediately after stimulation of the antagonist, which was consistent with a reduction in the reflex sensitivity. Note that 0° is the anatomic position of the foot (no plantar- or dorsiflexion).
Discussion
The MAS suggests that stimulation of the agonist muscle may be the best method, but because the MAS measures both the spastic hypertonia and the mechanical components of muscle stiffness,26 it is not clear which component has primarily changed. The H/M ratio showed no change, which indicates that the sensitivity of the spinal synapses36 was not affected by any of the interventions. Moreover, the EMG100, which can be regarded as another measure of the excitability of the spinal synapses, also showed no significant change after the interventions. Therefore, our results indicate that the spinal connections in the reflex loop are not influenced by electric stimulation, suggesting that the changes in the MAS due to agonist stimulation are primarily caused by mechanical components of muscle stiffness or the muscle spindles.
The significant change in the reflex-initiating angle indicates that antagonist stimulation is more effective for reducing spasticity. The outcome of the reflex-initiating angle depends mainly on the sensitivity of the sensors, which are controlled by the activity of the γ-motoneurons, and mechanical stiffness of the muscles and tendons. The mechanical stiffness (ie, viscoelasticity) of a muscle may depend on the blood flow in the tissue.37 Because of the muscle contractions, the blood flow will be increased in the stimulated area, agonist, and antagonist, which, in turn, can decrease the muscle stiffness.
The effect of the sequence was statistically controlled. It was found that the sequence did not influence any of the outcomes significantly. Therefore, we concluded that the washout period of 72 hours was adequate. This also indicated that randomization was not needed.
In other studies,3, 5, 6, 8, 9, 10, 11, 12 it has been found that patients with spasticity may benefit from electric stimulation. However, only 1 of these studies was controlled by a placebo group. This may be an important reason for the discrepancy in results between these studies and our study. If we had performed paired t tests for the pre- and postintervention measurement outcomes only, more significant changes would have been observed. For example, both the agonist and the antagonist stimulation would result in significant changes in the MAS. In addition, 2 studies3, 6 allowed movements of the limb during stimulation, in contrast to the isometric condition in our study. The movement of the stimulated limbs in itself may have caused the effect found in those studies. Limb movement (ie, muscle stretch) is a commonly applied and effective method of treatment for spasticity.1 In contrast to the inclusion criteria in our study, all the previous studies included patients with spasticity and more or less intact supraspinal control. This implies that the patients could feel the stimulation and, therefore, could not be blinded. This may have resulted in additional (placebo) effects.
Recently, the SPASM group38, 39 published a new definition of spasticity that included a greater range of signs and symptoms than those included in the commonly used Lance definition. The new definition includes the entire range of so-called positive signs and symptoms, such as increased tendon reflex, clonus, spasms, and increased resistance to passive movement. We measured several of these, but not all of the positive signs were included in our measurements.
The reflex sensitivity depends on the sensitivity at the level of sensors (mainly the muscle spindles) and spinal synapses (inhibition and facilitation). The sensitivity of the muscle spindles is mainly controlled by the γ-motoneuron activity,14 and mechanical changes resulting from muscle stretch may alter the response of the muscle to stretch. In addition, mechanical changes in muscles and tendons caused by muscle stretch may also, indirectly, alter the sensitivity of the muscle spindles: in muscles or tendons with higher tension the muscle spindles will be stretched at an earlier stage than in relaxed muscles. The sensitivity of the spinal synapses depends on several inhibitory and facilitating neural pathways (eg, presynaptic inhibition).20
According to the results of our study, the benefit of electric stimulation to reduce spasticity is limited, but in clinical practice the effect may be enhanced when movement is allowed during stimulation. The stimulation might also have more effect if series of stimulations are applied over a period of several weeks.9 Additionally, the inhibitory effect of stimulation could also be effective during activities, providing an instant reduction in the reflex excitability. In patients with spasticity and intact supraspinal control, electric stimulation may have an inhibitory effect because of changes in the corticomotoneural excitability.12
Conclusions
According to the MAS outcomes, triceps surae muscle stimulation results in a significant reduction in spasticity of that specific muscle. The reflex-initiating angle changed significantly after stimulation of the tibial anterior muscle.31
Suppliers
Acknowledgments
We thank Victorien Erren for performing the measurements in each session and Jaap Harlaar from the Vrije Universiteit in Amsterdam for allowing us to use the DYNO set-up.
References
- . Management of spasticity in stroke . Br Med Bull . 2000;56:476–485
- . Pain and spasticity after spinal cord injury (mechanisms and treatment) . Spine . 2001;26(24 Suppl):S146–S160
- . Effects of electrical stimulation on spinal spasticity . Scand J Rehabil Med . 1984;16:29–34
- Therapeutic neural effects of electrical stimulation . IEEE Trans Rehabil Eng . 1996;4:218–230
- . Electrical stimulation in treating spasticity resulting from spinal cord injury . Arch Phys Med Rehabil . 1985;66:515–517
- . Treatment of spinal spasticity by electrical stimulation . J Biomed Eng . 1988;10:266–270
- . Electrical treatment of spasticity. Reflex tonic activity in hemiplegic patients and selected specific electrostimulation . Scand J Rehabil Med . 1982;14:177–182
- . Spasticity in spinal cord injured patients: 1. Short-term effects of surface electrical stimulation . Arch Phys Med Rehabil . 1988;69:598–604
- . Effects of surface electrical stimulation on the muscle-tendon junction of spastic gastrocnemius in stroke patients . Disabil Rehabil . 2005;27:105–110
- . The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects . IEEE Trans Neural Syst Rehabil Eng . 2002;10:280–289
- . Mesh-glove. 2. Modulation of residual upper limb motor control after stroke with whole-hand electric stimulation . Scand J Rehabil Med . 1994;26:187–190
- Long-lasting modulation of human motor cortex following prolonged transcutaneous electrical nerve stimulation (TENS) of forearm muscles (evidence of reciprocal inhibition and facilitation) . Exp Brain Res . 2005;161:457–464
- . Spasticity in spinal cord injured patients: 2. Initial measures and long-term effects of surface electrical stimulation . Arch Phys Med Rehabil . 1988;69:862–868
- . Control of human voluntary movement . 2nd ed.. London: Chapman & Hall; 1994;
- . Reciprocal inhibition in hemiplegia (correlation with clinical features and recovery) . Can J Neurol Sci . 1996;23:15–23
- . Reciprocal Ia inhibition in patients with asymmetric spinal spasticity . Clin Neurophysiol . 2002;113:292–297
- . Impaired “natural reciprocal inhibition” in patients with spasticity due to incomplete spinal cord injury . Electroencephalogr Clin Neurophysiol . 1996;101:84–92
- . Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity . Brain . 2001;124(Pt 4):826–837
- . H-reflex modulations during voluntary and automatic movements following upper motor neuron damage . Electroencephalogr Clin Neurophysiol . 1998;109:475–483
- . Essentials of neural science and behavior . New York: McGraw-Hill; 1995;
- . Recurrent inhibition is decreased in patients with amyotrophic lateral sclerosis . Neurology . 1994;44:2148–2153
- . Involvement of spinal recurrent inhibition in spasticity. Further insight into the regulation of Renshaw cell activity . Brain . 1997;120(Pt 6):991–1003
- . Recurrent inhibition in human spinal spasticity . Ital J Neurol Sci . 1989;10:337–347
- . Recurrent inhibition in humans . Prog Neurobiol . 1999;57:325–355
- . Interrater reliability of a modified Ashworth scale of muscle spasticity . Phys Ther . 1987;67:206–207
- . A review of the properties and limitations of the Ashworth and modified Ashworth scales as measures of spasticity . Clin Rehabil . 1999;13:373–383
- . Biomechanical examination of a commonly used measure of spasticity . Clin Biomech . 2001;16:859–865 (Bristol, Avon)
- . SENIAM (European recommendations for surface electromyography) . Enschede: Roessingh Research and Development; 1999;
- . Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury . Exp Brain Res . 2000;133:233–241
- . Reflexen . In: Klinische neurofysiologie . Bussel: Notermans; 1981;p. 353–368
- . Intersession reliability for the H-reflex measurements arising from the soleus, peroneal nerve, and tibialis anterior musculature . Int J Neurosci . 2002;112:841–850
- . Development of a new method for objective assessment of spasticity using full range passive movements . Arch Phys Med Rehabil . 2005;86:1991–1997
- . Mechanical and electromyographic analysis of reciprocal inhibition at the human ankle joint . J Neurophysiol . 1995;74:849–855
- . Measures of muscle and joint performance in the lower limb of children with cerebral palsy . Dev Med Child Neurol . 2003;45:664–670
- . Analyzing medical data using S-Plus . New York: Springer; 2001;
- . Observations on the variability of the H reflex in humans soleus . Muscle Nerve . 1999;22:341–346
- . Effect of static stretching of the biceps brachii on torque, electromyography, and mechanomyography during concentric isokinetic muscle actions . J Strength Cond Res . 2003;17:484–488
- Spasticity (clinical perceptions, neurological realities and meaningful measurement) . Disabil Rehabil . 2005;27:2–6
- . Spasticity (disordered motor control) . In: Feldman RG , Young RR , Koella WP editor. Symposium synopsis . Miami: Symposia Specialists; 1980;p. 485–500
Supported by the Functional Strain, Work Capacity and Mechanisms of Restoration of Mobility in the Rehabilitation of Persons With Spinal Cord Injury, ZONMW-Rehabilitation (grant no. 1435.0010).No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.
PII: S0003-9993(05)01288-8
doi:10.1016/j.apmr.2005.09.024
© 2006 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved.
Volume 87, Issue 2 , Pages 222-228, February 2006
