| | Deficits in Upper-Limb Task Performance in Children With Hemiplegic Cerebral Palsy as Defined by 3-Dimensional KinematicsPresented in part to the Gait and Clinical Movement Analysis Society, April 2005, Portland, OR. Abstract Mackey AH, Walt SE, Stott NS. Deficits in upper-limb task performance in children with hemiplegic cerebral palsy as defined by 3-dimensional kinematics. ObjectiveTo define upper-limb movement deficits in children with hemiplegia using 3-dimensional (3-D) kinematic analysis of functional tasks. SettingUniversity gait laboratory. ParticipantsTen children with hemiplegic cerebral palsy (mean age, 13.3y; range, 10–17y) and 10 control children (mean age, 9.8y; range, 6–12y). InterventionsNot applicable. Main Outcome Measure3-D upper-limb movement analysis. Results3-D kinematics detected clinically significant between-group differences. Children with hemiplegia were significantly slower than control children in time taken to complete tasks (P<.05) and achieved slower movement velocities (P<.05). Group differences in range of motion (ROM) occurred in all 3 tasks examined (hand to mouth, hand to head, reach). Children with hemiplegia had significantly less supination (P<.03) and shoulder flexion (P<.03) and increased compensatory trunk flexion (P<.01) compared with control data (hand-to-mouth task). The reach task highlighted restriction of elbow extension in children with hemiplegia (minimum elbow extension: hemiplegia, 24±18°; control, 3±7°). Completing tasks bilaterally did not alter performance of the tasks in children with hemiplegia. Conclusions3-D kinematics detected deficits in timing, ROM, and proximal compensatory strategies during upper-limb functional task performance in children with hemiplegia.
CEREBRAL PALSY (CP) IS PRIMARILY a disorder of movement and posture, presenting with upper motoneuron signs and symptoms, including spasticity, muscle hypertonia, hyperreflexia, muscle weakness, and loss of selective motor control.1, 2 The functional consequences are varied and can potentially affect all activities of daily living (ADLs). About 30% of children with CP have hemiplegia with weakness and spasticity predominantly affecting 1 side of the body, including the arm, leg, and trunk musculature.3 Most children with hemiplegia are independent in both walking and most ADLs.4, 5 However, children with hemiplegia can have difficulties performing gross and fine motor hand activities, in addition to abnormal posturing of the upper limb during gait or other activities requiring effort.6, 7, 8, 9, 10 The combination of spasticity, dystonia, weakness, and sensory and motor control deficits are thought to contribute to the reduced functional abilities of the upper limb in children with hemiplegia. These movement deficits in the upper limb can result in children becoming “1-handed experts,” with their hemiplegic upper limb acting only as a stabilizing or helper hand when completing everyday activities.
Interventions for children with CP that address these deficits in the upper limb have traditionally included therapy and splinting, surgery, and more recently the use of botulinum toxin type A (BTX-A) injections.7, 11, 12 A number of the clinical interventions are specifically targeted at reducing spasticity or improving range of motion (ROM) to improve upper-limb function. However, to date there is limited evidence that show short- or long-term functional changes after any intervention for the upper limb in children with CP.13
One of the difficulties in assessing the outcomes of intervention in the upper limb is the lack of reliable and objective outcome measures. Many measures rely on subjective assessments of performance made by parents, child, or therapist (eg, goal attainment scale).14 Two upper-limb functional assessments for children with CP that have acceptable reliability, the Melbourne Assessment of Unilateral Upper Limb Function (Melbourne Assessment)15 and Quality of Upper Extremity Skills Test,16 both rely on visual assessment of the movement. This type of assessment in the lower limb has been shown to have only moderate validity (eg, Observational Gait Scale).17 Thus, in the lower limb, 3-dimensional (3-D) gait analysis is the criterion standard for assessing changes in performance after interventions such as surgery, BTX-A injections, and dorsal rhizotomy.18, 19 However, 3-D upper-limb kinematics are not routinely used for clinical populations because of lack of commercial software and perceived technical difficulties in establishing a representative mathematical model and in defining a repeatable task and movement of interest. The technical limitations to 3-D upper-limb movement analysis include accurately representing the large degrees of freedom at the shoulder complex with the use of external markers and addressing the potential motion errors that may arise from skin movement that occurs during forearm motion and scapular motion in particular.20 However, the potential benefits that may be obtained from an objective upper-limb measure for different patient populations mean that the proposed technical difficulties warrant further investigation.
We have previously described a 3-D upper-limb kinematic model that has shown moderate to high levels of repeatability in children with hemiplegic CP when performing standardized upper-limb tasks21 and has shown a strong association with static goniometric measures.22 However, sensitivity to differences across different patient populations is also an important requirement of any measure before it can be used as an outcome measure. The aim of this study was to test the sensitivity of the 3-D kinematic measure of upper-limb functional activities to quantify differences in performance of simple arm movements between a normative pediatric population and children with hemiplegic CP.
Methods  Participants The study participants consisted of 10 children with no history of musculoskeletal or neurologic problems, representing a normative pediatric population (2 boys, 8 girls; mean age, 9.8y; range, 6−12y) and 10 children with a diagnosis of hemiplegic CP (7 boys, 3 girls; mean age, 13.3y; range, 10−17y). Within this group, 6 of the children had a right hemiplegia and 4 had a left hemiplegia. Specific selection criteria were used as the children with CP were recruited as part of a separate intervention-based study, with data for this current study collected before the intervention. The children were required to have a diagnosis of hemiplegic CP; age range from 8 to 17 years; independent ambulation, with or without orthoses (Gross Motor Functional Classification23 level I or II); and increased muscle tone in the hemiplegic upper limb (minimum Ashworth Scale24 score 1). Subjects were excluded if they had other types of CP or neurologic disorder, if they had elbow joint contractures in the affected upper limb of more than 20°, or if they had had serial casting, BTX-A injections, or surgery in the affected upper or lower limb in the previous 12 months. This study had ethical approval from the local ethics committee, and all 20 participants and their guardians gave informed consent to participate in the study. 3-D Upper-Limb Kinematic Analysis To complete a 3-D kinematic analysis of upper-limb movement, 21 retroreflective markers were placed on each child’s trunk and upper limbs (fig 1). This upper-limb marker set was the same as that previously described to evaluate the repeatability of 3-D upper-limb kinematics in children with hemiplegia,21 apart from the use of a single marker to estimate the shoulder joint center, which replaced the 2 markers previously used. An additional marker was also placed on each hand to allow for determination of a wrist segment. (For the purpose of this study, wrist segment motion is not reported.) A total of 9 body segments were defined: right and left trunk, right and left upper arm, right and left forearm, right and left wrist, and pelvis (appendix 1). Each segment was assumed to be a rigid body defined by 3 markers, generally representing proximal and distal ends of the segment plus a third noncollinear marker to allow for rotational orientation.25 A joint coordinate system was implemented to describe the relative angles between segments.26, 27 Upper-limb joint centers at the elbow, wrist, and neck were defined by a virtual marker calculated from offsets of 2 external marker positions.21, 28, 29 In accordance with other 3-D upper-limb models described in the literature, assumptions were made for the assessment of shoulder movement, with both scapulothoracic and acromioclavicular motions being discounted.28, 29, 30 The shoulder joint was therefore assumed to have only 3 degrees of freedom. The shoulder joint center virtual marker was estimated from a single external marker placed on the superior aspect of the acromion and was individually calculated as a 10% offset (of arm length) in the inferior direction (offset range, 3−6cm for 10 subjects). Testing Procedures All testing was completed at the University of Auckland Gait Laboratory. Three upper-limb functional tasks were examined: hand-to-head task, hand-to-mouth task, and reach task. The tasks were considered to represent everyday functional activities, with similar tasks having been described in previous studies examining upper-limb movement.29, 31, 32 Additionally, the tasks corresponded to activities (items 2, 11, 16) described in the Melbourne Assessment,15 a frequently used clinical measure of arm function. Each child was seated on an adjustable stool with a table positioned in front of him/her. The starting position for each of the 3 tasks required children to place the hand on the table surface directly in front of them with elbow flexed to approximately 90° and the forearm in slight pronation. The hand-to-head task involved taking the hand from the table to touch the forehead with the palm of the hand (fig 2). The hand-to-mouth task involved reaching forward to pick up a 4-cm cube positioned on the table at 1 arm’s length distance away and bring it to the mouth, as has been previously described by Schneiberg et al31 (fig 3). This distance was measured individually for each subject (using the affected arm for children with hemiplegia) from the axilla to the wrist crease. Pretesting assessment of inclusion criteria confirmed that no child had an elbow flexion contracture of greater than 10°. The reach task involved leaning forward and extending the elbow to touch a stationary object at shoulder height and then returning the hand to the starting position (fig 4). This distance was measured individually for each child (using the affected arm for children with hemiplegia) from the axilla to the tip of the middle finger. The position of the table was moved for each child to achieve this set measured distance and allow standardization in reaching distance. For the unilateral condition, all tasks were completed separately by both the hemiplegic (affected) and unaffected arms, and then 2 of the tasks (hand to mouth, reach) were completed bilaterally to examine the effect that the unaffected hand has on the performance of the hemiplegic hand. Control children completed the same tasks with their dominant and nondominant hands. Each of the upper-limb tasks was completed by the child 3 times in the measurement session, in random order, at a self-selected speed. Data and Statistical Analysis Data were collected with an 8-camera Motion Analysis video systema at 60Hz. Kinematic information was collected and processed using EvA software version 3.12a and additional biomechanic analysis was completed using KinTrak software version 6.a As children completed each task at a self-selected speed, the movements were visually edited in the data collection software (EvA software version 3.12) to represent the start and end points of the movement. A mean kinematic trace was determined for each upper-limb task and used to calculate the ROM and velocity data for all subjects. The minimum and maximum joint angles were obtained for trunk, shoulder, and elbow motion across the 3 planes of movement for each upper-limb task. This allowed us to calculate a meaningful statistical comparison from the kinematic waveform data generated during analysis. These specific joint angles were used to best represent relevant time periods of the task. For example, during the reach task the minimum shoulder joint angle approximates the shoulder starting position and the maximum shoulder joint angle approximates the point at which the object is touched by the hand. Figures 2 through 4 show examples of points where the joint angle measurements (in degrees) were taken. The angle definition used for elbow rotation measures defined the full supination and full pronation position as 90° (pronation or supination), with midforearm position equivalent to 0°. Velocity (in deg/s) and time to peak velocity (in seconds) was determined from position and time data from the shoulder and elbow movement out toward the object during the hand-to-mouth and reach tasks. Statistical analyses were completed using analysis of variance and post hoc tests for group and arm comparisons of ROM, timing, and velocity data. Paired t tests were used to make dominant and nondominant arm comparisons for control children and dominant arm and unaffected arm comparisons between the control and hemiplegic groups. Statistical significance was set at P less than .05. Results Data were collected for both dominant and nondominant arms for the control group and for the affected and unaffected arm in the group with hemiplegia. When the 3 unilateral tasks were analyzed, no statistical differences in ROM, timing, or peak angular velocity were found between (1) the nondominant and dominant arms in the control group and (2) the dominant arm of control children compared with the unaffected arm of children with hemiplegia. Thus, the data for the nondominant arm of the control group are reported as the comparison for the data obtained with the hemiplegic (affected) arm in the hemiplegic group. 3-D Kinematic Measures of Joint ROM Used During Upper-Limb Tasks For each upper-limb task the relevant minimum and maximum ROMs were determined for trunk, shoulder, and elbow motion across the 3 planes of movement. Table 1 summarizes the kinematic data for the 3 tasks for both the normative pediatric population and the children with hemiplegia. The ROMs for the bilateral conditions of the hand-to-mouth and reach tasks are shown in Table 2, Table 3. The hand-to-head task tested the ability of each subject to touch the forehead with the palm of the hand. The control group used an arc of flexion at the shoulder averaging 79°±10° (starting at 26°±11° of shoulder flexion and flexing to 105°±10°) and an arc of flexion at the elbow averaging 58°±22° (starting at 108°±22° and flexing to 166°±8°). In the frontal plane, the control group used an arc of shoulder abduction of 22°±10° (range, 27°±10° to 49°±15°). Children with hemiplegia used a similar degree of sagittal and frontal plane motion at the shoulder and elbow to complete this task. Children with hemiplegia had variable abilities to supinate the forearm and overall achieved significantly less supination (hemiplegic, 49°±39° of supination; control, 77°±22° of supination) (P<.04). Greater trunk forward flexion was also seen in the children with CP (hemiplegic, 43°±14°; control, 29°±16°) (P=.02). The hand-to-mouth task required each child to reach forward to pick up a cube positioned on the table and bring the object to his/her mouth. An initial movement of elbow extension and shoulder flexion was required to reach the object, which was at the distance of 1 arm’s length, followed by combined elbow and shoulder flexion, with forearm supination to bring the object to the mouth. To complete this task, control children used an arc of shoulder flexion of 48°±13° (range, 23°±14° to 70°±10°) and achieved near-full forearm supination to bring their hands to their mouths (79°±9° of supination). Children with hemiplegia showed a significant increase in the arc of shoulder flexion used (66°±21°) (P<.03), flexing the shoulder more at the time the object was at the mouth. Associated with this increased shoulder flexion was significantly less supination in the children with hemiplegia (53°±18° of supination) (P<.03). Forward flexion of the trunk toward the hand was also significantly greater for children with hemiplegia during the hand-to-mouth task (control: maximum trunk flexion, 28°±15°; hemiplegia: maximum trunk flexion, 42°±13°) (P<.01). Bilateral performance of the hand-to-mouth task did not change the ROM used by the hemiplegic limb, when compared with the unilateral conditions (see table 2). For the reach task, children used elbow extension to reach toward and touch a stationary object at shoulder height, followed by elbow flexion when bringing the hand back to the starting position. Children in the control group achieved near-full elbow extension (3°±7°) when completing this task. Children with hemiplegia achieved significantly less elbow extension with the hemiplegic limb, with a range of elbow extension of 24°±18° (P<.01). There were no differences in shoulder motion between the 2 groups. There was a trend for subjects with hemiplegia to use more forward trunk lean—an average of 30°±14° (from an initial 8°±13° to 39°±13°)—than control subjects, who used on average 22°±10° (moving from an initial 12°±17° to 34°±12°), although this was not significant (P>.05). Bilateral performance of the reach task did not change the ROM used by the hemiplegic limb when compared with the unilateral performance of the task (see table 3). The lack of elbow extension in children with CP found during the unilateral task did not change during the bilateral condition (fig 5). Instead, in the bilateral performance of the task, some of the children with CP did not use the full elbow extension available in the unaffected limb, so the unaffected limb movement tended to match the affected limb movement. Time Taken to Complete Upper-Limb Tasks Table 4 shows the mean time (in seconds) taken to complete each of the upper-limb tasks for the 10 control children and 10 children with hemiplegia. The time taken for the control children to complete the unilateral tasks ranged from 2.4 to 3.4 seconds, with minimal variation between subjects (standard deviation [SD], 0.6−0.7s). The corresponding time taken to complete the tasks was significantly slower for the children with hemiplegia (range, 4.2−7.0s), with increased between-subject variability (SD, 1.3−2.1s) (hand to head, P<.05; hand to mouth, P<.05; reach, P<.05). A similar pattern was found for the bilateral performance of hand-to-mouth and reach tasks. Control subjects completed the reach task significantly faster than the children with CP, taking an average of 2.7±0.6 seconds (range, 1.9−3.5s), whereas subjects with CP took almost twice as long, with a mean time of 3.9±0.7 seconds (range, 2.9−5.1s) (P<.05). Children with CP also took nearly 2 seconds longer to complete the hand-to-mouth task compared with control children (children with hemiplegia: mean, 5.5±1.6s; range, 3.3–8.0s; control children: mean, 3.4±0.8s; range, 2.3−4.5s; P<.05). There was no significant difference between the time taken to complete the unilateral tasks and the time taken to complete the bilateral tasks in either control subjects or in children with hemiplegia (P>.05). However, the trend was for children with hemiplegia to be faster when they completed the hand-to-mouth tasks bilaterally compared with the unilaterally (hand-to-mouth: 5.5s bilateral, 7.0s unilateral). Peak Velocity and Time to Peak Velocity During Upper-Limb Functional Tasks Peak angular velocity (in deg/s) and time to reach peak velocity (in seconds) were calculated from the time and displacement data for shoulder forward flexion and elbow extension during the first movement of reaching out toward the object in the hand-to-mouth and reach tasks (unilateral and bilateral conditions). Table 5 shows the peak velocities and time to achieve peak velocities for control children and children with hemiplegia for unilateral and bilateral tasks. During the unilateral hand-to-mouth task, control subjects showed a trend of faster peak velocities and quicker time to peak velocity at the elbow than children with hemiplegia (P=.08). There was no difference found between unilateral and bilateral conditions in peak velocities and the mean time to reach peak velocity in both control subjects and children with hemiplegia (P=0.6). During the reach task, control subjects had significantly faster peak velocities at the elbow than children with hemiplegia in both unilateral and bilateral conditions (P<.05). There was no difference in the peak velocities achieved by children with hemiplegia in the unilateral condition compared with the bilateral condition (P=0.9). Discussion In this study, we were interested in the ability of 3-D kinematic analysis to detect differences in ROM and overall movement patterns at the trunk, shoulder, and elbow between the normative pediatric population and children with CP in the performance of simple upper-limb functional tasks. We found that 3-D upper-limb kinematic analysis was able to detect differences in the arc of motion between the affected and unaffected arms of children with hemiplegia. Significant differences were also found between the affected arm motion of children with hemiplegia and the dominant and nondominant arm motion of normative subjects. Children with hemiplegia had reduced elbow extension and supination, with a compensatory increase in trunk flexion, when completing reaching and grasping tasks with their affected hands. More striking than the reduced movement were problems with the speed of movement in the hemiplegic upper limb, evidenced by longer task duration, slower peak angular velocities, and a trend toward slower time to reach peak angular velocity. Several studies have examined different aspects of motor control of upper-limb movements in children with CP and have identified deficits in movement time and manual asymmetries during upper-limb functional tasks in hemiplegic subjects.9, 10, 31, 33, 34, 35, 36 However, these previous studies did not use 3-D kinematic analysis to define joint movement during the tasks. We found that 3-D kinematic analysis was able to detect the significant changes in the ROM used by children with hemiplegia to complete simple upper-limb functional tasks and also that it identified resulting compensatory movement strategies. Children with hemiplegia had reduced elbow extension during the reach task and achieved less forearm supination than control children when completing the hand-to-mouth and hand-to-head tasks. Compensatory movements were also found in completing the hand-to-mouth task, where children with hemiplegia had increased shoulder flexion and forward trunk flexion compared with the control population. The hand-to-mouth task was a more complicated task requiring increased accuracy in bringing the object to the mouth, as shown by the longer performance time for children with hemiplegia compared with controls in both the unilateral and bilateral conditions (see table 4). The increased shoulder and trunk motion in children with hemiplegia during the task may have indicated proximal compensation for lack of distal movements, such as forearm supination, and difficulties with grasp. Alternatively the additional proximal movements may be due to an inability to selectively isolate specific movements resulting in a mass flexion activity. In addition to the differences in the ROMs used between the groups, 3-D analysis clearly identified marked asymmetries in the speed of movement. Distal motor control deficits, particularly in the ability to grasp and release an object, can contribute to observed manual asymmetries.35, 37 However, in this study, even the reach and hand-to-head tasks, which did not involve the need to pick up objects, were performed significantly more slowly by the hemiplegic group than by the control group. Thus, it seems unlikely that a difference in distal hand motor control is the only contributing factor in the marked asymmetries in speed of movement. Other possible causes of these deficits include a combination of muscle weakness and fatigue together with inappropriate muscle co-contraction and a lack of ability to generate sufficient muscle force.38 Additionally, it may be that subjects with hemiplegia may have to slow down the movement to ensure acceptable accuracy and reduction in variability.37 The use of bilateral movements has recently been suggested as a treatment intervention for adults with hemiplegic stroke in an attempt to improve the performance of the hemiplegic limb to mimic the unaffected limb.39, 40, 41 Interestingly, some studies35 have found that during bilateral tasks the unaffected limb can instead slow down to complete the movement at the speed of the hemiplegic limb, suggesting more adaptability in the unaffected limb. In the current study, completion of the same tasks bilaterally did not lead to significant improvements in ROM, timing, or speed of movement in children with hemiplegia. There was a trend for children with hemiplegia to increase the peak velocity in elbow extension and reduce the total time to complete the task when performing the hand-to-mouth task bilaterally, but the movements were still slower than those of control subjects. A review of sagittal plane video taken during data collection indicated that the changes in speed and timing of the bilateral condition may have occurred because the unaffected hand was primarily used to pick up the object, thus speeding up this part of the task. The preliminary data obtained from this study suggest that further investigation is required into bilateral movement in children with hemiplegia—in particular, whether repetitive training of bilateral hand movements can ultimately lead to improvements in unilateral function. There are limitations to the use of a 3-D kinematic upper-limb analysis that need to be considered when interpreting our results. The assumptions made at the shoulder joint, in disregarding scapulothoracic movement, mean the model does not fully represent anatomically correct shoulder motion. The estimated joint centers determined from an external marker offset may also be a source of systematic error because of the lack of availability of precise joint center offsets for pediatric subjects and also skin movement underlying the external markers. It is also important to realize that a 3-D kinematic assessment of movement should be just 1 part contributing to overall assessment after any intervention. Additional measures, such as quality-of-life questionnaires or sensory testing, should also be included to ensure that all aspects of function are considered. The International Classification of Functioning, Disability and Health framework42 allows clinicians to consider a person’s health status, not only in terms of impairment, but more importantly on the level of activity and participation limitations. Joint kinematics are still a measure of a person’s impairment, although assessment of specific upper-limb tasks may make this a more relevant activity measure. However, further work needs to be done to link the movement deficits identified in this study to everyday functional limitations experienced by children with hemiplegia. Clinical Implications Movement analyses of upper-limb functional tasks can provide valuable information on several aspects of motor control that could potentially assist in assessing rehabilitation strategies for children with CP. This study confirms that 3-D assessment of upper-limb functional tasks can be completed successfully in both normative pediatric populations and those with CP and that it can detect differences in clinically relevant measurement parameters. These findings suggest that 3-D kinematics can contribute valuable objective information to an overall clinical assessment of arm function and assess whether interventions that alter tone and ROM in the hemiplegic limb, such as BTX-A injections, therapy, and splinting, can favorably alter patterns of movements in the upper limb. Conclusions In future studies upper-limb kinematic analysis could also be used to evaluate functional changes after interventions for children with CP such as constraint-induced therapy and/or bilateral movement programs, as have recently been described for adult stroke populations.41 Supplier
Acknowledgments We acknowledge the assistance of Craig Sutherland and Anna-Marie Ruhe from Department of Sport and Exercise Science, University of Auckland, during data collection. References 1.
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a Department of Surgery, University of Auckland, Auckland, New Zealand. b Department of Sport and Exercise Science, University of Auckland, Auckland, New Zealand.  Reprint requests to Anna H. Mackey, PhD, Dept of Surgery, University of Auckland, Private Bag 92019, Auckland, New Zealand
Supported by the Decade of Bone and Joint and the Neurological Foundation, New Zealand. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. PII: S0003-9993(05)01338-9 doi:10.1016/j.apmr.2005.10.023 © 2006 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
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