Numerous qualitative and quantitative measures have been proposed for the measurement of spasticity (Katz and Rymer, 1989; Pierrot-Deseilligny, 1990; Allison and Abraham, 1995). Clinicians and researchers have expressed dissatisfaction with existing ordinal spasticity scales, which lack precision, rely on clinical judgements, and may not have generalizable reliability. This dissatisfaction has fuelled the search for quantitative spasticity measures.
If qualitative and proposed quantitative spasticity measures are to be useful for patient management decisions, such measures must be able to detect differences in spasticity brought about by clinical treatments. One such clinical treatment for spasticity is cryotherapy. Muscle cooling was chosen as the treatment for this study because of its frequent mention in spasticity treatment literature, for its relatively negligible side effects, and for its ease of application. The purpose of this study was to test the sensitivity of qualitative and quantitative measures for spasticity by applying those measures before and after a reduction in spasticity brought about by cryotherapy.
Several authors have used qualitative ordinal scales to assess the severity of spasticity by applying a manual stretch to a muscle group and scoring the resistance encountered (Ashworth, 1964; Bohannon and Smith, 1987; Peacock and Staudt, 1991; Allison et al., 1996). Despite the limitations of these scales and a recognized need for newer, more quantitative spasticity measures, Katz and Rymer (1989) stated that these qualitative scales are the ‘present yardstick against which newer, more exact methods must be compared’.
Some potential quantitative spasticity measures have been investigated. Tendon vibration will reduce the amplitude of H-reflexes (Gillies et al., 1969; Lance et al., 1973) caused by presynaptic Ia inhibition (Iles and Roberts, 1986; Pierrot-Deseilligny, 1990), but this inhibition is impaired in patients with spasticity (Hagbarth, 1973; Milanov, 1992a). Some investigators (Nance et al., 1989; Milanov, 1992b) have used the ratio of the H-wave evoked during vibration to the H-wave at rest (Hvib/Hctrl) as a measure of spasticity. Others have studied the sensitivity of H-reflexes to reciprocal inhibition associated with voluntary antagonistic muscle contraction. Leonard et al. (1990) and Boorman et al. (1992) defined reciprocal inhibition as the ratio of the soleus H-reflex amplitude during dorsiflexion to the H-reflex at rest (Hdf/Hctrl), and found deficits in patients with spasticity.
A third quantitative measure that discriminates between spastic and non-spastic muscle groups has been called the reflex threshold angle (RTA), stretch reflex angle or stretch reflex threshold by investigators (Powers et al., 1988, 1989Katz and Rymer, 1989; Katz et al., 1992; Levin and Hui-Chan, 1993; Wolf et al., 1996). The test consists of stretching spastic muscle groups and recording the angle at which a simultaneous rise in torque and/or EMG activity occurs during the imposed stretch. Allison and Abraham (1995) demonstrated significant correlations among the modified Ashworth scale (MAS) and the Hdf/Hctrl ratio, the Hvib/Hctrl, the RTA and a simple functional test called timed toe tapping (TTT). Although these quantitative measures show promise as potentially useful measures of spasticity, only the RTA has been used to assess the efficacy of spasticity treatment (Dewald et al., 1996; Brouwer et al., 1998).
Cold applications have been used for some time to reduce spasticity clinically. Bassett and Lake (1958) reported three case studies of patients with UMN lesions, noting reduced clonus and spasticity for both cold water immersion and crushed ice wrapped in wet towels. Inasmuch as no spasticity measurements were reported, the assessments of reduced spasticity were apparently based on clinical judgment.
Electromyographic measurements have shown clonus to be reduced or abolished with local ice applications over the spastic muscles (Knutsson, 1970; Miglietta, 1973). Overall resistance to stretch has also been shown to decrease with ice treatment (Knutsson, 1970). Price and Lehmann (1990) reported passive (non-reflexive) stiffness to increase with cold application, and they attributed the overall decrease in stiffness with cryotherapy to a reduced stretch reflex response. This result is in harmony with the findings of reduced Achilles tendon reflex (Petajan and Watts, 1962) and reduced H-reflexes (Knutsson and Mattson, 1969) with cooling. Functional improvements consistent with spasticity reduction have also been reported with cooling. Knutsson (1970) studied the kinematics of spastic gait before and after cooling and observed increased dorsiflexion in late swing phase, consistent with a reduction in spasticity in the antagonistic spastic plantarflexors.
Miglietta (1973) concluded that reduced clonus was dependent on reducing the sensitivity of the muscle spindles, noting over the duration of the cryotherapy application that clonus did not abate until intramuscular temperature dropped. Indeed, Mense (1978) observed a strong depression of cat Ia activity with cold application. In contrast, type II fibers were found to be more active and Ib fibers were largely unaffected by cold.
Not all authors, however, have reported consistent findings with cooling. Urbscheit et al. (1971) found spastic patients to respond in unpredictable ways when ankle jerks and H-reflexes were measured before and after cooling. Bell and Lehmann (1987) found no reduction in H-reflexes or tendon reflexes after cooling in normal subjects. Price et al. (1993) reported a significant reduction of spasticity during cryotherapy for 11 of 17 subjects with significant spasticity levels. However, they also found a significant increase in spasticity for two of these subjects. Chiara et al. (1998) found that a cold bath slightly increased spasticity in subjects with multiple sclerosis. These contrary findings underscore the possibility that the underlying neural and mechanical mechanisms are complex and variable between spastic patients.
Cooling time required to reduce spasticity is controversial. Miglietta (1964) reported a reduction in clonus frequency within one minute of ice water immersion. Lehmann and deLateur (1990) argued that cryotherapy must be applied long enough to allow for intramuscular cooling: typically 20–30 minutes but dependent on the thickness of subcutaneous fat. This suggestion was based on Miglietta's (1973) finding of no reduction in clonus before intramuscular cooling, plus the suspicion that reduced spindle sensitivity with cold is the mechanism underlying the reduced stretch reflex with cooling (Ottoson, 1965; Mense, 1978). Bell and Lehmann (1987) measured cooling of the medial gastrocnemius with an intramuscular temperature probe during cryotherapy with an ice/water pack. They found only a slight reduction in intramuscular temperature (to about 31 °C) after 20 minutes of cooling. However, using ice water immersion, Miglietta (1973) measured lateral gastrocnemius intramuscular temperature at 15 °C after only 10 minutes of cooling.
The weighted linear composite variable formed by the following five dependent variables is significantly different when pre- and post-cryotherapy measures are compared:
- Modified Ashworth scale (MAS) scores
- Timed toe tapping (TTT) scores
- Ratio of maximum soleus H-wave amplitudes measured with and without vibration to the Achilles tendon (Hvib/Hctrl ratio)
- Ratio of maximum soleus H-wave amplitudes measured with and without dorsiflexor muscle activation (Hdf/Hctrl ratio)
- Reflex threshold angle (RTA): the ankle angle at which a reflexive burst in EMG activity begins during an imposed plantarflexor stretch.
Material and methods
Twenty-six adult traumatic brain injured (TBI) subjects were examined in this study. These included 22 males and 4 females. The mean age was 28.15 years (range: 18–57, SD 10.78). Following physician approval, subjects were selected from a pool of volunteers at the Healthcare Rehabilitation Center in Austin, TX. Inclusion criteria were:
- Age 18 or older
- History of TBI at least six months prior to testing
- Stable medical condition
- Adequate range of motion at the ankle (zero degrees dorsiflexion to 40 degrees plantar flexion) without excessive inversion or hypersensitive tactile plantar reflexes
- Ability to understand and follow instructions to relax the ankle and sit in a wheelchair for about one hour
- Rancho Los Amigos cognitive scale score of 7 or 8
- Absence of Raynaud's syndrome, peripheral vascular disease and pregnancy
Patients were interviewed to determine etiology, characteristics and duration of deficits. All subjects provided informed consent according to the guidelines set forth by the Department of Health and Human Services concerning protection of human subjects.
This study employed a doubly multivariate repeated measures experimental design with the dependent measures taken before and after the experimental treatment. Each of the 26 subjects received a battery of tests applied to both ankles, resulting in 52 cases for the analyses. The within-subjects factors were cryotherapy (with two levels: pre and post) and ankle side (two levels: right and left); dependent measures were: MAS scores, TTT scores, Hvib/Hctrl and Hdf/Hctrl ratios and RTA measures.
data and instrumentation
A full description of the data collection apparatus and testing procedures has been provided in a previous report (Allison and Abraham, 1995); a brief description is presented here. The instrumentation included electrical stimulation equipment (Grass Instruments model S48D), electromyographic recording apparatus (Iomed, Inc.), a vibrator (Panasonic model EV242W), an oscilloscope (Tektronix model 5111A), a torque motor (Parker Compumotor Inc., model 1030B) and a Macintosh LC II computer with an analog-to-digital converter board (LabLC) and controlling software (LabView version 2.2, National Instruments). Subjects were seated in an adjustable chair with armrests and headrest, and the apparatus was adjusted such that the hip joint was flexed to 80o and the knee to 60o.
The sequence of tests was randomized for each subject to avoid order effects. The one exception was that Hctrl was measured before Hvib or Hdf because the targeted range of M-wave amplitudes for the latter two tests was determined during Hctrl testing.
Subjects removed shoes and socks and assumed a sitting position. The investigator assigned MAS scores after passively moving the ankle from a position of full plantarflexion to full dorsiflexion. The investigator performed five to eight repetitions of the ankle movement before assigning a score based on the descriptions in Table 1.
With the resting subjects seated and the vibration and electrical stimulation apparatus prepared, the torque motor was used to position the footplate such that the ankle was in a neutral (zero degrees dorsiflexion) position. Stimulating intensity was adjusted to evoke the largest H-wave amplitude available in the presence of a measurable M-wave. Ten second intervals separated the electrical stimuli used to evoke the H-reflexes, to allow for H-reflex baselines to return to normal (Hugon, 1973; Lance et al., 1973). A set of ten H-waves was averaged to provide the Hctrl value for analysis.
Vibration was applied to the Achilles tendon at a point 5 cm proximal to its insertion on the calcaneus. Following 20 seconds of vibration, an H-reflex (Hvib) was elicited with an electrical stimulus intensity adjusted to elicit an M-wave amplitude within the range of values for M-waves observed during the collection of the Hctrl measures. A set of ten H-waves was averaged to provide the Hvib value for analysis.
To obtain the Hdf measure, subjects first performed a maximal voluntary contraction (MVC) of the dorsiflexors with the foot neutrally positioned by the torque motor. Using the oscilloscope display of the torque signal as a guide, the subjects then provided dorsiflexion contractions of 75% MVC at the same ankle position. Again, electrical stimulus intensity was adjusted to elicit M-wave amplitudes within the range of M-waves amplitudes observed with Hctrl measures, and a set of ten H-waves was averaged to provide the Hdf value for analysis.
The torque motor provided a ramp stretch of the triceps surae by rotating the ankle from 40 degrees plantarflexion to zero degrees neutral at an average angular velocity of 235 degrees per second. This procedure was repeated ten times, with a 20 second rest between repetitions. The RTA was identified as the ankle angle at which a reflexive burst in EMG activity began during the imposed plantarflexor stretch (Figure 1). The ten measurements of RTA were averaged to provide one representative RTA score for each ankle.
Timed toe tapping scores
While sitting, subjects began tapping the toes on a wedge as rapidly as possible, alternating between dorsiflexion and plantarflexion ankle motions. The 15 second test period was timed with a stopwatch and the number of times the toes tapped on the wedge was recorded with an electronic counter. The highest TTT score from three trials was entered into the analyses.
After all the above measures had been completed, the triceps surae muscle group was cooled by a 20 minute application of a gel-filled cold pack (at 10 to 15 degrees Fahrenheit), placed against the skin of the posterior calf. The cold pack was molded to conform closely to the contours of the calf, and Velcro straps secured the cold pack in place. During cryotherapy, the subject remained in the chair used for data collection and kept the limbs relaxed.
Immediately after the 20 minute period of cryotherapy, the battery of tests was repeated. The post-treatment sequence of tests was also randomized to avoid order effects. Post-cryotherapy testing was completed within 25–30 minutes following removal of the cold pack. In order to test for post-cryotherapy warming effects, scores for each post-cryotherapy spasticity measure were compared for two groups: those tested earliest in the sequence and those tested last. Paired t-tests with alpha level set to 0.05 revealed no significant differences between earliest- and last-tested scores for any of the variables, indicating that the effects of cryotherapy did not significantly dissipate during the 25–30 minutes required for post-cryotherapy testing.
Descriptive statistics were calculated for subject and experimental variables. The RTA was identified as the joint angle at which a burst of soleus EMG activity indicated a reflex response to the stretch. Average Hvib/Hctrl and Hdf/Hctrl ratios were calculated after peak-to-peak H-wave measurements were obtained for the H-reflexes evoked under the three conditions (at rest, vibration and isometric dorsiflexion). M-wave stability under the three conditions was assessed by one-way analyses of variance (ANOVA) using the software package Microsoft Excel, version 4.0. SPSS for Windows, release 8.0 was used to perform a multivariate repeated measures ANOVA for the four ratio scale variables (Hvib/Hctrl, Hdf/Hctrl, RTA and TTT). Post-hoc analyses consisted of paired t-tests (pre-cryotherapy versus post-cryotherapy) for the ratio scale variables and a Wilcoxon signed-ranks test for the ordinal scale variable (MAS). The alpha level was set to 0.10 for the ANOVA and the post-hoc procedures.
MAS scores ranged from zero to three but the distribution was positively skewed. Lowered post-cryotherapy MAS scores demonstrated an effective reduction in spasticity for 28 of the 52 cases. The remaining 24 cases had no change in pre- to post-cryotherapy MAS scores. Post-cryotherapy MAS scores were lowered by one category in 27 cases and by two categories in one case. Mode and median for pre-cryotherapy MAS scores were both one; post-cryotherapy MAS score median and mode were both zero. Frequencies of cases for each MAS score before and after cooling are presented in Figure 2. Descriptive statistics for the other dependent measures are displayed in Table 2.
The multivariate repeated measures ANOVA revealed a significant difference in test scores between the pre- and post-cryotherapy test batteries. No significant effects were observed for ankle side or the interaction between sidedness and cryotherapy. The MANOVA source table is presented as Table 3. Significant pre- and post-cryotherapy differences for all dependent measures contributed to the main effect for cryotherapy, as shown in Table 4.
M-wave amplitudes were consistently stable across conditions, evidenced by F-ratios below the critical F-value of 3.35 in all 104 comparisons for the 26 subjects included in the analyses. One additional subject was measured but not included in the analyses because of unstable M-waves.
The significant main effect for cryotherapy was expected inasmuch as the treatment is used to reduce spasticity. The most pertinent question for this study, however, was not whether the main effect would be significant, but how each dependent measure would contribute to the effect. Analysis of individual contributions from the dependent measures showed test scores were affected by cold, but not necessarily in a direction associated with reduced spasticity.
Post-hoc analyses revealed that all five dependent measures contributed to the main effect for cryotherapy. However, only two of the five dependent measures (MAS and RTA) showed changes in the anticipated directions; that is, they demonstrated appropriate sensitivity to the reduction in spasticity resulting from cryotherapy. MAS scores were closer to zero (normal tone) after cooling, indicating a reduction in spasticity (Figure 2). RTA scores were similarly closer to the zero degrees (neutral) ankle position after cooling; thus, the EMG reflex response occurred later in the stretch, after greater angular excursion compared to RTA scores pre-cryotherapy (Figure 1).
The effect size for cryotherapy as measured by RTA was so small (mean difference = 1.5 degrees) that its clinical relevance may be questionable. However, our aim was not to demonstrate the effectiveness of cryotherapy for spasticity treatment. Rather, we wished to discover whether quantitative measures such as RTA might be sensitive enough to detect changes in spasticity brought about by a treatment assumed to be effective. The ability of the RTA measure to detect such a small treatment effect underscores a potential advantage of using a quantitative spasticity measure in other circumstances where qualitative ordinal scales may not be sensitive to small changes.
Elevations in the post-cryotherapy H-reflex ratios might be mistakenly interpreted to indicate an increase in spasticity, particularly given the demonstrated positive correlations between each of these ratios and MAS scores (Allison and Abraham, 1995). Rather, this result suggests that presynaptic and reciprocal inhibition, the underlying mechanisms tested by the H-reflex ratio tests, are not improved by cryotherapy although other measures show that spasticity is reduced. Indeed, the significant elevations of the H-reflex ratios suggest that these two inhibitory mechanisms are further impaired by cryotherapy. These contrary results underscore the complex nature of spasticity and the competing influence of central and peripheral mechanisms.
Elevation of the H-reflex ratios following cryotherapy may be explained by investigations into reflex modulation by cutaneous afferents responding to cold. Summarizing numerous studies of these effects, Michlovitz (1990) concluded that cold facilitates alpha-motoneurons and inhibits gamma-motoneurons. Consequently, for these effects to result in spasticity reduction, the net effect of gamma inhibition must exceed that of alpha facilitation. If these mechanisms operate simultaneously, spasticity tests which incorporate muscle spindle activation (MAS and RTA) would be sensitive to gamma inhibition and would reveal cold-induced spasticity reduction; H-reflex tests of the monosynaptic reflex arc that bypass the spindles would detect only the alpha facilitation, resulting in elevated H-reflexes.
The usual inhibitory effects of vibration and voluntary antagonist muscle activation might well be diminished if cutaneous afferents respond to cold by facilitating the alpha motoneurons and inhibiting the gamma motoneurons. Reduced gamma input to the muscle spindles would render them less sensitive to vibration, resulting in fewer action potentials transmitted via the Ia afferents and consequently less presynaptic inhibition. A facilitated antagonist alpha pool would be closer to firing threshold, requiring less descending facilitation for activation; reduced descending input to the dorsiflexors would also mean less reciprocal inhibition of the plantarflexors.
It may be counterintuitive to think of a simultaneous reduction in spasticity and a facilitation of the alpha motoneuron pool. However, since spasticity is defined as an increased sensitivity to stretch, the manifestation of spasticity depends on an intricate interplay between peripheral and central mechanisms. If there is strong central inhibition of the gamma motoneuron pool, the muscle spindles in the peripheral muscle may be so insensitive that even a vigorous stretch will fail to elicit much afferent activity in the Ia pathway. Consequently, the alpha pool responsible for reflex activation of a stretched muscle may fail to respond to stretch even if its neurons are depolarized near threshold by prior facilitation. Therefore, cryotherapy may reduce spasticity (as tested by mechanically stimulating desensitized peripheral receptors) even while further contributing to dysfunction in the central mechanisms potentially responsible for spasticity in the resting state. In light of these considerations, findings from this study are consistent with the idea of competing alpha and gamma effects when cutaneous afferents respond to cold.
Competing effects of cold may also have been responsible for the lowered post-cryotherapy TTT scores. Although it seemed reasonable to propose that a reduction in spasticity might enhance motor control and improve performance on a task requiring coordination, the speed required for the TTT test was probably impaired by muscle and nerve cooling. Cold is known to increase joint stiffness and retard joint motion (Hecox, 1994). If the speed impairment was greater than the improvement in coordination, the net effect would be poorer TTT performance. Furthermore, slower nerve conduction velocities resulting from cryotherapy (Denys, 1991) and the consequent retardation of muscle activations may have combined to overshadow any TTT advantage gained by spasticity reduction.
Of the battery of potential quantitative measures of spasticity only the RTA test demonstrated appropriate sensitivity to spasticity reduction resulting from cryotherapy. The RTA measure demonstrated sufficient sensitivity to detect even a small treatment effect. Future studies of other spasticity interventions, particularly those thought to enhance spinal cord inhibitory mechanisms, should show whether tests such as RTA, Hdf/Hctrl and Hvib/Hctrl might be useful in documenting effectiveness of spasticity treatments.
The authors wish to thank Mr Christopher Stanford for technical assistance with the data collection apparatus and with software development. Financial support for this study was provided by Healthcare Rehabilitation America, Inc. Portions of this work have been presented orally at professional meetings. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting the views of the Department of the Army or the Department of Defense.
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