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What does the The Ashworth scale (Ashworth 1964) has gained widespread

clinical acceptance as a measure of spasticity of central or


peripheral origin. Its use is also reported frequently in clinical
Ashworth scale really trials documenting changes in spasticity throughout the
course of a disease or as a result of an intervention. The classic
measure and are description had the examiner rate the amount of tone felt as a
limb was moved passively through its arc of motion (Table I).

instrumented Later modifications incorporated an estimation of how soon


in the motion, and how much during the motion, the resis-
tance was felt (Bohannon and Smith 1987). To our knowl-
measures more valid edge, how this added specification may have affected the
validity of the scale for measuring spasticity has not been
and precise? addressed. An observed tendency for scores to cluster in the
mid-ranges has led some authors to spread out the middle
portion of the scale (Bohannon and Smith 1987). However,
poorer reliability may accompany the greater discriminatory
Diane L Damiano* PhD PT; ability of this modification (Pandyan et al. 1999). Despite its
Jeffrey M Quinlivan ME; shortcomings and lack of consensus in the exact scoring, the
Bryan F Owen MS; Ashworth scale with all of its variants remains the standard
Patricia Payne BS PT; with which other measures of spasticity are compared.
Karen C Nelson MD; The clinical import of the Ashworth scale has not been well
Mark F Abel MD, University of Virginia, Department of established and is, in part, enmeshed in the controversy as to
Orthopaedics, Charlottesville, VA, USA. whether spasticity has a significant or causal relationship with
motor performance (Sahrmann 1977). Ashworth scores are
*Correspondence to first author at Washington University, consistently reduced in cerebral palsy (CP) after surgical inter-
Human Performance Laboratory/Barnes-Jewish Hospitals, ventions designed specifically to reduce spasticity (McLaughlin
4555 Forest Park Parkway, St. Louis, MO 63108, USA. et al. 1998, Butler et al. 2000). However, ordinal scales such as
E-mail: dld6830@bjc.org the Ashworth may lack precision and sensitivity for measuring
and detecting smaller degrees of, or changes in spasticity. Even
though the Ashworth scale purportedly gauges the degree of
spasticity, which by definition is a heightened response to
stretch that is velocity dependent (Lance 1980), the test is per-
This study aimed to explore the limitations of the Ashworth formed at a single, although moderately brisk, speed. Even
scale for measuring spasticity. An isokinetic dynamometer to more importantly, the Ashworth scale does not quantify spas-
quantify resistance to passive stretch and surface EMG was ticity exclusively, if at all; rather, it measures passive resistance
used to verify if a stretch response occurred and, if so, at what to motion that may or may not be caused by a heightened
joint angle. The authors sought to determine which stretch response. In order to develop a more valid and quanti-
components of passive resistance (magnitude, rate of change, tative measure of spasticity, or to identify components of spas-
onset angle of stretch, or velocity dependence) were most ticity or resistance more precisely, multiple biomechanical
related to Ashworth scores and which were related to motor and electrophysiological methods have been developed.
function in cerebral palsy (CP). Twenty-two individuals with These methods include, but are not limited to, H-reflex test-
spastic CP (11 males, 11 females; mean age 11.9 years, SD 4.3) ing (Angel and Hoffman 1963), quantification of deep tendon
and a comparison group of nine children without CP (four reflexes (Zhang et al. 2000) and clonus (Hidler and Rymer
males, five females; mean age 11.3 years, SD 2.5)participated 1999), resonant frequency tests (Price et al. 1991), ramp and
in the study. The group with CP included those with a hold tests (Katz and Rymer 1989), pendulum tests (Bajd and
diagnosis of spastic diplegia, hemiplegia, or quadriplegia, Vodonik 1984, Fowler et al. 2000), and instrumented torque
distributed across Gross Motor Functional Classification measurements during passive motion at preset velocities
Levels. Procedures included: (1) clinical assessment at the (Broberg and Grimby 1983, Firoozbakhsh et al. 1993,
knee joint, (2) functional assessments, and (3) isokinetic Engsberg et al. 1996, Perell et al. 1996, LaMontagne et al. 1998,
assessment of passive resistance torque in hamstrings and Akman et al. 1999, Damiano et al. 2001a). Each of these meth-
quadriceps at three velocities. EMG data were recorded ods varies in the degree of expertise and special equipment
simultaneously to identify stretch responses. Detecting stretch required, the neural or peripheral component measured, the
responses using the Ashworth scale compared with joints that can be tested, the reliability of the measurements,
instrumented measures showed near complete agreement at and the correlation of the parameters obtained with clinical
extremes of the scale, with marked inconsistencies in mid- and functional measures. Multiple reports have been pub-
range values. Ashworth scores were correlated with lished describing, validating, and comparing these measures
instrumented measures, particularly for the quadriceps, with in a variety of patient populations (Katz et al. 1992, Skinner
higher correlations to the rate of change in resistance 1992, Sehgal and McGuire 1998).
(stiffness) and onset angle of stretch than to peak resistance In this investigation, the goal was to determine the validity
torque. Those with greater resistance tended to have poorer of the Ashworth scale by using an isokinetic dynamometer to
function with isokinetic relations typically stronger. quantify resistance to passive stretch in knee flexion and
extension, and EMG recording to verify if a stretch response

112 Developmental Medicine & Child Neurology 2002, 44: 112118


occurred and, if so, at what joint angle. Furthermore, we want- measures because this method closely simulates the Ashworth
ed to compare the multiple parameters quantified through scale; its use has been reported as reliable and valid in several
instrumentation, such as magnitude of resistance, change in populations and it is clinically accessible (Broberg and Grimby
resistance with angle, onset angle of stretch, and velocity 1983, Firoozbakhsh et al. 1993, Perell et al. 1996, Damiano et
dependency of each of these parameters, with those obtained al. 2001a). In this protocol, the isokinetic device was used to
by the Ashworth scale, and also to relate each of these impair- move the knee joint passively at three preset velocities through
ment measures to validated functional scales. We chose to the arc of motion in flexion and extension while resistance
employ an isokinetic device instead of other instrumented torque was measured and EMG data were also recorded to ver-
ify the state of muscle activation including the presence or
a absence of stretch responses. We hypothesized that the severity
of the Ashworth scores would be directly related to the magni-
150 tude and rate of change in resistance torque and to an earlier
angle of onset of the stretch response. We further projected
100 that both clinical and instrumented measures would be related
Angle

to functional severity in CP.


50

0
Method
PARTICIPANTS

50 0 A total of 31 individuals gave their consent to participate in


0 1 1 2 2 3
this study including 22 (11 males, 11 females) patients with
Time (s)
spastic CP and a comparison group of nine (four males, five
females) normally developing children. The mean age for
the children included here with CP was 11.9 years (SD 4.3 ) and
EMG

Table I: Original Ashworth scale

Score Description

0 No increase in tone
0 0 1 1 2 2 3 1 Slight increase in tone giving a catch when the limb is
Time (s) moved in flexion or extension
b 2 More marked increase in tone but limb easily flexed
3 Considerable increase in tone, passive movement difficult
150
4 Limb rigid in flexion or extension

100
Angle

50
Table II: Number of participants with CP per Gross Motor
0 Functional Classification System (GMFCS) level

GMFCS level Number of children


500 0 1 1 2 2 3
I 1
Time (s)
II 10
III 8
IV 0
V 3
EMG

Table III: Number of muscle groups with or without identified


stretch responses listed by Ashworth score
0 0 1 1 2 2 3
Time (s) Ashworth score (+) Stretch () Stretch

0 1 0
Figure 1: (a) absence and (b) presence of hamstring stretch 1 1 9
response. Top portion of each figure shows position 2 6 7
(uppermost lines) data from passive knee trials. Up-slope of 3 9 4
position graph = flexion; down-slope = extension. Lower 4 4 0
portion is EMG data for hamstrings which shows no activity 5 3 0
in (a), but in (b) a consistent and prolonged stretch response
that begins during extension is seen. Bold, result inconsistent with isokinetic/EMG assessment.

Precision of Ashworth Scale and Instrumented Measures Diane L Damiano et al. 113
for the comparison group of nine children without CP the passive motion (determined by EMG) in at least one direction
mean age was 11.3 years (SD 2.5). Participants were recruited was also eliminated from the study, as this would distort the
as part of a preoperative protocol for patients undergoing resistance torque calculations.
orthopaedic or neurosurgical procedures. Inclusion criteria
were: no major surgery within the past 6 months, the ability to PROCEDURES
fit anatomically on the isokinetic device, and the ability to Clinical and functional assessments
comply with instructions. Any participant who assisted the All individuals participated in a clinical assessment of spasticity

Table IV: Correlation of knee extensor (KE) and knee flexor (KF) Ashworth scores with
isokinetic parameters in participants with CP

Correlations /s n KE Ashworth (rho) KF Ashworth (rho)

Resistance torque 30 22 0.64 ns


Resistance torque 60 22 0.53 ns
Resistance torque 120 22 0.59 ns
Stiffness 30 22 0.58 ns
Stiffness 60 22 0.56 ns
Stiffness 120 22 0.73 0.56
Onset angle 30 10Q/14H 0.80 ns
Onset angle 60 10Q/14H ns ns
Onset angle 120 10Q/14H ns 0.58

Q, quadricep stretch response; H, hamstring stretch response.

a a
0.3
0.8
0.25
Resistance torque in ft-lbs/lbs

0.7
Comparison
Slope of torque by angle

0.6 Comparison 0.2


ASH1
0.5 ASH1 ASH2
ASH2 0.15
0.4 ASH3
ASH3
0.3 0.1 ASH4
ASH4
ASH5
0.2 ASH5
0.05
0.1
0
0

b b
0.24 0.5
Resistance torque in ft-lbs/lbs

0.2
Slope of torque by angle

0.4

0.16
0.3
0.12
0.2
0.08

0.04 0.1

0 0
Figure 3: Rate of change in resistance or slope of resistance
Figure 2: Resistance torque in ft-lbs/lbs plotted by Ashworth
torque by angle (TXA) curve plotted by Ashworth scores for
scores for (a) quadriceps during knee flexion and (b)
(a) quadriceps during knee flexion and (b) hamstrings
hamstrings during knee extension at 120/s.
during knee extension at 120/s.

114 Developmental Medicine & Child Neurology 2002, 44: 112118


including Ashworth score, Ely test (or Duncan-Ely; Gage 1992), resistance from the quadriceps during knee flexion and knee
and deep tendon reflexes. The Ashworth scale used was similar flexor Ashworth scores indicate resistance from the ham-
to the classic one (Ashworth 1964; see Table I) with the excep- strings during knee extension. Similarly, resistance torque
tion here that scores were shifted so that a 0 score indicated and stiffness in the quadriceps refers to isokinetic measure-
when resistance was less than normal. The Ely test is used to ments during passive knee flexion and during knee exten-
assess rectus spasticity during rapid passive knee flexion while sion for the hamstring values.
the patient is prone. For those in the CP group, knee joint Resistance joint torque was measured in ft-lb/lbs, the limb
range of motion, selective control of knee flexion and exten- weight was removed and the torque was normalized by body
sion, and the Gross Motor Function Measure (GMFM; Russell weight. Peak resistance torque was the measure of magni-
et al. 1989) were also assessed. The parent/caregiver accompa- tude. In addition, resistance torque was plotted against joint
nying the child or adolescent completed the Parent Baseline angle for the isokinetic part of the range and the slope of this
Form of the Pediatric Outcomes Data Collection Instrument line was computed and used as a measure of stiffness (see
(Daltroy 1998). Glossary in Appendix).
EMG data were used to identify the state of muscle activa-
Passive isokinetic and EMG assessments tion during the passive trials, i.e. whether the muscles were
Surface EMG electrodes (Noraxon USA Inc, Scottsdale, AZ, quiescent or whether a stretch response was consistently evi-
USA) were placed over the quadriceps and hamstrings mus- dent in the antagonist. Figure 1 illustrates the EMG response
cles. The child was seated on the isokinetic device (System 3 to passive knee motion for a child without a stretch response
Pro; Biodex Medical Systems, Shirley, NY, USA) in a semi- in either muscle (Fig. 1a) and a child with a stretch response
reclining position with the hip joint angle at 60 of flexion. in the hamstrings muscles during knee extension (Fig.1b).
The left leg was the tested leg, except for three patients with Participants were categorized by whether or not they demon-
right hemiplegia on whom the right leg was tested. Passive strated hamstrings or quadriceps stretch responses. Onset
isokinetic testing of the knee at 30, 60, and 120/s was per- angle was also recorded for each trial where a stretch response
formed. EMG and resistance torque data were collected was identified by finding the angle equivalent of the EMG
simultaneously at a sampling rate of 1200 Hz (Datapac 2000; onset. Changes in stiffness, peak resistance, and onset angle
RUN Technologies, Laguna Hills, CA, USA). with velocity (values from 120/s trials values from 30/s tri-
als) were also quantified to evaluate the velocity dependency
DATA ANALYSIS of each parameter.
For clarification, knee extensor Ashworth scores indicate Spearmans rho and Pearsons r procedures were used to
examine correlations between variable pairs.

Results
The group with CP included those with a diagnosis of spastic
diplegia, hemiplegia, or quadriplegia, with the distribution
a across Gross Motor Functional Classification Levels (Palisano
60 et al. 1997) shown in Table II.
No individual in the comparison group showed a stretch
50
response at any of the velocities tested. Of the 22 children with
40 ASH0 CP, 14 demonstrated stretch responses in the hamstrings, 10
ASH2 had stretch responses in the quadriceps, seven had these in
30
ASH3 both muscles, and five had these in neither muscle. We first
20 ASH5 examined the predictive value of the Ashworth scale in detect-
ing or failing to detect stretch responses compared with the
10
isokinetic examination (Table III). Of the 10 muscles assigned
0 a grade of 1 in either the knee flexor or extensor Ashworth

b
120
Table V: Spearmans correlation of knee extensor (KE)
100 Ashworth scores and functional measures in those with CP
80 ASH1
Correlations KE Ashworth (rho)
ASH2
60 ASH3
POSNA Global Function Scale 0.48
ASH4
40 ASH5 Upper Extremity 0.52
Transfers and Basic Mobility 0.61
20
Gross Motor Function Measure TOTAL 0.68
0 Lying and Rolling 0.63
Sitting 0.66
Figure 4: Onset angle in degrees of knee flexion plotted by Crawling and Kneeling 0.63
Ashworth scores for (a) quadriceps during knee flexion and Standing 0.58
(b) hamstrings during knee extension at 120/s. Walk, Run and Jump 0.57

Precision of Ashworth Scale and Instrumented Measures Diane L Damiano et al. 115
score, only one child was shown to have a stretch response in ed to passive knee extension (r=0.48 for Ashworth; r=0.51
the hamstrings during the isokinetic/EMG tests. That same to 0.59 for stiffness) indicating that greater resistance in the
child had been assigned 0 for the quadriceps Ashworth score, hamstrings is associated with more restricted muscle lengths.
yet had also demonstrated a stretch response in that muscle. Only three children with CP demonstrated increased knee jerk
Of the 13 muscles assigned an Ashworth score of 2, six had responses (greater than 3/5) on tendon tap. Each of those
identifiable stretch responses. Of the 13 muscles assigned children also demonstrated a stretch response during the
Ashworth scores of 3, nine had stretch responses. Finally, of knee extension isokinetic tests with a knee flexor Ashworth
the seven muscles assigned scores of 4 or 5, all seven had evi- score of 4 in two children and 3 in one child, despite the fact
dence of stretch responses on the isokinetic/EMG evaluation. that no correlation was found between tendon reflexes and
Ashworth scores. Isolated control of the hamstrings (graded
RESISTANCE TORQUE, STIFFNESS, AND ONSET ANGLE BY ASHWORTH from 0 for no control, 1 if they could initiate the movement
A clear gradient was apparent in the mean resistance (Figs 2a with the hip in extension or complete it while flexing the hip,
and b) and stiffness values (Figs 3a and b) as Ashworth scores and 2 if they could complete the movement without flexion
increased. Onset angle of the stretch response tended to at the hip) was inversely related to resistance torque in the
occur sooner in the motion in those with higher Ashworth quadriceps (rho=0.48), indicating that greater active con-
scores (Figs 4a and b). In all patients, the EMG response, trol in the hamstrings was associated with lower passive
once initiated, continued throughout the motion. resistance in the antagonist.

RELATIONS BETWEEN ASHWORTH SCORES AND QUANTITATIVE Discussion


MEASURES Lance (1981) described spasticity in a clinical sense as, the
Significant correlations tended to be in the weak to moderate sensation of resistance felt as one manipulates a joint
range with the quadriceps measurements showing typically through a range of motion, with the subject attempting to
higher and more consistent relations (see Table IV). relax (p 128). However, our investigation corroborated pre-
vious reports showing that increased resistance in CP can be
CORRELATION WITH FUNCTION from intrinsic stiffness, or altered muscle properties in the
Knee extensor Ashworth scores were significantly related to absence of EMG activity, from stretch responses that cause an
the functional scores (Table V) while knee flexor Ashworth involuntary muscle activation, or from both factors com-
scores were not. Instrumented measures for both muscle bined (Katz and Rymer 1989, Dietz and Berger 1995). Several
groups had significant relationships with the functional mea- of the children with CP showed no stretch responses in one
sures as shown in Tables VI and VII. However, the correla- or more of the muscle groups and no one in the control
tions with the hamstrings tended to be lower and/or more group showed a stretch response at either joint at any of the
sporadic than those seen for the quadriceps. An inverse cor- angular velocities tested. While stretch responses can be
relation between change in hamstring stiffness and the detected in normal muscles, the threshold velocity needed
Global Function Scale score was found (r=0.51) with a to elicit these is much greater than those employed here
greater change across velocity related to poorer ability. (Fellows et al. 1994). A protocol designed to increase the
angular velocity incrementally until a stretch response can
OTHER INTERIMPAIRMENT CORRELATIONS be elicited in all participants may more clearly differentiate
Knee extensor Ashworth scores and quadriceps stiffness at responses in CP versus non-CP muscles.
all three velocities were related to the Ely test (r=0.45 for It was apparent in this sample that the magnitude of resis-
Ashworth; r=0.67 to 0.77 for stiffness). The knee flexor tance in patients with identifiable stretch responses can
Ashworth score and hamstring stiffness were inversely relat- reach much higher levels, particularly at faster velocities,
than typically seen in those without stretch responses.

Table VI: Pearsons correlation of Gross Motor Function


Measure (GMFM) total and Global Function Scale Score Table VII: Pearsons correlation of Gross Motor Function
(GLOBAL) of Pediatrics Outcomes Data Collection Measure (GMFM) total and Global Function Scale Score
Instrument with instrumented passive motion tests for (GLOBAL) of Pediatrics Outcomes Data Collection
quadriceps muscle group Instrument with parameters from instrumented tests for
hamstrings muscle group
Correlation/s GMFM (r) GLOBAL (r)
Correlations/s GMFM (r) GLOBAL (r)
Resistance torque 30 0.58 0.45
Resistance torque 60 0.53 0.47 Resistance torque 30 ns ns
Resistance torque 120 ns ns Resistance torque 60 ns ns
Resistance torque 120 ns ns
Stiffness 30 0.76 0.54
Stiffness 30 0.60 ns
Stiffness 60 0.73 0.63 Stiffness 60 0.57 ns
Stiffness 120 0.70 ns Stiffness 120 0.52 ns
Onset angle 30 0.85 ns Onset angle 30 ns ns
Onset angle 60 ns ns Onset angle 60 ns ns
Onset angle 120 ns ns Onset angle 120 ns ns

ns, not statistically significant at p<0.05.

116 Developmental Medicine & Child Neurology 2002, 44: 112118


However, patients may exist in whom the magnitude of the such as restrictions in muscle length, and uncovering the
spastic response is very small or the magnitude of passive mechanism by which spasticity, a passive phenomenon, dis-
stiffness alone is fairly high. Patients assigned Ashworth rupts voluntary muscle activation (Damiano et al. 2001a,b)
scores in the mid-ranges of resistance yet who had passive and motor performance.
stiffness alone could be incorrectly judged to have mild to
moderate spasticity and, consequently, may be treated Conclusions
inappropriately. It is also possible that the degree of spastic- A standard rehabilitation device, an isokinetic dynamometer,
ity could be overestimated, even when present, which could can be used to quantify validly resistance torque during pas-
also adversely affect treatment outcomes. In the absence of sive joint motion. In this investigation, the instrumented
EMG verification, evaluating patients at different velocities measures tended to have stronger relationships with func-
may help to distinguish passive stiffness alone from reflex tion than the current clinical standard, the Ashworth scale.
stiffness (spasticity); however, the Ashworth scale is only Passive resistance to motion, as measured clinically and with
performed at a single velocity. Therefore, instrumented instrumentation, shows a consistent direct relationship with
devices or other clinical methods, such as the newly revised validated measures of function in CP.
Tardieu Scale (Boyd and Graham 1999) that gauge resis-
tance at several speeds may be more useful, especially in Accepted for publication 1st August 2001.
more equivocal cases. Acknowledgements
As Ashworth scores and isokinetic tests both measure This work was supported by funding from the National Institutes of
resistance to passive stretch, it is logical to assume that they Health (R29HD36516), United Cerebral Palsy Educational and
would be correlated. Stiffness, rather than the magnitude of Research Foundation, and Medtronics Neurological.
resistance, appeared to have higher, more consistent correla-
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Appendix

GLOSSARY OF TERMS
Spasticity. Consistent with the traditional physiologic
definition (Lance 1980), this is defined here as the presence
of a stretch response during passive muscle stretch at an
angular velocity of 120/s or less, as indicated by a consistent
EMG response in the muscle group being stretched.

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