PTJ
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

PHYS THER
Vol. 88, No. 10, October 2008, pp. 1124-1134
DOI: 10.2522/ptj.20070331
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
ptj.20070331v1
88/10/1124    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when Rapid Responses are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pierce, S. R
Right arrow Articles by Lauer, R. T
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pierce, S. R
Right arrow Articles by Lauer, R. T
Related Collections
Right arrow Injuries and Conditions: Knee
Right arrow Cerebral Palsy
Right arrow Spasticity
Right arrow Cerebral Palsy (Pediatrics)
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

Research Reports

Roles of Reflex Activity and Co-contraction During Assessments of Spasticity of the Knee Flexor and Knee Extensor Muscles in Children With Cerebral Palsy and Different Functional Levels

Samuel R Pierce, Mary F Barbe, Ann E Barr, Patricia A Shewokis and Richard T Lauer

SR Pierce, PT, PhD, NCS, is Research Physical Therapist, Shriners Hospitals for Children, Philadelphia, Pennsylvania, and Assistant Professor, Institute for Physical Therapy Education, Widener University, One University Place, Chester, PA 19013 (USA)
MF Barbe, PhD, is Professor, Physical Therapy Department, College of Health Professions, and Professor, Department of Anatomy and Cell Biology, School of Medicine, Temple University, Philadelphia, Pennsylvania
AE Barr, PT, DPT, PhD, is Chair and Professor, Department of Physical Therapy, Jefferson College of Health Professions, Thomas Jefferson University, Philadelphia, Pennsylvania
PA Shewokis, PhD, is Associate Professor, College of Nursing and Health Professions, Drexel University, Philadelphia, Pennsylvania
RT Lauer, PhD, is Assistant Professor, Physical Therapy Department, College of Health Professions, Temple University, and Research Engineer, Shriners Hospitals for Children, Philadelphia, Pennsylvania

Address all correspondence to Dr Pierce at: srpierce{at}mail.widener.edu


Submitted November 6, 2007; Accepted June 9, 2008


   Abstract
 
Background and Purpose: Spasticity is a common impairment in children with cerebral palsy (CP). The purpose of this study was to examine differences in passive resistive torque, reflex activity, coactivation, and reciprocal facilitation during assessments of the spasticity of knee flexor and knee extensor muscles in children with CP and different levels of functional ability.

Subjects: Study participants were 20 children with CP and 10 children with typical development (TD). The 20 children with CP were equally divided into 2 groups: 10 children classified in Gross Motor Function Classification Scale (GMFCS) level I and 10 children classified in GMFCS level III.

Methods: One set of 10 passive movements between 25 and 90 degrees of knee flexion and one set of 10 passive movements between 90 and 25 degrees of knee flexion were completed with an isokinetic dynamometer at 15°/s, 90°/s, and 180°/s and concurrent surface electromyography of the vastus lateralis and medial hamstring muscles.

Results: Children in the GMFCS level III group demonstrated significantly more peak knee flexor torque with passive movements at 180°/s than children with TD. Children in the GMFCS level I and level III groups demonstrated significantly more repetitions with medial hamstring muscle activity, vastus lateralis muscle activity, and co-contraction than children with TD during the assessment of knee flexor spasticity at a velocity of 180°/s.

Discussion and Conclusion: Children with CP and more impaired functional mobility may demonstrate more knee flexor spasticity and reflex activity, as measured by isokinetic dynamometry, than children with TD. However, the finding of increased reflex activity with no increase in torque in the GMFCS I group in a comparison with the TD group suggests that reflex activity may play a less prominent role in spasticity.


   Introduction
Top
 Abstract
 Introduction
Method
 Results
 Discussion
 Conclusion
 References
 
Cerebral palsy (CP) is a heterogeneous collection of nonprogressive motor disorders of the developing brain that may occur antenatally or postnatally up to the age of 2 years.1 The most common type of CP, in terms of motor control, is spastic CP, which affects approximately 70% to 80% of the population of children with CP.2 Although alternative definitions for spasticity have been proposed,3 spasticity has been most commonly defined as a "velocity dependent increase in tonic stretch reflexes (muscle tone) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex."4 The most common methods for measuring spasticity in clinical settings use passive movements of a limb to assess the resistance of a muscle to stretching, but there are laboratory-based assessments of spasticity during active movements.5 Although the importance of spasticity in relation to other impairments, such as impairments in strength (force-generating capacity), has been debated,6 spasticity, as measured during passive movements, often is negatively correlated with function in children with CP.7,8 Therefore, the treatment of spasticity is often a primary goal for therapeutic interventions, such as dorsal rhizotomy, botulinum toxin, and oral medications.9–11 However, evaluation of the effectiveness of these interventions has been limited by difficulty in measuring spasticity reliably.12–14

As a result, quantitative tests, such as isokinetic dynamometry, have been developed as alternative methods for assessing spasticity. Spasticity may be measured by using a dynamometer to passively move a limb through a defined range of motion while the peak resistive torque15 is calculated. The reliability of isokinetic dynamometry for the measurement of spasticity has been supported in children with CP15,16 and adults with spinal cord injury.17 Isokinetic dynamometry also has been used to measure the effects of selective dorsal rhizotomy18,19 and intrathecal baclofen20 in children with CP.

The difficulties encountered in spasticity measurement and management may be attributable to the multifactorial nature of spasticity. Traditionally, physical therapists have viewed spasticity as being primarily reflexive.21 Therefore, spasticity has been quantified by measuring the strength or latency of a reflex response to passive movement22 or electrical stimulation by use of H-reflex testing.23 However, researchers often found no increase in reflexes during the assessment of spasticity and theorized that the passive stiffness of a muscle caused the velocity-dependent resistance characterizing spasticity.24 A major advantage of using isokinetic dynamometry to assess spasticity is that both reflex and nonreflex components of spasticity can be quantified through concurrent electromyography (EMG) data acquisition.25,26 The identification of reflexive muscle contractions during passive movements by use of isokinetic dynamometry and EMG has been reported, but analysis of the EMG data has been limited.6,27

Additional factors that may influence spasticity in children with CP have not been well investigated; these include muscle co-contraction and reciprocal facilitation. Muscle co-contraction is defined as the simultaneous activation of antagonist and agonist muscle groups of the same joint and in the same plane of movement.27 Muscle co-contraction has been well investigated during gait27–29 and active movements27,30,31 in children with CP but has only recently been reported for assessments of spasticity during passive movements by use of isokinetic dynamometry.32 A related phenomenon that may affect spasticity in children with CP is reciprocal facilitation, which is the activation of the motor pool of the muscle group antagonistic to a muscle group being stretched or stimulated.33,34 Reciprocal facilitation has been reported in children with CP,34 adults with spinal cord injury,35 and adults with hemiplegia36 during a variety of methodologies, including tendon taps, H-reflex testing, and passive movements completed with motors similar to a dynamometer. However, reciprocal facilitation often could not be distinguished from co-contraction in those studies because tendon taps35 and H-reflex testing36 caused contractions in the agonist muscle or because the investigators did not operationally define co-contraction and reciprocal facilitation.34

Spasticity in children with CP also may vary according to the functional status of children with CP. One method used for the classification of functional status in children with CP is the Gross Motor Function Classification System (GMFCS), which classifies function from level I (least severely involved) to level V (most severely involved).37 The reliability,37–39 validity,40 and stability41 of the GMFCS have been supported in the literature. Ostensjo and colleagues42 reported that children classified in GMFCS levels I and II had significantly less spasticity, as measured with the Modified Ashworth Scale (MAS), than children classified in GMFCS levels III and IV. Damiano and colleagues7 also found a significant negative correlation (Spearman rho= –.68) between Ashworth Scale scores for the knee extensor muscles and the total score on the Gross Motor Function Measure,43 another tool that is used to measure function in children with CP and that is highly correlated with GMFCS levels.40,44 However, changes in passive torque and reflex activity during the assessment of spasticity in children with CP and different GMFCS classifications have not been reported.

The purpose of this study was to examine differences in the amount of peak passive resistive torque, reflex activity, coactivation, and reciprocal facilitation during assessments of the spasticity of knee flexor and knee extensor muscles in children with CP and various levels of functional involvement and children with typical development (TD) by use of isokinetic dynamometry and surface EMG. A preliminary report of the data included the frequency of reflex activity and co-contraction in this sample of children with CP without an analysis of the role of functional status.32 We hypothesized that children with CP would demonstrate significantly more peak passive resistive torque, reflex activity, coactivation, and reciprocal facilitation than children with TD. Also, we hypothesized that children with CP and classified in GMFCS level III would demonstrate more peak passive resistive torque, reflex activity, coactivation, and reciprocal facilitation than children with CP and classified in GMFCS level I.


   Method
Top
 Abstract
 Introduction
 Method
Results
 Discussion
 Conclusion
 References
 
Subjects

Written informed consent from each subject's parents and verbal assent from each subject were obtained before participation. A sample of convenience of 20 children with CP (age, in years: X=10.4, SD=1.7, range=8.0–13.0) was recruited from the population of children receiving care at Shriners Hospitals for Children in Philadelphia. Subjects met the following inclusion criteria: diagnosis of spastic CP; GMFCS level I or level III; ages between 7 and 13 years; no documentation in the medical record of hip subluxation, hip dislocation, or significant scoliosis (curvature of >40°); no seizures or controlled seizures; ability to follow one-step commands and ability to attend to tasks associated with data collection; 1 year or more after surgery to the lower extremities; 6 months or more after botulinum toxin injection; and passive range of motion in lower-extremity joints of 10 degrees or less of knee flexion contracture. The range of motion in other muscle groups of the lower extremity was not assessed. Table 1 shows the demographic characteristics of the study participants with CP. Ten children with TD (age, in years: X=10.0, SD=1.6, range=7.6–12.5) and with no known history of orthopedic or neurological disease were recruited from the siblings of children receiving care in the hospital and the community at large.


View this table:
[in this window]
[in a new window]

  		Table 1. Characteristics of Study Participants With Cerebral Palsy (CP)

 
Protocol

One limb was randomly selected for testing in children with TD, diplegic CP, or quadriplegic CP. For children with hemiplegic CP, the more affected limb was tested. Two surface EMG electrodes were placed on the child's leg. One electrode was placed on the vastus lateralis (VL) muscle at a point one half the distance from the greater trochanter to the superior-lateral pole of the patella, and one electrode was placed on the medial hamstring (MH) muscle at a point one half the distance from the ischial tuberosity to the medial condyle. These muscles were selected because their activities are easily recorded with surface EMG and because reflex responses of these muscle groups in a similar protocol were reported previously.7 Muscles were palpated to confirm proper electrode placement. The skin was cleaned with alcohol prior to placement of the electrodes. Signal conditioning electrodes* with a parallel-bar arrangement (contact area=1x10 mm, interelectrode distance=10 mm) were used to detect the electrical activities of the muscles. These electrodes have a built-in gain of 1,000 V/V, a common-mode rejection ratio of greater than 80 dB at 60 Hz, a noise level of 1.5 µV root-mean-square, and a band-pass filter of 20 to 450 Hz. Additional filtering and amplification of the EMG signals were achieved with a Bagnoli 4-channel EMG system,* which has a band-pass filter of 20 to 450 Hz and a gain set at 1,000. The EMG signals were sampled at a rate of 1.2 kHz. Coflex wrap{dagger} was used to secure the electrodes to the thigh in an attempt to reduce the motion of the electrodes on the skin during testing.

Subjects were seated on the isokinetic dynamometer{ddagger} in a position of 80 degrees of hip flexion and 90 degrees of knee flexion and with the ankle unrestricted. The trunk and leg were stabilized with straps across the chest, waist, and upper thigh. The axis of the dynamometer was visually aligned with the axis of the knee joint, which was defined as a line between the medial and lateral condyles of the femur. Distal attachment of the lower limb to the lever of the dynamometer was made approximately 3 cm above the lateral malleolus. One submaximal voluntary contraction of the knee flexor and knee extensor muscles was completed to verify electrode placement by visual analysis of the resultant EMG response.

The subjects were instructed to relax as much as possible and to not move the limb or trunk on the dynamometer so that baseline EMG data could be collected for at least 5 seconds. The EMG signals were displayed on a computer monitor for visual assessment. One set of 3 continuous passive movements at a velocity of 5°/s from 90 degrees of knee flexion to 25 degrees of knee flexion and back to 90 degrees of knee flexion was collected for gravity correction calculation of the weight of the limb during data processing.16 The subjects were instructed to relax as much as possible and to not assist the passive movement of the limb. The EMG output from the amplifier and the force, velocity, and position data were collected with a personal computer and custom software written in Labview 5.1§ for data analysis. The EMG signals were displayed on a computer monitor for visual assessment. If the subject performed a volitional movement into knee extension or knee flexion, detectable by visual assessment of the EMG signals, an additional set of movements was collected for gravity correction. Any subject who was unable to adhere to the protocol was excluded from the analysis. Any subject who exhibited reflexive contraction of either the VL or the MH muscle during the collection of data for gravity correction also was excluded from the analysis.

One set of 10 continuous passive movements from 90 degrees of knee flexion to 25 degrees of knee flexion was completed at 15°/s, 90°/s, and 180°/s with a return speed of 5 degrees per second to assess knee flexor spasticity. One set of 10 continuous passive movements from 25 degrees of knee flexion to 90 degrees of knee flexion was completed at 15°/s, 90°/s, and 180°/s with a return speed of 5 degrees per second to assess knee extensor spasticity. The order of muscles tested and the velocity of movement were randomized. The acceleration during movement reversals was set at high, which is equivalent to approximately 9,000°/s.2 A 60-second rest break occurred after each movement velocity assessment. The total time for data collection for this investigation was approximately 30 minutes.

Data Processing

A custom-written Matlab|| program was used for postprocessing and analysis of the torque and EMG data. The gravity-corrected knee flexor and knee extensor peak resistive torque values were calculated for each repetition while the knee was extended between 85 and 30 degrees to measure knee flexor spasticity and while the knee was flexed between 30 and 85 degrees to measure knee extensor spasticity. The peak resistive torque was not calculated until the limb was moving at a constant velocity. The mean passive resistive torque for all movement repetitions at a given speed was quantified and identified as passive torque. The maximum passive resistive torque of the 10 movement repetitions at each movement velocity was identified as peak torque. The EMG data were full-wave rectified and processed by use of a second-order Butterworth 10-Hz low-pass filter with phase correction to create a linear envelope. The EMG onset and offset then were defined as muscle activity that was 3 SDs above the baseline and that occurred for a minimum of 50 milliseconds (Figure).45 The number of movement repetitions and the percentage of each movement repetition with EMG activity classified as reflexive, coactivation, or reciprocal facilitation were quantified. Reflex activity was defined as the presence of EMG activity of either the MH or the VL muscle during passive movement. Co-contraction was defined as simultaneous EMG activity of both the MH and the VL muscles during passive movement. Reciprocal facilitation was defined as the presence of EMG activity of the VL muscle with no activity of the MH muscle during passive movements of knee extension or EMG activity of the MH muscle with no activity of the VL muscle during passive movements of knee flexion.


Figure 1
View larger version (29K):
[in this window]
[in a new window]

  		Figure. (A) Examples of raw electromyography (EMG) recordings of the vastus lateralis muscle (in millivolts) during passive movements at 180°/s from 25 degrees of knee flexion to 90 degrees of knee flexion in children with typical development (TD), children with Gross Motor Function Classification System (GMFCS) level I cerebral palsy (CP), and children with GMFCS level III CP. (B) Examples of raw EMG recordings of the medial hamstring muscle (in millivolts) during passive movements at 180°/s from 90 degrees of knee flexion to 25 degrees of knee flexion in children with TD, children with GMFCS level I CP, and children with GMFCS level III CP.

 
Data Analysis

Data were analyzed by use of MedCalc version 2.07# and SPSS version 14.0.** Data were tested for normality and homogeneity of variance by use of the Shapiro-Wilks test, the Levene test, and histograms across groups, muscles, and velocity of movement. Passive torque and peak torque were nonnormally distributed, and a nonparametric test—the Kruskal-Wallis one-way analysis of variance (ANOVA)—was used for each movement velocity and muscle group. The Tukey rank-of-sums multiple comparisons test was used to determine significant differences. With each muscle group as a family of tests, an inflated type I error rate was controlled for with Bonferroni corrections for each muscle group, resulting in an alpha level of .025 (.05/2).

The mean percentage of each movement repetition and the number of movement repetitions that exhibited reflex activity, coactivation, and reciprocal facilitation for each movement velocity and for each muscle group were nonnormally distributed and thus were analyzed with a Kruskal-Wallis one-way ANOVA. The Tukey rank-of-sums multiple comparisons test was used for post hoc testing. To control for an inflated type I error rate, we used Bonferroni corrections for the number of statistical tests for each muscle group, so that the alpha level was .025 (.05/2).


   Results
Top
 Abstract
 Introduction
 Method
 Results
Discussion
 Conclusion
 References
 
Torque Differences

Table 2 shows the median values and interquartile ranges for passive torque and peak torque across groups and across movement velocities for the knee flexor and knee extensor muscles. A Kruskal-Wallis one-way ANOVA revealed significant differences (P=.017) between subject groups in the peak torque of the knee flexor muscles during passive movements at 180°/s. Post hoc testing revealed that children in the GMFCS level III group demonstrated significantly more peak torque of the knee flexor muscles than children in the TD group. There were no significant differences in the passive torque of the knee flexor muscles, the peak torque of the knee extensor muscles, or the peak torque of the knee extensor muscles for the GMFCS level I, GMFCS level III, and TD groups. The interquartile ranges for the peak torque and passive torque of the knee flexor and knee extensor muscles for children in the GMFCS level III group appeared to be much higher than those for children in the TD or GMFCS level I group for assessments at 180°/s.


View this table:
[in this window]
[in a new window]

  		Table 2. Median Knee Extensor and Knee Flexor Muscle Peak Torque and Passive Torque Across Movement Velocitiesa

 
EMG Differences

Tables 3 and 4 show the median EMG responses of the knee flexor muscles and knee extensor muscles, respectively, obtained during passive movements at 15°/s, 90°/s, and 180°/s. A Kruskal-Wallis one-way ANOVA revealed no significant differences (P>.025) between subject groups in the number of repetitions exhibiting EMG activity and the percentage of EMG activity during assessments of the knee extensor muscles at 15°/s, 90°/s, and 180°/s and during assessments of the knee flexor muscles at 15°/s and 90°/s. Significant differences between subject groups were found in the number of repetitions exhibiting MH muscle activity, VL muscle activity, and co-contraction during assessments of the knee flexor muscles at 180°/s (P<.025). Post hoc testing revealed that children in the GMFCS level I and GMFCS level III groups demonstrated significantly more repetitions exhibiting MH muscle activity, VL muscle activity, and co-contraction than those in the TD group.


View this table:
[in this window]
[in a new window]

  		Table 3. Median Electromyography Responses During Assessments of Knee Flexor Muscles at Various Velocities

 

View this table:
[in this window]
[in a new window]

  		Table 4. Median Electromyography Responses During Assessments of Knee Extensor Muscles at Various Velocities

 

   Discussion
Top
 Abstract
 Introduction
 Method
 Results
 Discussion
Conclusion
 References
 
This investigation examined differences in the amount of passive resistive torque, reflex activity, coactivation, and reciprocal facilitation during assessments of the spasticity of knee flexor and knee extensor muscles in children with CP. Children in the GMFCS level III group demonstrated significantly more peak knee flexor torque with passive movements at 180°/s than children in the TD group. Children in the GMFCS level I and GMFCS level III groups demonstrated significantly more repetitions with MH muscle activity, VL muscle activity, and co-contraction than children in the TD group during assessments of knee flexor spasticity at a velocity of 180°/s. However, there were no differences in these variables between the groups of children with CP. Our results should be considered with caution because of the small sample size used in this investigation.

The finding of no significant increase in peak knee flexor torque in the GMFCS level I group in comparison with the GMFCS level III group was surprising, because Ostensjo and colleagues42 reported that children classified in GMFCS levels I and II had significantly less spasticity, as measured with the MAS, than children classified in GMFCS levels III and IV. One possible explanation for our results is that isokinetic dynamometry may be a more sensitive method of measuring spasticity than the MAS. The validity and reliability of the MAS as a method of assessing spasticity have been questioned in several investigations,12–14 although the reliability of isokinetic dynamometry for measuring spasticity has been supported.15,16 In addition, Damiano and colleagues7 reported that isokinetic measurements of the spasticity of the knee flexor and extensor muscles tended to show a stronger association with function than the Ashworth Scale; this finding suggests that isokinetic dynamometry may be a more sensitive tool for measuring spasticity than this clinical scale. Also, the lack of a significant difference between the TD group and the GMFCS level I group in knee flexor torque was unexpected, because Engsberg and colleagues46 and Ross and Engsberg47 reported significant differences in knee flexor spasticity, as measured by isokinetic dynamometry, between children with CP and children with TD. The effect of the increase in the variability of passive torque and peak torque of the knee flexor muscles in the GMFCS level III group is uncertain. This finding may be interpreted to suggest that children classified in a given GMFCS level may show wide variations in the amount of spasticity of the knee flexor muscles, so that spasticity may be an important impairment in some children but not in others. Additional research investigating the validity and sensitivity of isokinetic measurements of spasticity is required to determine the usefulness of this method in comparison with more commonly used clinical scales for measuring spasticity.

The differences in peak knee flexor torque in this investigation may have been attributable to increased passive stiffness of the knee flexor muscles, because there were no differences in muscle reflex activity between children in the GMFCS level I and GMFCS level III groups, but there were differences in peak knee flexor torque between children in the GMFCS level III and TD groups. The findings of no significant differences in passive torque but significant differences in reflex activity in a comparison of the GMFCS level I and TD groups further suggest that reflex activity may be less important than passive torque in spasticity. Berger et al29 first hypothesized that muscle stiffness played a prominent role in spasticity in children with CP. Mechanical changes in spastic muscle may be the cause of increased muscle stiffness.5 Friden and Lieber48 reported that spastic muscle cells are shorter and stiffer than muscle cells with normal fibers and suggested that changes in intracellular or extracellular structures may have caused these changes. Lieber and colleagues49 later found that spastic muscle bundles consisted of only 40% muscle fibers; in comparison, normal bundles consisted of 95% muscle fibers. The remaining 60% of the muscle bundles consisted of a poorly organized extracellular matrix; this matrix may have been primarily collagen, because previous studies reported increased levels of collagen in the muscles of children with CP.50

However, the finding of no differences in muscle reflex activity and torque during assessments of knee flexor muscles in children in the GMFCS level I and GMFCS level III groups may be related to the specific isokinetic protocol used in this investigation. The completion of 6 sets of 10 passive movements into flexion and extension may have affected the results, because Nuyens and colleagues51 found that repeated passive motions may diminish reflex activity and torque during assessments of spasticity. Because there were no differences in peak torque, passive torque, or EMG activity with movements at 15°/s and 90°/s in either muscle group, perhaps future investigations should eliminate testing at one or both of these velocities to minimize this stretching effect. In addition, the development of isokinetic protocols that require less time for data collection may make isokinetic dynamometry more feasible for use in the clinical environment, because isokinetic dynamometry may be viewed by clinicians as being too time-consuming. Finally, the possible effects of contractures and spasticity of the ankle plantar flexor muscles on knee flexor torque and EMG are unknown because these muscles were not assessed in the present study. However, because the ankle was unrestricted during passive movements in the present study, we hypothesize that this muscle group had little effect on our results, as it was never placed in a stretched position.

The finding of no significant differences in torque and reflex activity during testing of the knee extensor muscles may also have been related to a stretching effect, because investigators have reported decreases in passive torque with repeated movements.51 In addition, the positioning of subjects during testing of the knee extensor muscles in the present study may have affected the results. Children were assessed with their hips in a flexed position for testing of both muscle groups to minimize the time required for data collection and to maximize the likelihood of adherence to the data collection protocol. However, with testing in this position, the knee extensor muscles were not placed in a maximally stretched position; this positioning may have affected the amount of reflex activity and torque elicited. Furthermore, the influence of possible contracture of the rectus femoris muscle, which crosses both the hip and the knee joints and which was in a partially slack position, on the knee extensor torque results in the present study is unknown, because hip flexion contractures were not screened for in this investigation. Future investigations in which isokinetic dynamometry is used to measure spasticity may benefit from assessments of knee extensor spasticity with subjects’ muscles in a stretched position to increase the likelihood of evoking a stretch response.

Children with CP and classified in GMFCS level I or GMFCS level III demonstrated significantly more repetitions with MH muscle activity, VL muscle activity, and co-contraction than children with TD during assessments of the knee flexor muscles with passive movements into knee extension at 180°/s. The significant increase in the number of repetitions with co-contraction and VL muscle activity during testing at 180°/s suggests that co-contraction may play a role in spasticity. Our preliminary report of these data indicated that co-contraction is strongly associated with reflex activity in children with CP.32 Future research should investigate the specific relationship between co-contraction and torque because co-contraction may increase the stiffness associated with a joint.52 Researchers have hypothesized that co-contraction during volitional movement may be attributable to several factors, including abnormal supraspinal input from the motor cortex and decreased Ia reciprocal inhibition in the antagonistic muscle.53 The mechanisms causing co-contraction during passive movements are unknown, and additional investigation is needed. The finding of no difference in either muscle group at speeds of 15°/s and 90°/s suggests that these velocities may not be high enough to elicit spastic muscle responses. The importance of movement velocity during isokinetic testing also was reported by Rabita et al,54 who found that the velocity and acceleration generated during isokinetic testing of the plantar-flexor muscles were insufficient to generate reflex activity of the plantar-flexor muscles in people with stroke.

Our data also suggest that reciprocal facilitation does not appear to play a role in spasticity because there were no differences in reciprocal facilitation in any muscle group tested at any speed. Although other investigators have reported the presence of reciprocal facilitation in children with CP,34 adults with spinal cord injury,35 and adults with hemiplegia,36 differences in the operational definitions and methods used in these studies may explain the conflicting results. The methods used in previously published investigations were unable to distinguish agonist and antagonist muscle activities, either because tendon taps35 and H-reflex testing36 caused contractions in the agonist muscle or because the investigators did not operationally define co-contraction and reciprocal facilitation.34 In the present study, we operationally defined reciprocal facilitation and co-contraction as distinct phenomena that could be isolated through the use of isokinetic dynamometry to measure spasticity. The significant differences that we found in co-contraction between subjects with CP and subjects with TD with movements at 180°/s may have been reported as reciprocal facilitation in those earlier studies because of the differences in the methods used.

Clinical Implications

The clinical implications of our findings, which suggest that passive stiffness plays a larger role in spasticity than increased reflex activity, may affect clinical decision making with regard to the treatment of children with CP. We speculate that interventions that attempt to decrease muscle reflexes, such as oral medications or botulinum toxin, may not be focusing on the most relevant impairment affecting spasticity; thus, their effectiveness may be limited in some children with CP. Interventions that attempt to address passive stiffness in children with CP, such as stretching or serial casting, may be more likely to cause a meaningful change in spasticity if the spasticity is attributable to nonreflexive components; however, additional research is needed to determine their effectiveness.55 The large amount of variability in reflexes seen in the GMFCS III group indicates that individual children with CP may exhibit spasticity that is primarily reflexive in nature; this finding suggests that their treatment should be very different from that for children who exhibit primarily increased passive stiffness. It is clear there is a need for additional research that attempts to determine the most effective interventions for spasticity in subsets of children with CP and with different degrees of reflex activity and passive stiffness.

One difficulty in determining the clinical implications of our investigation is our use of assessments of passive movements rather than active movements to measure spasticity.5,56 Although our use of passive movements with an isokinetic dynamometer fits the Lance definition of spasticity,4 there is a lack of consensus in the research literature and clinical practice regarding the definition of spasticity. For example, a new definition of spasticity was recently proposed by the Support Program for Assembly of a Database for Spasticity Management project, which defines spasticity as "disordered sensory-motor control, resulting from an upper motor neuron lesion, presenting as intermittent or sustained involuntary activation of muscles."56(p72) It is clear that this definition of spasticity does not indicate whether spasticity should be assessed by passive or active movements and will allow researchers and clinicians to explore alternative methods for measuring spasticity.

There are several advantages and disadvantages of using passive versus active movements to measure spasticity. The most common passive methods used to measure spasticity are clinical scales, such as the Ashworth Scale and the MAS, because these scales require no equipment and are easy to use; however, their reliability has not been well established.57 A passive method such as isokinetic dynamometry has the advantage of being able to measure resistance reliably16 and EMG concurrently to determine reflex responses.25,26 However, the expense, time, and technology required to collect such data have severely limited the application of this method in clinical practice. Active movements during functional or nonfunctional activities may be able to determine the role of reflexes in active movements5 but are not available for clinical use because of the technology and time required for data collection.56 Additional research is needed to develop the optimal tool for spasticity measurement—one that would be clinically applicable and able to distinguish reflexive and nonreflexive aspects of spasticity during active and passive motions.56


   Conclusion
Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 Conclusion
References
 
Children with CP and more impaired functional mobility may have more knee flexor spasticity and reflex activity, as measured by isokinetic dynamometry, than children with TD. However, the finding of increased reflex activity with no increase in torque in a comparison of the GMFCS level I group and the TD group suggests that reflex activity may play a less prominent role in spasticity.


   Footnotes
 
All authors provided concept/idea/research design, writing, and consultation (including review of manuscript before submission). Dr Pierce and Dr Lauer provided data collection and facilities/equipment. Dr Shewokis provided data analysis. Dr Pierce provided project management and subjects.

The Temple University institutional review board approved this investigation.

This work was completed in partial fulfillment of the requirements for Dr Pierce's doctoral degree at Temple University.

A preliminary report of the data has been published elsewhere: Pierce SR, Barbe MF, Barr AE, et al. Co-contraction during passive movements of the knee joint in children with cerebral palsy. Clin Biomech. 2007;22:1045–1048.

The data from children with TD will be published in conjunction with a different study: Pierce SR, Johnston TE, Lauer RT, Shewokis PA. Examination of spasticity of the knee flexors and knee extensors using isokinetic dynamometry and clinical scales in children with spinal cord injury. J Spinal Cord Med. 2008;31:208–214.

The study was funded by Shriners Hospitals for Children (grant 8520). The funding source for this investigation had no role in the design, conduct, or reporting of results for this article.

* Delsys Inc, PO Box 15734, 650 Beacon St, 6th Floor, Boston, MA 02215. Back

{dagger} Andover Healthcare Inc, 9 Fanaras Dr, Salisbury, MA 01952. Back

{ddagger} Chattex Corp, PO Box 4287, 101 Memorial Dr, Chattanooga, TN 37405. Back

§ National Instruments Corp, 11500 N Mopac Expressway, Austin, TX 78759. Back

|| The MathWorks Inc, 3 Apple Hill Dr, Natick, MA 01760. Back

# MedCalc Software, Broekstraat 52, 9030 Mariakerke, Belgium. Back

** SPSS Inc, 233 S Wacker Dr, Chicago, IL 60606 Back


   References
Top
 Abstract
 Introduction
 Method
 Results
 Discussion
 Conclusion
 References
 

  1. Lin JP. The cerebral palsies: a physiological approach. J Neurol Neurosurg Psychiatry. 2003;74(suppl 1):i23–i29.[Free Full Text]
  2. Taft LT. Cerebral palsy. Pediatr Rev. 1995;16:411–418.[Abstract/Free Full Text]
  3. Pandyan AD, Gregoric M, Barnes MP, et al. Spasticity: clinical perceptions, neurological realities and meaningful measurement. Disabil Rehabil. 2005;27:2–6.[CrossRef][Web of Science][Medline]
  4. Lance JW. The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture. Neurology. 1980;30:1303–1313.[Free Full Text]
  5. Dietz V, Sinkjaer T. Spastic movement disorder: impaired reflex function and altered muscle mechanics. Lancet Neurol. 2007;6:725–733.[CrossRef][Web of Science][Medline]
  6. Damiano DL, Quinlivan J, Owen BF, et al. Spasticity versus strength in cerebral palsy: relationships among involuntary resistance, voluntary torque, and motor function. Eur J Neurol. 2001;8(suppl 5):40–49.[CrossRef][Web of Science][Medline]
  7. Damiano DL, Quinlivan JM, Owen BF, et al. What does the Ashworth scale really measure and are instrumented measures more valid and precise? Dev Med Child Neurol. 2002;44:112–118.[CrossRef][Web of Science][Medline]
  8. Goh HT, Thompson M, Huang WB, Schafer S. Relationships among measures of knee musculoskeletal impairments, gross motor function, and walking efficiency in children with cerebral palsy. Pediatr Phys Ther. 2006;18:253–261.[CrossRef][Medline]
  9. Boyd RN, Hays RM. Current evidence for the use of botulinum toxin type A in the management of children with cerebral palsy: a systematic review. Eur J Neurol. 2001;8(suppl 5):1–20.[Web of Science][Medline]
  10. Green LB, Hurvitz EA. Cerebral palsy. Phys Med Rehabil Clin N Am. 2007;18:859–882, vii.[Medline]
  11. McLaughlin J, Bjornson K, Temkin N, et al. Selective dorsal rhizotomy: meta-analysis of three randomized controlled trials. Dev Med Child Neurol. 2002;44:17–25.[CrossRef][Web of Science][Medline]
  12. Blackburn M, van Vliet P, Mockett SP. Reliability of measurements obtained with the modified Ashworth scale in the lower extremities of people with stroke. Phys Ther. 2002;82:25–34.[Abstract/Free Full Text]
  13. Fosang AL, Galea MP, McCoy AT, et al. Measures of muscle and joint performance in the lower limb of children with cerebral palsy. Dev Med Child Neurol. 2003;45:664–670.[CrossRef][Web of Science][Medline]
  14. Pandyan AD, Johnson GR, Price CI, et al. A review of the properties and limitations of the Ashworth and modified Ashworth scales as measures of spasticity. Clin Rehabil. 1999;13:373–383.[Abstract/Free Full Text]
  15. Boiteau M, Malouin F, Richards CL. Use of a hand-held dynamometer and a Kin-Com dynamometer for evaluating spastic hypertonia in children: a reliability study. Phys Ther. 1995;75:796–802.[Abstract/Free Full Text]
  16. Pierce SR, Lauer RT, Shewokis PA, et al. Test-retest reliability of isokinetic dynamometry for the assessment of spasticity of the knee flexors and knee extensors in children with cerebral palsy. Arch Phys Med Rehabil. 2006;87:697–702.[CrossRef][Web of Science][Medline]
  17. Lamontagne A, Malouin F, Richards CL, Dumas F. Evaluation of reflex- and nonreflex-induced muscle resistance to stretch in adults with spinal cord injury using hand-held and isokinetic dynamometry. Phys Ther. 1998;78:964–975.[Abstract/Free Full Text]
  18. Engsberg JR, Ross SA, Park TS. Changes in ankle spasticity and strength following selective dorsal rhizotomy and physical therapy for spastic cerebral palsy. J Neurosurg. 1999;91:727–732.[Web of Science][Medline]
  19. Engsberg JR, Ross SA, Wagner JM, Park TS. Changes in hip spasticity and strength following selective dorsal rhizotomy and physical therapy for spastic cerebral palsy. Dev Med Child Neurol. 2002;44:220–226.[CrossRef][Web of Science][Medline]
  20. Schmit BD, Gaebler-Spira D. Mechanical measurements of the effects of intrathecal baclofen dosage adjustments in cerebral palsy: a pilot study. Am J Phys Med Rehabil. 2004;83:33–41.[CrossRef][Web of Science][Medline]
  21. Bobath B. Treatment of adult hemiplegia. Physiotherapy. 1977;63:310–313.[Medline]
  22. Thilmann AF, Fellows SJ, Garms E. The mechanism of spastic muscle hypertonus: variation in reflex gain over the time course of spasticity. Brain. 1991;114:233–244.[Web of Science][Medline]
  23. Misiaszek JE. The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve. 2003;28:144–160.[CrossRef][Web of Science][Medline]
  24. Dietz V, Berger W. Normal and impaired regulation of muscle stiffness in gait: a new hypothesis about muscle hypertonia. Exp Neurol. 1983;79:680–687.[CrossRef][Web of Science][Medline]
  25. Biering-Sørensen F, Nielsen JB, Klinge K. Spasticity-assessment: a review. Spinal Cord. 2006;44:708–722.[CrossRef][Web of Science][Medline]
  26. Wood DE, Burridge JH, van Wijck FM, et al. Biomechanical approaches applied to the lower and upper limb for the measurement of spasticity: a systematic review of the literature. Disabil Rehabil. 2005;27:19–32.[CrossRef][Web of Science][Medline]
  27. Damiano DL, Martellotta TL, Sullivan DJ, et al. Muscle force production and functional performance in spastic cerebral palsy: relationship of co-contraction. Arch Phys Med Rehabil. 2000;81:895–900.[CrossRef][Web of Science][Medline]
  28. Unnithan VB, Dowling JJ, Frost G, et al. Co-contraction and phasic activity during gait in children with cerebral palsy. Electromyogr Clin Neurophysiol. 1996;36:487–494.[Medline]
  29. Berger W, Quintern J, Dietz V. Pathophysiology of gait in children with cerebral palsy. Electroencephalogr Clin Neurophysiol. 1982;53:538–548.[CrossRef][Web of Science][Medline]
  30. Ikeda AJ, Abel MF, Granata KP, Damiano DL. Quantification of co-contraction in spastic cerebral palsy. Electromyogr Clin Neurophysiol. 1998;38:497–504.[Medline]
  31. Lebiedowska MK, Fisk JR. Quantitative evaluation of reflex and voluntary activity in children with spasticity. Arch Phys Med Rehabil. 2003;84:828–837.[CrossRef][Web of Science][Medline]
  32. Pierce SR, Barbe MF, Barr AE, et al. Co-contraction during passive movements of the knee joint in children with cerebral palsy. Clin Biomech. 2007;22:1045–1048.[CrossRef][Medline]
  33. Gottlieb GL, Myklebust BM, Penn RD, Agarwal GC. Reciprocal excitation of muscle antagonists by the primary afferent pathway. Exp Brain Res. 1982;46:454–456.[Web of Science][Medline]
  34. Myklebust BM, Gottlieb GL, Penn RD, Agarwal GC. Reciprocal excitation of antagonistic muscles as a differentiating feature in spasticity. Ann Neurol. 1982;12:367–374.[CrossRef][Web of Science][Medline]
  35. Xia R, Rymer WZ. Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord. 2005;43:14–21.[CrossRef][Web of Science][Medline]
  36. Marque P, Simonetta-Moreau M, Maupas E, Roques CF. Facilitation of transmission in heteronymous group II pathways in spastic hemiplegic patients. J Neurol Neurosurg Psychiatry. 2001;70:36–42.[Abstract/Free Full Text]
  37. Palisano R, Rosenbaum P, Walter S, et al. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39:214–223.[Web of Science][Medline]
  38. Morris C, Galuppi BE, Rosenbaum PL. Reliability of family report for the Gross Motor Function Classification System. Dev Med Child Neurol. 2004;46:455–460.[CrossRef][Web of Science][Medline]
  39. Wood E, Rosenbaum P. The gross motor function classification system for cerebral palsy: a study of reliability and stability over time. Dev Med Child Neurol. 2000;42:292–296.[CrossRef][Web of Science][Medline]
  40. Palisano RJ, Hanna SE, Rosenbaum PL, et al. Validation of a model of gross motor function for children with cerebral palsy. Phys Ther. 2000;80:974–985.[Abstract/Free Full Text]
  41. Palisano RJ, Cameron D, Rosenbaum PL, et al. Stability of the gross motor function classification system. Dev Med Child Neurol. 2006;48:424–428.[CrossRef][Web of Science][Medline]
  42. Ostensjo S, Carlberg EB, Vollestad NK. Motor impairments in young children with cerebral palsy: relationship to gross motor function and everyday activities. Dev Med Child Neurol. 2004;46:580–589.[CrossRef][Web of Science][Medline]
  43. Russell DJ, Avery LM, Rosenbaum PL, et al. Improved scaling of the gross motor function measure for children with cerebral palsy: evidence of reliability and validity. Phys Ther. 2000;80:873–885.[Abstract/Free Full Text]
  44. Oeffinger DJ, Tylkowski CM, Rayens MK, et al. Gross Motor Function Classification System and outcome tools for assessing ambulatory cerebral palsy: a multicenter study. Dev Med Child Neurol. 2004;46:311–319.[Web of Science][Medline]
  45. Hodges PW, Bui BH. A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalogr Clin Neurophysiol. 1996;101:511–519.[CrossRef][Medline]
  46. Engsberg JR, Olree KS, Ross SA, Park TS. Quantitative clinical measure of spasticity in children with cerebral palsy. Arch Phys Med Rehabil. 1996;77:594–599.[CrossRef][Web of Science][Medline]
  47. Ross SA, Engsberg JR. Relation between spasticity and strength in individuals with spastic diplegic cerebral palsy. Dev Med Child Neurol. 2002;44:148–157.[CrossRef][Web of Science][Medline]
  48. Friden J, Lieber RL. Spastic muscle cells are shorter and stiffer than normal cells. Muscle Nerve. 2003;27:157–164.[CrossRef][Web of Science][Medline]
  49. Lieber RL, Runesson E, Einarsson F, Friden J. Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material. Muscle Nerve. 2003;28:464–471.[CrossRef][Web of Science][Medline]
  50. Booth CM, Cortina-Borja MJ, Theologis TN. Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol. 2001;43:314–320.[CrossRef][Web of Science][Medline]
  51. Nuyens GE, De Weerdt WJ, Spaepen AJ Jr, et al. Reduction of spastic hypertonia during repeated passive knee movements in stroke patients. Arch Phys Med Rehabil. 2002;83:930–935.[CrossRef][Web of Science][Medline]
  52. Damiano DL. Reviewing muscle co-contraction: is it a developmental, pathological, or motor control issue? Phys Occup Ther Pediatr. 1993;12:3–20.[CrossRef]
  53. Gracies JM. Pathophysiology of spastic paresis, II: emergence of muscle overactivity. Muscle Nerve. 2005;31:552–571.[CrossRef][Web of Science][Medline]
  54. Rabita G, Dupont L, Thevenon A, et al. Differences in kinematic parameters and plantarflexor reflex responses between manual (Ashworth) and isokinetic mobilisations in spasticity assessment. Clin Neurophysiol. 2005;116:93–100.[CrossRef][Web of Science][Medline]
  55. Wiart L, Darrah J, Kembhavi G. Stretching with children with cerebral palsy: what do we know and where are we going? Pediatr Phys Ther. 2008;20:173–178.[CrossRef][Medline]
  56. Burridge JH, Wood DE, Hermens HJ, et al. Theoretical and methodological considerations in the measurement of spasticity. Disabil Rehabil. 2005;27:69–80.[CrossRef][Web of Science][Medline]
  57. Platz T, Eickhof C, Nuyens G, Vuadens P. Clinical scales for the assessment of spasticity, associated phenomena, and function: a systematic review of the literature. Disabil Rehabil. 2005;27:7–18.[CrossRef][Web of Science][Medline]

Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?



This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
ptj.20070331v1
88/10/1124    most recent
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when Rapid Responses are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pierce, S. R
Right arrow Articles by Lauer, R. T
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pierce, S. R
Right arrow Articles by Lauer, R. T
Related Collections
Right arrow Injuries and Conditions: Knee
Right arrow Cerebral Palsy
Right arrow Spasticity
Right arrow Cerebral Palsy (Pediatrics)
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Copyright © 2008 by the American Physical Therapy Association.