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Research Reports |
EG Fowler, PT, PhD, is Assistant Professor, UCLA Department of Orthopaedic Surgery, University Affiliated Program and the UCLA/Orthopaedic Hospital Center for Cerebral Palsy, 22–70 Rehabilitation Center, Los Angeles, CA 90095-1795 (USA) (efowler{at}mednet.ucla.edu).
TW Ho, PT, MPT, was Staff Physical Therapist, UCLA/Orthopaedic Hospital Center for Cerebral Palsy, at the time the study was performed
AI Nwigwe, BS, is a doctoral student in the Department of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, Calif. She was Research Assistant, UCLA/Orthopaedic Hospital Center for Cerebral Palsy, at the time the study was performed
FJ Dorey, PhD, is Professor, Departments of Orthopaedic Surgery and Biostatistics, University of California, Los Angeles
Address all correspondence to Dr Fowler
Submitted February 29, 2000;
Accepted December 3, 2000
 | Abstract |
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Key Words: Cerebral palsy • Pendulum test • Spasticity • Strengthening exercises
| Introduction |
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 TopAbstract Introduction MethodsResultsDiscussionConclusionReferences |
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Investigators4–9 have demonstrated the benefits of strengthening exercises in individuals with CP. Improvements in muscle performance have been demonstrated for people with CP using isometric exercise,4 isotonic exercise,4–6 isokinetic exercise,7,8 and a combination of isotonic exercise and weight machines.9 These programs were generally done 3 times a week for periods ranging from 6 to 8 weeks. Functional benefits, as a result of improved muscle performance, were reported for isotonic exercise using gait analysis5 and for isokinetic exercise using the Gross Motor Function Measure.8
Although the benefits of strengthening exercises have been demonstrated, the potential negative effects of an associated increase in spasticity have not been critically examined. MacPhail and Kramer8 used a modified version of the Ashworth scale10 to measure the effect of spasticity on resistance to passive knee motion before and after an 8-week exercise program for subjects with mild spastic CP. They reported that the number of subjects exhibiting an Ashworth scale grade of at least 1 (slight increase in muscle tone) in the quadriceps femoris and hamstring muscles decreased after the completion of the exercise program. However, the authors stated that these results should be interpreted with caution. Many of the subjects had Ashworth scale grades of either 0 (normal) or 1. The investigators had difficulty making the differentiation between these 2 grades due to lack of sensitivity of the scale and inability to ascertain whether the subjects were truly relaxed. Healy4 and Hovart9 reported that range of motion increased, rather than decreased, after an 8-week strengthening exercise program, which they believed indicated no increase in spasticity.
The aim of our study was to assess spasticity before and after the performance of right quadriceps femoris muscle strengthening exercises. There exist varying definitions of spasticity in the literature. We defined spasticity as a velocity-dependent hyperexcitability of the muscle stretch reflex, consistent with the definition proposed by Lance11 in 1980. Spasticity is often assessed by applying motion to the joint or tendon and measuring the response.12 Factors such as central reflexes and biomechanical restraint from muscle or connective tissue also can contribute to this response; however, we believe that these factors would not be expected to change following interventions aimed at reducing spasticity. We believe that the most common method of measuring spasticity uses the Ashworth scale,13 in which categories of "mild tone," "moderate tone," "severe tone," and "extreme tone"10 are used to define an individual's level of spasticity. For detecting small changes in spasticity due to therapeutic interventions, alternative methods such as the pendulum test have been shown to be more sensitive.14,15
The pendulum test, first described by Wartenberg,16 involves lifting the relaxed leg against gravity and releasing it, causing it to swing freely. The pendulum test has been reported to yield reliable measurements17 and to be sensitive to variation in spasticity in people with CP.18 Bohannon17 assessed the reliability of measurements obtained with the pendulum test in people without known neurological impairments using an isokinetic dynamometer to quantify knee joint motion. He reported an intraclass correlation coefficient of .96 for 4 successive trials. The pendulum test is most sensitive to spasticity of the quadriceps femoris muscles, which is an important muscle group for functional activities18 and the focus of many of the studies examining strengthening exercises in people with CP. The pendulum test is particularly suited to the evaluation of spasticity in children because it is not intimidating and can be administered in a relatively short period of time.18
The purpose of our study was to examine the premise that strengthening exercises will increase spasticity, as measured with the pendulum test, in people with CP. Spasticity was examined before and after a single bout of exercise training. Our aims were to examine the effect of quadriceps femoris muscle exercise on resistance to passive knee motion in: (1) the exercised limb, (2) the nonexercised limb, and (3) children with CP as compared with control subjects of similar ages with no known neurological impairments. Three different types of exercises were utilized: isometric, isotonic, and isokinetic.
| Methods |
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TopAbstractIntroductionMethodsResultsDiscussionConclusionReferences |
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Because the severity of spasticity was a potential confounding variable, all subjects with CP were assessed for their degree of right quadriceps femoris muscle spasticity using a modified version of the Ashworth scale.19 This version used the same methods to elicit spasticity as the original Ashworth scale13 but added hypotonia as a possible grade. In this modified grading system, hypertonia was assessed as 0 and normal as 1, as opposed to 0 in the original grading system. Eight subjects with CP had grade 1 spasticity (no resistance to passive motion), 6 had grade 2 spasticity (mild resistance to passive motion), 6 had grade 3 spasticity (moderate resistance to passive motion), and 4 had grade 4 spasticity (substantial resistance to passive motion). A greater number of subjects with CP were recruited as compared with control subjects with no known neurological impairments in anticipation of the need for subgroups to test for a relationship between the level of baseline spasticity and changes that might occur with exercise. The mean age was 11.6 years (SD=3.5, range=7–17) for the control subjects and 11.4 years (SD=3.0, range=7–17) for the subjects with CP.
Instrumentation/Testing Protocol
Electrogoniometers can provide a record of pendulum test oscillations.20 The electrogoniometer we used consisted of a potentiometer attached to both a stationary arm and a movable arm. The movable arm slid within a milled encasement that allowed the center of the potentiometer to maintain alignment with the knee joint center. Electromyographic (EMG) data were collected using disposable surface silver-silver chloride electrodes that were hardwired and attached to the remote unit of an EMG system*. The signal was differentially amplified and sent to a base unit via a fiber optic cable where it was sampled at 1 kHz and high-pass filtered (40 Hz). The EMG and electrogoniometer data were simultaneously displayed on a computer screen during collection using customized software.
All subjects wore shorts and were barefoot to prevent clothing from interfering with the instrumentation (EMG system and electrogoniometer) and to prevent variation in leg movement due to different types of shoes. Surface electrodes were placed over the vastus lateralis (VL), medial hamstring (MH), tibialis anterior (TA), and medial gastrocnemius (MG) muscles bilaterally, and a reference electrode was placed over the anterior medial aspect of the left lower leg. A maximum muscle contraction was elicited from the subjects, and the electrode was placed over the most prominent aspect of the muscle belly. Prior to electrode placement, the skin was prepared by shaving, when necessary, and rubbing with an alcohol wipe to cleanse and lightly abrade the skin. Subjects were seated in a specially designed chair with the trunk reclined between 20 and 40 degrees from vertical to minimize the effect of possible hamstring muscle tightness (Fig. 1). The trunk and thighs were secured to the chair with padded straps to maintain the position throughout the testing procedures, and a pillow was placed behind the subjects' head to promote comfort and relaxation.
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The testing protocol is outlined in Table 1. Four pendulum tests were conducted bilaterally before and after each type of resistive exercise. Subjects were asked to relax and sit quietly during pendulum tests. The investigator (EGF or TWH) held each subject's heel and extended the knee from its resting position to the point of maximum knee extension (or the onset of an increase in passive hamstring muscle force for subjects with spasticity). The examiner then released the heel, allowing the leg to drop into flexion and swing freely (Fig. 1). In subjects without CP, the resulting motion is a series of oscillations that gradually diminish in amplitude.12,16,18,20,21 In the presence of spasticity, the stretch reflex is elicited when the lower limb is released, causing muscle contractions that modify the swinging motion. The result is reduced excursions of the swinging limb, a fewer number of oscillations, and a shorter test duration.18 A minimum of 15 seconds of rest occurred between successive pendulum tests for the same leg in order to ensure reliable measurements.17
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Isometric and isokinetic exercises were done using a Kin-Com dynamometer (Hardware Version 125E Plus, Software Version 3.20),
with verbal encouragement and visual feedback from the monitor to obtain maximum efforts. Isometric exercises were done with the knee positioned at 60 degrees of flexion, which was sustained to a count of 5 seconds. Isokinetic knee extension exercises were done at 60°/s. Starting from a relaxed, gravity-neutral position of approximately 90 degrees of knee flexion, the subjects were instructed to extend their knee as rapidly and as far as possible. The end positions set on the machine were the subjects' maximum joint range of motion for knee flexion and extension. Isotonic knee extension was performed using cuff weights around the ankle. Prior to the exercise session, the maximum amount of weight possible for 5 repetitions of isotonic exercises was determined for each subject. Varying weights were assessed until the maximum load that could be lifted through full range of motion for 5 repetitions was determined using subject feedback and the physical therapist's observations. The subject was instructed to extend his or her knee joint to a count of 5 seconds provided by the examiner. Following each repetition of knee extension exercise, the examiner held the ankle and passively flexed the knee to its starting position at approximately 90 degrees.
Data Analysis
Pre- and post-exercise resistance to passive motion was assessed for both the right (exercised) and left (nonexercised) knees using the pendulum test data. Electrogoniometer data (in volts) was converted to joint angular data (in degrees) using the conversion factor obtained during the calibration procedure. Outcome measurements obtained from the pendulum data were:
Measurements are illustrated for a control subject and a subject with CP in Figure 2. A decrease in any of these measurements following exercise would indicate an increase in spasticity. These measurements have been found to be sensitive to the severity of spasticity in people with CP, with first swing excursion exhibiting the greatest sensitivity to quadriceps femoris muscle spasticity.18
During the pendulum test, EMG data for the tested limb were examined for evidence of inappropriate muscle contractions. For a trial to be successful, there would have been an absence of muscle activity throughout the test in the control subjects. In the subjects with CP, VL activity was often visible during downward swings and MH activity was often visible during upward swings due to the elicitation of the stretch reflexes. All trials that did not exhibit evidence of voluntary muscle activity during data collection were evaluated further. The data were examined to determine that there was no increase over baseline activity for all subjects and that the EMG activity observed for subjects with CP occurred as a response to stretch (eg, during knee flexion for the VL and knee extension for the MH). Trials in which EMG activity was observed during muscle shortening, indicating voluntary activity, were excluded.
A main-effects repeated-measures analysis of variance (ANOVA) based on the Latin square randomized design was performed with a random subject effect and 4 fixed effects (order, subject group (subjects with CP versus control subjects), limb, exercise type). After pooling the data over exercise type, 2-sample t tests were used to examine the difference in pre- and post-exercise outcome measurements between the subjects with CP and the control subjects. A linear regression analysis was used to examine the effect of varying severity of quadriceps femoris muscle spasticity on each measure for the subjects with CP. Subjects with CP were placed into 1 of 3 groups based on their degree of quadriceps femoris muscle spasticity, as indicated by modified Ashworth scale scores19: (1) subjects with no resistance to passive movement, (2) subjects with mild or moderate spasticity, and (3) subjects with severe spasticity.
| Results |
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TopAbstractIntroductionMethodsResultsDiscussionConclusionReferences |
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The main-effects repeated-measures ANOVA revealed no differences in pre-exercise versus post-exercise data based on exercise order, exercise type, or subject group (subjects with CP versus control subjects) (P>.05). A suggestion of a difference was found between the exercised and nonexercised limbs. Because all subjects received all 3 exercises and there was no exercise type effect, the results were averaged and differences in means between pre- and post-exercise measurements were calculated (Tab. 2D). In order to determine whether the limb effect was similar for the subjects with CP and the control subjects, the differences in pre- and post-exercise measurements were calculated by subtracting the pre-exercise value from the post-exercise value.
Comparisons were made between the exercised limb and the nonexercised limb using a paired t test with 95% confidence intervals. No specific limb effects were found for number of oscillations or duration of oscillations (P>.10) for either subject group. There was no difference in first swing excursion for the nonexercised limb versus the exercised limb for the control subjects (P=.07) and the subjects with CP (P=.06). These results suggest that the limb effect was similar for both subject groups and illustrates the importance of including a control group.
Although the main-effects repeated-measures ANOVA did not find a difference in pre-exercise versus post-exercise data based on subject group (subjects with CP versus control subjects), further statistical analyses were performed to examine these data. Two-sample t tests were used to compare the differences between pre- and post-exercise outcomes between the 2 subject groups after averaging over the 3 types of exercise. Separate tests were done for the exercised and nonexercised limbs. Confidence intervals at 95% were calculated. No differences were found in outcome measures between the subjects with CP and the control subjects (Tab. 3). Confidence intervals were similar for the exercised and the nonexercised limbs and could be in the direction of increased or decreased resistance to passive motion for the subjects with CP versus the control subjects.
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Because the subjects were asked to perform exercises with maximum efforts, we believed that it was important to examine the joint moments and forces used during each exercise. The control subjects were able to generate greater joint moments as compared with subjects with CP for all 3 types of exercise. The control subjects generated an average of 89.4 N·m (SD=42, range=24.0–162.2) during isometric exercise and 82.9 N·m (SD=38, range=30.6–161.4) during isokinetic exercise. The subjects with CP generated 37.2 N·m (SD=21, range=10.2–89.2) and 29.8 N·m (SD=21, range=3.6–84.1), respectively, for these exercises. Isotonic exercises were done with ankle weights that were 11.2 kg (SD=4, range=5.5–15.9) for the control subjects and 6.4 kg (SD=4, range=1.4–14.3) for the subjects with CP.
| Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionConclusionReferences |
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The considerable variation in spasticity within the group of subjects with CP was a potential confounding variable that could have been masked in the ANOVA. We recruited a greater number of subjects with CP and created subgroups based on severity of spasticity, and the statistical tests performed did not result in significant findings. These groups, however, were not equal and contained a small number of subjects. Despite these limitations, we believe that the severity of spasticity was not an important factor. The change in mean first joint excursion following exercise—our most sensitive measure—was greater for subjects with CP and no detectable quadriceps femoris muscle spasticity (grade 1) than for those with severe spasticity (grade 4). In addition, the 3 subjects with CP who consistently exhibited decreased first joint excursion for the exercised limb did not exhibit severe quadriceps femoris muscle spasticity.
We contend that a fundamental problem in the interpretation and application of Bobath concepts is that their clinical view of "spasticity" differs substantially from the definition that is widely adopted and supported today. The Bobaths described spasticity as a phenomenon that could be assessed by observing a patient move.2,22 They stated that hypertonus is caused by tonic reflexes (tonic labyrinthine, asymmetrical tonic neck reflexes; symmetrical tonic neck reflexes; associated reactions; and positive and negative supporting reactions),2 and they included co-contraction2 and "abnormal coordination"22 in their description of spasticity. They were critical of clinicians who measured spasticity at the "local muscular" level.22,23 Clearly, their descriptions differed from the definition accepted by neuroscientists in 198011 and used for the present study. In this definition, spasticity is a velocity-dependent increase in muscle stretch reflexes resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome.
The children with CP who performed exercises in this study appeared to change posture, and this might fit the Bobath description of increased spasticity. Many children with CP moved their left lower extremity and tensed muscles in their upper extremities, trunk, and face when asked to perform isolated right knee extension exercise. Although extraneous, or nonagonist, movement was also observed in the subjects without CP, especially younger children, it was most pronounced in the children with CP.
Once a theory becomes shaped and championed, the clinical practice model is not always adjusted as new knowledge is gained.24 The view that muscular effort will increase spasticity continues to be taught in some physical therapy curriculums. Despite evidence that strengthening exercise programs can improve function in children with CP,4,5,7–9 the use of weight training equipment is not common. We have seen reluctance to use resistive exercise following surgical or pharmacological treatments that have reduced or eliminated spasticity.
In our study, we assessed spasticity before and after a single bout of exercise training. Although long-term exercise programs have not demonstrated detrimental effects on related outcomes such as range of motion, spasticity, in our view, was not critically examined, and this is a direction for future research.
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TopAbstractIntroductionMethodsResultsDiscussionConclusionReferences |
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| Footnotes |
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Study approval was obtained from the UCLA Human Subject Protection Committee.
This project was supported by Foundation for Physical Therapy grant 95R-23-FOW-01 and by United Cerebral Palsy of Los Angeles and Ventura Counties.
* Konigsberg Instruments Inc, 2000 E Foothill Blvd, Pasadena, CA 91107. 
Chattanooga Group Inc, 4747 Adams Rd, Hixson, TN 37343.
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This article has been cited by other articles:
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  O. Verschuren, M. Ketelaar, J. W. Gorter, P. J. M. Helders, C. S. P. M. Uiterwaal, and T. Takken Exercise Training Program in Children and Adolescents With Cerebral Palsy: A Randomized Controlled Trial Arch Pediatr Adolesc Med, November 1, 2007; 161(11): 1075 - 1081. [Abstract] [Full Text] [PDF]
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 E. G Fowler, T. H. Kolobe, D. L Damiano, D. E Thorpe, D. W Morgan, J. E Brunstrom, W. J Coster, R. C Henderson, K. H Pitetti, J. H Rimmer, et al. Promotion of Physical Fitness and Prevention of Secondary Conditions for Children With Cerebral Palsy: Section on Pediatrics Research Summit Proceedings Physical Therapy, November 1, 2007; 87(11): 1495 - 1510. [Abstract] [Full Text] [PDF]
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 M. Unger, M. Faure, and A. Frieg Strength training in adolescent learners with cerebral palsy: a randomized controlled trial Clinical Rehabilitation, June 1, 2006; 20(6): 469 - 477. [Abstract] [PDF]
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S W Blundell, R B Shepherd, C M Dean, R D Adams, and B M Cahill Functional strength training in cerebral palsy: a pilot study of a group circuit training class for children aged 4-8 years Clinical Rehabilitation, January 1, 2003; 17(1): 48 - 57. [Abstract] [PDF]
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