A stiff-knee gait pattern is frequently associated with several impairments including quadriceps spasticity in children diagnosed with cerebral palsy (CP). The relationship of clinical measures of quadriceps spasticity and the stiff-knee gait pattern in children diagnosed with CP has not been well established. Therefore, the purpose of this study was to determine the ability of clinical measures of quadriceps spasticity (modified Ashworth scale [MAS], Ely tests, and pendulum test) to categorize a stiff-knee gait pattern in children with CP. Children were categorized as having a stiff-knee gait pattern based on kinematic and EMG gait data. Results of a logistic regression model revealed that the only significant measure was A1 of the pendulum test. Discriminant analysis functions were used to predict group membership (stiff-knee, not stiff-knee gait pattern) for each measure. The A1 of the pendulum test demonstrated the highest classification accuracy and the highest sensitivity compared to the other measures. Therefore, a negative pendulum test (indicated by an A1 value of 45 degrees or more) is more useful for ruling out a stiff-knee gait pattern compared to the other clinical measures.
The clinical presentation of cerebral palsy (CP) includes a broad spectrum of motor impairments of the neuromusculoskeletal systems such as joint contractures, decreased motor control, and muscle spasticity [
A review of clinical spasticity measures reported that most clinical scales (Modified Ashworth Scale and the Ely test) are subjective and their reliability and validity have not been thoroughly evaluated [
The pendulum test is an objective measure of quadriceps spasticity that has been reported in the literature for over 50 years [
If a patient demonstrates a certain gait pattern, then certain clinical measures are performed to determine the cause of the gait deviation. However, the expected relationships between clinical measures and gait pattern are not always present, causing some to question whether a passive measure of an impairment can relate to the dynamic functional activity of walking [
Procedures were approved by a local institutional review board and informed consent was obtained. Children previously diagnosed with spastic CP (diplegia or hemiplegia) and referred to our facility over a two-year period for clinical gait analysis were recruited for this prospective observational study (
Characteristics of subjects (
Cerebral palsy |
|
% |
---|---|---|
Diagnosis | ||
Spastic diplegia | 55 | 81 |
Right hemiplegia | 5 | 7 |
Left hemiplegia | 8 | 12 |
GMFCS level | ||
I | 29 | 43 |
II | 24 | 35 |
III | 14 | 21 |
IV | 1 | 1 |
Assistive device | ||
None | 53 | 78 |
Walker | 9 | 13 |
Loft strand crutches | 6 | 9 |
Data were collected in the same order for all children by one examiner. Kinematic and EMG data while walking were first collected using surface reflective markers and surface electrodes following the standard gait analysis protocol (Cleveland clinic marker set) [
The surface EMG and reflective markers were then removed and then a standard clinical examination was performed including three clinical tests of quadriceps spasticity. First, the MAS was performed using an ordinal scale (0, 1, 1.5, 2, 3, and 4) [
Next, the subject was placed in prone position. The Ely-S test (an assessment of quadriceps spasticity) was recorded as the presence/absence of resistance experienced by the examiner when performing prone knee flexion rapidly [
A subject’s gait pattern was classified as stiff-knee if at least 4 out of 6 previously reported criteria of kinematic and electromyographic data were present [
Statistical analyses were conducted using SPSS, V22.0. (Chicago, IL). In order to compare categorical and continuous clinical measures from those with and without stiff-knee gait, chi-square and two sample
Thirty-one of the 68 (46%) children were classified positive for a stiff-knee gait pattern. Table
Dependent and independent measures (
Measures | Stiff-knee |
Not-stiff-knee |
---|---|---|
Criteria of knee gait pattern | ||
Knee flexion angular velocity at toe-off (degrees/sec), mean (SD) | 120 (80) |
263 (95) |
Time to maximum knee flexion in swing (percent of swing phase), mean (SD) | 55 (18) |
43 (11) |
Maximum swing phase knee flexion (degrees), mean (SD) | 56 (13) | 60 (6) |
Total knee motion (degrees), mean (SD) | 38 (14) |
50 (13) |
Inappropriate quadriceps EMG activity, |
25 (81) | 24 (65) |
Toe drag, |
11 (36) | 1 (3) |
Pendulum test | ||
A1 [max knee angle − start knee angle = amount of knee flexion |
34 (15) |
57 (23) |
Modified Ashworth Score |
||
0 | 16 (52) |
32 (87) |
1 | 10 (32) | 5 (13) |
1.5 | 3 (10) | |
2 | 2 (6) | |
Ely-S (quadriceps spasticity) |
||
Yes | 12 (39) |
29 (78) |
No | 19 (61) |
8 (22) |
Ely-F (quadriceps flexibility) |
||
90 degrees or less | 23 (74) | 15 (40) |
Greater than 90 degrees | 8 (26) | 22 (60) |
All dependent and predictor measures were normally distributed (skewness < ±2). None of the 68 subjects demonstrated significant multiple measure outliers. Logistic regression model was significant (chi-square 23 with 4 degrees of freedom
Logistic regression model.
Measures |
|
SE | Wald | df | Sig. |
|
95% CI for |
|
---|---|---|---|---|---|---|---|---|
MAS |
0.816 | 0.624 | 1.711 | 1 | 0.191 | 2.261 | 0.666 | 7.674 |
Ely-S test |
|
0.734 | 0.134 | 1 | 0.715 | 0.765 | 0.181 | 3.223 |
Ely-F test |
|
0.020 | 0.011 | 1 | 0.915 | 0.998 | 0.960 | 1.037 |
A1 (knee flexion during first swing of pendulum test) |
|
0.022 | 4.952 | 1 | 0.026 | 0.952 | 0.911 | 0.994 |
Constant |
|
1.718 | 1.422 | 1 | 0.233 | 7.758 |
Sensitivity, specificity, and positive and negative likelihood ratios for clinical measures of spasticity (
Spasticity measure | Overall accuracy | Sensitivity |
Specificity |
Positive likelihood ratio |
Negative likelihood ratio |
---|---|---|---|---|---|
A1 of pendulum test | 77% | 0.87 |
0.68 |
2.69 |
0.19 |
|
|||||
MAS | 69% | 0.48 |
0.87 |
3.59 |
0.60 |
|
|||||
Ely-F | 62% | 0.52 |
0.70 |
1.74 |
0.69 |
|
|||||
Ely-S | 71% | 0.61 |
0.78 |
2.84 |
0.50 |
The impetus for this study came from interest in better understanding the relationship between measures of quadriceps spasticity and the stiff-knee gait pattern of children diagnosed with CP. Because quadriceps spasticity has been proposed as one cause of the stiff-knee gait pattern in children diagnosed with CP the purpose of this study was to assess the ability of measures (MAS, Ely tests, and pendulum test) to correctly categorize a stiff-knee gait pattern. Logistic regression analysis revealed that only the A1 of the pendulum test was a significant measure for correctly categorizing the children’s gait pattern as stiff-knee or not. For each one-degree increase in the A1 the odds are decreased by 5% that the child will have a stiff-knee gait.
The regression analysis identified those clinical measures most related to the target problem (stiff-knee gait pattern). From the regression analysis, the greatest amount of variance of the knee gait patterns was explained by the A1 measure of the pendulum test. However, from a clinical perspective, this information is not very applicable. Clinically, it is more important to know the discriminant ability of a test, or how well a test can identify the target problem. Therefore, discriminant analysis was performed to assess the ability of the clinical measure to correctly identify stiff-knee gait pattern. The A1 measure demonstrated a higher overall accuracy to correctly classify the original groups as having a stiff- or not-stiff-knee gait pattern 77% compared to the other measures (MAS 69%, Ely-F 62%, and Ely-S 71%) (Table
However, the overall accuracy of a test does not provide information regarding false positive and the false negative rate of a test [
A limitation of sensitivity and specificity is that one has to know if the target problem is truly present to calculate the sensitivity or specificity of a test. Sensitivity and specificity only indicate the probability of a correct test result (true positive, false positive, false negative, and true negative) [
By multiplying the pretest probability of a target problem by the likelihood ratio gives the posttests odds of the target problem [
Two possible explanations exist for the A1 measure of the pendulum test being the only significant measure in the logistic regression. First, four of the six criteria of a stiff-knee gait pattern and the A1 measure of the pendulum test are all measures of knee displacement. Second, the methodological difference between subjective clinical measures (Ely-F, Ely-S, and MAS) and the objective pendulum test are significant. During the pendulum test, a constant force (gravity) is applied and the knee motions are objectively measured by the motion analysis system. In contrast, the MAS and Ely-S test are subjective assessment performed at inconsistent knee flexion velocities. Therefore, the combination of a consistent application of force with a quantitative measurement of knee displacement motion, instead of subjective assessments, resulted in the pendulum test being the only significant measure to identify stiff-knee gait patterns.
Previous studies using the pendulum test and EMG data have only presented a visual example of EMG data [
A limitation of this study is that ten of the children had previously undergone spasticity reducing interventions (rhizotomy or baclofen pump). Due to the small sample size no detailed analyses were performed on this subset of children. However, consistent with previous study results [
Because the logistic regression model explained 29–39% of the variance of the gait patterns, there are other factors not accounted for by the model contributing to the stiff-knee gait pattern. Previous studies using computer modeling of children diagnosed with CP reported that the knee flexion velocity at toe-off had a larger influence on knee range of motion in swing than hip flexion velocity, knee angle, and hip angle at early swing phase [
Presently the pendulum test requires the use of biomechanical instrumentation techniques (electronic goniometer or three-dimensional motion analysis system) to quantitatively measure the knee motion. Therefore, some clinicians may believe that the pendulum test is not a clinically useful tool. We acknowledge that this is a limitation of the pendulum test. However, a video camera or smart phone could record the knee motion during the pendulum test and then it could be played back and paused to estimate the value of A1. Therefore, future studies to assess the accuracy of visual analysis of the pendulum test are needed.
The purpose of this study was to assess the relationship of the different measures of quadriceps spasticity (MAS, Ely, and pendulum test) in the presence of a stiff-knee gait pattern, measured using motion analysis laboratory. Logistic regression analysis revealed that only the A1 of the pendulum test was a significant measure for correctly categorizing the children’s gait pattern as stiff-knee or not. The A1 measure demonstrated a moderate negative likelihood ratio of 0.19. Hypothetically, if a clinician was 50% confident a child has a stiff-knee gait pattern. Multiplying the pretest probability of a target problem by the likelihood ratio gives the posttests odds of the target problem. Therefore, a negative pendulum test (as evident by an A1 greater than or equal to 45 degrees) decreases the pretest probability from 50% to the posttest probability of 10% that the child has a stiff-knee gait pattern. By implementing the pendulum test clinicians can objectively and reliably identify if quadriceps spasticity is absent. If spasticity of the quadriceps is not present, as evident by 45 degrees or more of knee flexion during the first swing of the pendulum test, then other body structures or impairments (decrease force generation of the hip flexors and ankle plantar flexors) should be assessed for the cause of the stiff-knee gait pattern in a subject diagnosed with CP.
A subject’s gait pattern was classified using the characteristics listed below. A participant gait could be rated from 0 (no characteristics present) to 6 (all characteristics present) for a stiff-knee gait pattern. For example, if a subject had any 4 characteristics present, then they would be rated as 4. A delay in timing of maximum knee flexion in swing phase defined as two or more standard deviations above the normal value (as a percent of the swing phase of the gait cycle) [ Two or more standard deviations below the average normal value of maximum knee flexion occurring during swing phase [ Two or more standard deviations below the average normal value of total sagittal plane knee motion occurring throughout the gait cycle [ Two or more standard deviations below the average normal value of knee angular velocity at toe-off [ Impaired foot clearance considered present if the toe/foot was noted to drag on the ground (based on visual observation of “toe drag” during walking trials) during the swing phase of the gait cycle [ Inappropriate quadriceps activity was present if the dynamic EMG activity during the swing phase of the gait cycle was two or more standard deviations above the minimum activity during the stance phase of the gait cycle [
Tim L. Uhl and Sam Augsburger are coauthors.
Funding for this project was provided by Kosair Charities of Louisville, KY. However, the authors have no potential for material gain as a result of this study.
The authors would like to thank the children and their families for their participation in this study. The authors would also like to thank Bobbie Edester for her assistance in collecting the data for this study.