(Stroke. 2001;32:1875.)
© 2001 American Heart Association, Inc.
Original Contributions |
From the School of Rehabilitation, University of Montreal and Research Centre, Rehabilitation Institute of Montréal, Quebec, Canada (S.M.M., A.L., M.F.L.); and CNRS EP 1848 and Hôpital Raymond-Poincaré, Garches, France (A.R.-B.).
Correspondence to Mindy F. Levin, PhD, Research Centre of Rehabilitation Institute of Montreal, CRIR, 6300 Darlington, Montreal, Quebec H3S 2J4, Canada. E-mail levinm{at}poste.umontreal.ca
| Abstract |
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Methods Eleven healthy and 11 hemiparetic individuals participated. Three-dimensional kinematic analysis was used to quantify reaches made to a close and a distant target (near the limit of arms length). Unrestrained reaches were compared with those in which shoulder girdle and trunk movements were restrained by a harness.
Results During unrestrained reaching, abnormal trunk recruitment and limitations in elbow and shoulder movements were correlated with the degree of clinical stroke severity (r=-0.91 to -0.96) in hemiparetic patients. During trunk restraint, ranges of elbow and shoulder joint movement increased in both groups. In addition, elbow and shoulder interjoint coordination improved. This was caused by increases in the range of joint motion as well as by a better dynamic temporal relation between joints.
Conclusions Trunk restraint allowed patients with hemiparetic stroke to make use of arm joint ranges that are present but not normally recruited during unrestrained arm-reaching tasks. Thus, the underlying "normal" patterns of movement coordination may not be entirely lost after stroke. Appropriate treatments, such as trunk restraint, may be effective in uncovering latent movement patterns to maximize arm recovery in hemiparetic patients.
Key Words: arm hemiplegia motor control recovery therapy
| Introduction |
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Previous studies in hemiparetic patients have described excessive trunk or shoulder girdle movement in pointing2 and in reach-to-grasp movements1 for targets placed close to the body. Levin and colleagues5 have suggested that this increased recruitment is a compensatory mechanism by which the central nervous system may extend the reach of the arm when the control of the active range of arm joints is limited. Other studies have reported that elbow-shoulder interjoint coordination is disrupted in hemiparetic patients.68 In contrast to healthy individuals, reaching in hemiparetic patients is characterized by a lack of smoothness, as evidenced by both temporal and spatial segmentation.7
Therapists may approach the rehabilitation of reaching in several ways. For example, one assumption underlying traditional reflex-based neurofacilitation approaches is that the acquisition of trunk and shoulder girdle stability must precede the retraining of arm movement.9,10 Unwanted movements and spasticity are inhibited and normal patterns are facilitated under the assumption that regaining voluntary control over key movements will transfer to functional improvement. However, empirical evidence for this assumption is lacking. More recently, the rehabilitation of reaching has been based on a task-oriented approach in which movement is behaviorally driven and the interaction of the individual with the environment is stressed.11,12 This approach may tolerate or even encourage compensatory involvement of other degrees of freedom to move the hand closer to the object.13 It has recently been suggested, however, that the presence of excessive trunk movement in hemiparetic individuals while reaching may limit the potential recovery of normal arm movement patterns.14,15 Reducing compensatory mechanisms by limiting trunk displacement may encourage the return of movement patterns typically seen in healthy individuals. To date, the effectiveness of this type of "restraint therapy" on arm motor recovery in chronic hemiparetic patients has not been assessed.
As a first step in the process of determining the clinical efficacy of restraint therapy, we evaluated the effects of limiting compensatory trunk movement on the recovery of arm interjoint coordination during reaching to targets placed within arms reach in hemiparetic patients. A reach-to-grasp instead of a pointing task was used to evaluate the efficacy of the treatment approach for the retraining of a functionally relevant movement. Preliminary data have been presented in abstract form.16
| Subjects and Methods |
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Clinical Evaluation
Before data collection, all patients underwent a series of clinical tests administered by an experienced physiotherapist that evaluated balance and the status of their affected arm. Upper extremity impairment was evaluated with the arm section of the Fugl-Meyer Scale17 for voluntary movements made into and out of abnormal movement synergies as well as pain and sensation of the arm. The scale ranges from 0 to 66, with scores >65 reflecting normal movement. In our patients, Fugl-Meyer scores ranged from 19, indicating severe motor impairment, to 65, reflecting almost no impairment. Spasticity of elbow flexors was determined by the valid and reliable Composite Spasticity Index.1820 This index sums measures on 3 scales: (1) biceps brachii tendon jerks evoked with a reflex hammer; (2) resistance to stretch of passive elbow flexors at moderate speed (modified Ashworth Scale21); and (3) wrist clonus, for a total possible score of 16. Spasticity in our patients ranged from 2 (mild) to 10 (moderately severe). Finally, sitting and standing balance was measured on the Berg Balance Scale,22 having a total of 56 points in which function is scored as poor (0 to 20) to good (40 to 56). All patients scored higher than 44 (mean 50.8±4.6) on this scale, indicating that they had little problem with balance (Table 1).
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Reaching Task
Participants were seated on a chair and reached forward to grasp a cone (7-cm diameter base, 17.5 cm high) placed in the sagittal plane in the trunk midline (Figure 1). Because seat height and extent of thigh and foot support may affect reaching distance,23 seat height was adjusted to 100% of lower leg length, which was measured from the lateral knee joint line to the floor with the participant standing. In addition,
75% of the thigh was supported on the chair, and the feet made full floor contact. The cone was placed at midsternal height at 2 different distances (targets) defined in terms of the participants arm length (T1, one-half arms length; T2, arms length). Arms length was measured from the medial border of the axilla to the distal wrist crease. The targets were placed so that biomechanically, only arm movement was required to grasp and retrieve the cone. Initial hand position was directly in front of the lower third of the sternum, the thumb 5 cm in front of the sternum, and the elbow close to the side of the body. With full vision, participants reached toward, grasped, and returned the cone to the midchest region at a comfortable self-paced speed (trunk-free condition). Reaches to T1 and T2 were then repeated with the trunk secured to the chair back with a harness minimizing shoulder girdle movement and preventing trunk flexion and rotation (trunk-fixed condition). Twenty trials were recorded for each target distance and condition, and testing order of the 4 blocks was randomized.
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Movement kinematics (sampling frequency, 100 Hz) were recorded with 10 infrared lightemitting diodes placed on the tips or interphalangeal joints of the index and thumb, the wrist ulnar styloid process, the lateral humeral epicondyle, bilateral acromion processes, 2 points along the vertical axis of the sternum, the hip (anterior superior iliac spine), and the anterior knee above the patella. Data from sternal, hip, and knee markers were monitored to ensure that participants did not slide forward on the chair to extend their reach during the task. Data were collected for 2 to 6.5 seconds, with the use of an Optotrak Motion Analysis System (Northern Digital, model 3010).
Data Analysis
Data analysis focused on 4 types of movement variables: end point and trunk trajectories, tangential velocities, maximal joint and trunk excursions, and interjoint coordination.
From filtered (low-pass cutoff, 20 Hz) position data, 2- and 3-dimensional trajectories were plotted. Tangential velocity profiles of the end point and trunk were computed from the magnitude of the velocity vector, using time derivatives of x, y, and z positional data for markers placed on the fingertip and sternum, respectively. Although the task involved reaching, grasping, and returning the cone to the body, only the transport component of the hand to the target was analyzed. The requirement to grasp and retrieve the cone was used so that participants would make natural goal-directed movements.13,24 Trajectory smoothness was determined by the index of curvature (ratio of actual end point path length to that of a straight line joining initial and final positions). This index has been found to better characterize trajectories than area measurements.25 Thus, a straight line has an index of 1, whereas that of a semicircle has an index of 1.57. To quantify the temporal segmentation of the trajectory, the number of movement units in the tangential velocity was summed for each target and movement condition. A movement unit was defined as a maximum in the tangential velocity trace preceded by increasing values for at least 20 ms and followed by decreasing values for at least 20 ms.26
Movement times and peak velocities were determined from tangential velocity traces. Movement times were defined as differences between movement onsets and offsets, determined for each trial as the times at which the tangential velocity rose above or fell and remained below 10% of the peak tangential velocity of the end point and trunk, respectively.
To determine changes in joint ranges and to analyze spatial and temporal interjoint coordination patterns, vectors joining the appropriate infrared lightemitting diodes were used to compute, using vector algebra, shoulder (2 df=flexion/extension and horizontal abduction/adduction) and elbow (1 df=flexion/extension) angles. In addition, trunk flexion was measured in millimeters from the sagittal displacement of the sternal marker. Sagittal trunk displacement was expressed as a percentage of end point path length to account for arm length differences between participants.
Interjoint coordination patterns between shoulder and elbow movements were determined. First, angle/angle diagrams between shoulder horizontal adduction/abduction and elbow flexion/extension as well as between shoulder and elbow flexion/extension were averaged and plotted for each individual in each condition. The relation between angular displacements was determined by linear regression in which the slope and cross-correlation were calculated.
Statistical Analysis
We tested the hypotheses that reducing or arresting compensatory movements would increase the arm joint excursions and improve patterns of interjoint coordination. We compared maximal joint excursions of 3 df for movements made to T1 and T2 with and without trunk restraint with 2-factor (group, condition) ANOVAs and appropriate post hoc tests (Tukey honestly significant difference tests). If trunk restraint leads to changes in joint excursions, improvements would be identified when range of motion values approach mean values recorded in healthy individuals performing the same task. Within-group comparisons were made with paired Students t tests. Consistency of specific variables was estimated with the coefficient of variability, defined as the ratio between the standard deviation and the mean times 100. Parametric statistics were used for comparisons between groups when requirements for homogeneity of variance were met. A significance level of P<0.05 was used for all tests.
| Results |
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The mean arm curvature was significantly higher for T1 (1.54±0.13) than for T2 (1.20±0.12; Students t test, P<0.001; Figure 3), suggesting that healthy individuals used a more curved trajectory to grasp the target closer to the body. The group coefficient of variability was <10% for both T1 (8.4%) and T2 (9.7%).
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Healthy individuals used minimal trunk displacement to reach either target, which was not surprising because both were placed within arms reach. For the group, mean trunk displacement was negligible for T1 and 5.5±3.5% of target distance for T2. The high variability for T2 was a result of the data of the oldest individual (80 years of age), whose trunk movement contributed 14.8% of target distance. For the other 10 participants, excluding this individual, the variability was much smaller (±1.7%).
Since T2 was placed in line with T1, individuals used virtually the same interjoint coordination pattern for reaches to both targets except that the total angular displacements were greater for T2. This was reflected in a near superposition of patterns in most individuals. A typical example of the elbow-shoulder interjoint coordination pattern for one healthy individual reaching to T2 is shown in Figure 4 (top left).
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Effects of Trunk Restraint in Healthy Individuals
Trunk restraint had little effect on tangential velocity, end point trajectories, and interjoint coordination patterns (Figure 5) in healthy individuals. For example, the peak tangential velocity for T2 decreased from 1409.3 mm/s to 1351.5 mm/s when the trunk was restrained (Table 2). Trajectory profiles and patterns from trials in which trunk movement was blocked were virtually indistinguishable from those in which the trunk was free (Figure 2, top left). The number of peaks in the tangential velocity profiles was not affected by trunk restraint. For example, for T2, this number decreased from 2.3 (±0.5) to 2.1 (±0.4) peaks (Table 2). Nevertheless, restriction of the trunk movement was associated with a significant increase in elbow extension in 6 of 11 and 9 of 11 healthy individuals for T1 and T2, respectively (Figure 6). For T2, the mean elbow extension significantly increased
8° (paired t test, P<0.05) and mean shoulder horizontal adduction increased
5° (paired t test P<0.001), whereas there was no change in shoulder flexion with trunk restraint (Table 2).
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Analysis of the slopes of the shoulder/elbow angle/angle diagrams was made for restrained and unrestrained reaches to T2 only. Higher slopes indicate relatively more shoulder horizontal adduction compared with elbow extension, whereas lower slopes indicate the inverse. Slopes were highly variable in healthy individuals, ranging from 0.372 to 2.068 (0.903±0.452) when trunk motion was unrestrained and from 0.456 to 1.065 (0.769±0.223) when the trunk was restrained. This difference was nonsignificant. Despite the large range in slopes, the correlations between shoulder and elbow movements for both conditions were >0.94 (P<0.0001; Table 2).
Kinematics of Unrestrained Reaching in Stroke Patients
Hemiparetic patients made slower arm movements than did healthy individuals. Mean peak tangential velocities (Table 2) for free movements to T1 and T2 corresponded to 75% and 78%, respectively, of those in healthy individuals.
Arm and trunk trajectories were less smooth in hemiparetic compared with healthy individuals (Figure 2). All patients were able to reach toward and grasp the cone. However, end point trajectories tended to be more hook-shaped, as shown for S6 and S11 in Figure 2. One exception was S1, who used more wrist extension for grasping, and, consequently, his hand paths were straighter. As in healthy individuals, the mean arm curvature was significantly higher (P<0.05) for T1 (1.80±0.52, coefficient of variability=27.8%) than T2 (1.34±0.22, coefficient of variability=16.4%, Figure 3). In addition, when compared with healthy individuals, both indexes of curvature were also significantly higher and more variable. Finally, there were a significantly larger number of peaks in the tangential velocity profiles for movements to both targets (4.2±2.0 for T1 and 4.3±2.3 for T2).
Hemiparetic patients used considerably more trunk recruitment to move the hand to the target than did healthy individuals. Compared with negligible trunk recruitment in healthy individuals reaching to T1, hemiparetic patients used between 3.0 and 179.6 mm of trunk movement (mean, 51.2±56.7 mm). For T2, the mean trunk displacement for hemiparetic patients was 124.8±95.1 mm compared with 25.8±14.9 mm for healthy individuals (P<0.001), representing a mean of 24.5% of the target distance (Table 1 and Figure 2, bottom right). The amount of trunk displacement used for reaching was significantly correlated with clinical stroke severity (r=-0.91), so that the more severe the clinical syndrome (lower Fugl-Meyer score), the greater the trunk displacement. Interestingly, there was also a significant negative correlation between the amount of trunk displacement and the coefficient of correlation between elbow and shoulder movement (r=-0.96). This indicated that those individuals who used the most trunk displacement had the most disrupted coupling (dyscoordination) between arm joint movements.
The degree of clinical stroke severity was also related to angular displacement. Individuals with the mildest symptoms used the most elbow and shoulder movement for reaching (Figure 6). However, for T2, the overall amount of elbow extension was
16° less in hemiparetic compared with healthy individuals (P<0.05, Table 2). Similarly, the mean amounts of shoulder flexion and horizontal adduction were significantly less in hemiparetic patients for movements to both targets (
7° to 8° and 22° to 23° less for T1 and T2, respectively, P<0.001, Table 2).
Effects of Trunk Restraint in Hemiparetic Patients
In contrast to healthy individuals, trunk restraint resulted in a decrease in movement speed to both targets in hemiparetic patients. This was significant for T2, for which peak tangential velocity decreased to 831.2±494.8 mm/s (P<0.05). For patients with mild to moderate stroke, restraining the trunk had no significant effect on curvature or arm trajectory variability for either target (Figure 2) or on the number of peaks (Table 2). However, in more severely affected individuals (S9 to S12), trunk restraint led to a decrease in the total end point displacement. In other words, for these individuals, limiting trunk movement made it more difficult for the hand to reach the target. At the same time, the most striking effect of trunk restraint was the increase in elbow and shoulder joint ranges for all individuals. Elbow extension increased on average 4° (paired t test, P<0.001) for T1 and 14° (paired t test, P<0.001) for T2 (Table 2 and Figure 6). Shoulder flexion increased 14° for T1 and 11° for T2 (P<0.001). For shoulder horizontal adduction, although group effects were not significant, trunk fixation resulted in increases of >5° in 6 of 11 individuals for T1 and in 4 of 11 individuals for T2 (Figure 6).
In contrast to healthy individuals, trunk restraint significantly altered the pattern of interjoint coordination, an effect that was most evident in clinically severe patients (Figure 5). The slope of the shoulder/elbow relationships significantly changed in 4 of 7 mild-to-moderate and 4 of 4 severe patients. In addition, when the trunk was restrained, correlations significantly increased in the 4 severe patients who had poor shoulder/elbow correlations when reaches were made without trunk restraint (Figure 7).
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| Discussion |
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Despite the relative preservation of end point trajectories, interjoint coordination was severely disrupted in most patients (see Figures 2 and 4, S11). This underscores the need for therapists to assess not only the capacity of patients to perform activities of daily living with the affected arm but, more importantly, to evaluate key components of limb control associated with movement quality.31 In particular, with respect to reaching and manipulating objects with the hemiparetic arm, assessment should focus on the amount of compensatory trunk and shoulder girdle movements as well as the range of active joint movement used. This type of analytical approach is not possible with the use of functional outcome scales such as the Barthel Index32 or the Frenchay Arm Test33 that mainly assess the level of independence for task completion. A need exists for the development of scales to allow clinicians to isolate and quantify such key task components. Bernhardt et al34 have described an assessment of an object manipulation task in hemiparetic patients that is based on observational analysis of movement speed, trajectory jerkiness, and path indirectness. They compared therapists ratings of videotapes of patients performing the task to criterion measures analyzed with an instrumented motion analysis system. Moderate to highly accurate judgments by therapists on these 3 parameters were reported. Compensatory movements, however, were not assessed. Recently, a new scale has been proposed that focuses on movement quality, which includes compensatory movement in well-defined functional tasks, including reaching.35 Quality of movement information derived from these types of scales may complement functionality information from other assessment tools and help therapists design more effective treatment programs for hemiparetic patients.
Effect of Trunk Restriction on the Increase of Arm Range of Motion
The effects of trunk restraint indicate that hemiparetic patients did not use their potential joint range for free arm movements. A likely explanation stems from recent findings of Levin et al.36 They defined articular ranges in which hemiparetic patients could make isolated elbow flexion and extension movements by using a reciprocal muscle activation pattern. The angular range was correlated with the motor deficit such that the most severely affected patients could only make isolated elbow movements in midrange. With further encouragement, movement beyond the defined ranges was possible, but this required more effort and was accompanied by a pattern of excessive agonist/antagonist coactivation. For elbow extension, the excessive coactivation occurred when patients attempted to extend the elbow beyond the angular position defined by the static stretch reflex threshold for the antagonist elbow flexors. If these findings at a single joint may be extended to the multijoint reaching task, it may be postulated that restriction of trunk movement enabled patients to extend their reach by using the joint range characterized by coactivation. The additional energy cost of using more elbow extension probably was avoided by hemiparetic individuals when reaching without trunk restraint. Indeed, evidence from studies in healthy individuals suggests that minimization of metabolic energy costs may govern the selection of muscle activation patterns, movement trajectories, and interjoint coordination by the central nervous system.37 A better understanding of the mechanisms underlying the increases in elbow and shoulder motion may be gained by an electromyographic analysis of muscle activation patterns during restrained and unrestrained reaching.
Effect of Trunk Restriction on Arm Reaching Patterns
Trunk restraint decreases the number of joints involved in reaching because it blocks shoulder girdle and trunk movements naturally accompanying arm movements. Indeed, scapular movement contributes
60° to both shoulder flexion and abduction.38 However, the task still involved a redundant number of degrees of freedom (3 for the glenohumeral joint, 2 for elbow, 2 for wrist) to position and orient the hand in space for reaching. Thus it did not reduce the movement to a 2-dimensional task.
The increase in joint ranges with trunk restraint may be partly due to an adaptation involving anticipation of changed external load conditions. Indeed, in healthy individuals, adaptation to perturbation of single joint movement may occur within one trial,39 and preliminary results indicated that this type of adaptation may also occur in mild to moderately affected hemiparetic patients.40 Another possibility is that the adaptation was triggered by somatosensory input from the trunk or shoulder caused by the trunk restraint.41 Adamovich et al41 demonstrated that unexpected trunk perturbations did not affect hand trajectories for reaches made within the workspace. Similarly, we found that healthy individuals preserved arm trajectories marked by smooth interjoint coordination despite the change in the ranges of motion when the trunk was restrained. A similar adaptation may have occurred in hemiparetic patients. The finding that trunk restraint led to an increase in active angular range in hemiparetic patients suggests that they may have retained the ability to adapt their motor commands to new external conditions. An explanation of this adaptability seems necessary. To begin with, it is well documented that hemiparetic patients use abnormal interjoint synergies to accomplish arm movement.9,42,43 The arm extension synergy is characterized by scapular elevation and protraction together with shoulder extension, adduction and internal rotation, elbow extension, and wrist flexion. Limiting components of this synergy (scapular protraction and elevation) may encourage the recovery of combined shoulder flexion and elbow extension. In other words, patients are forced to make movements "out of synergy," which probably involves a focused and greater effort on their part. Interestingly, requiring patients to make this additional effort may indeed be effective in increasing active joint range as well as improving interjoint coordination. The finding that reaching movements using increased angular ranges obtained by this method are made in a more coordinated way is indeed surprising. It suggests that underlying "normal" patterns of movement coordination are not entirely lost after stroke and that appropriate treatments may be applied to uncover them to maximize function. One cost of this recovery may be a short-term decrease in movement speed.
Knowledge of the capacity of stroke patients to recover lost movement elements is essential to the resolution of the debate concerning the degree to which therapy should emphasize the recovery of normal versus the teaching of compensatory strategies for reaching. Traditionally, the choice between rehabilitation strategies has been based on the phase of stroke recovery. Thus, in the acute phase, therapy focuses on the prevention of maladaptive compensatory strategies while promoting the recovery of normal function. In the chronic phase, the emphasis is placed on maximizing function, often through the teaching of compensatory strategies.31 Our observation that some recovery of normal reaching patterns could occur in patients with chronic stroke suggests that such a clear division between treatment approaches may not be justified.
A limitation of this study is that the longer-term effects of trunk-restraint therapy were not investigated. The results of a recent literature review indicate that recovery in hemiparetic patients may occur when interventions involve repetitive training and stimulate the active participation of the patient.44 However, improvements in patients with moderate to severe clinical syndromes may be associated with increased trunk displacement when unrestrained pointing movements are practiced.45 This suggests that in some cases, repetitive training or unrestrained reaching may reinforce undesirable compensatory strategies. It remains to be demonstrated that the use of trunk restraint as a treatment paradigm aimed at decreasing compensatory strategies has the potential of becoming an effective therapy. Further studies are necessary to determine if the improvement may outlast the period of training.
| Acknowledgments |
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Received October 3, 2000; revision received April 26, 2001; accepted May 25, 2001.
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